Attachment and the regulationof the right brain

ALLAN N SCH ORE

ABSTRACT It has been three decades since John Bowlby rst presented anover-arching model of early human development in his groundbreakingvolume Attachment In the present paper I refer back to Bowlbyrsquos originalcharting of the attachment landscape in order to suggest that current researchand clinical models need to return to the integration of the psychological andbiological underpinnings of the theory Towards that end recent contributionsfrom neuroscience are offered to support Bowlbyrsquos assertions that attachmentis instinctive behavior with a biological function that emotional processes lieat the foundation of a model of instinctive behavior and that a biologicalcontrol system in the brain regulates affectively driven instinctive behaviorThis control system can now be identied as the orbitofrontal system and itscortical and subcortical connections This lsquosenior executive of the emotionalbrainrsquo acts as a regulatory system and is expanded in the right hemispherewhich is dominant in human infancy and centrally involved in inhibitorycontrol

Attachment theory is essentially a regulatory theory and attachment can bedened as the interactive regulation of biological synchronicity betweenorganisms This model suggests that future directions of attachment researchshould focus upon the early-forming psychoneurobiological mechanisms thatmediate both adaptive and maladaptive regulatory processes Such studies willhave direct applications to the creation of more effective preventive andtreatment methodologies

KEYWORDS affective processes ndash attachment theory ndash orbitofrontal system ndashpsychobiological regulation ndash right hemisphere

In 1969 which was 29 years after his initial publication of an article in theInternational Journal of Psycho-Analysis on how the early environmentcould in uence the development of character (1940) John Bowlby integratedhis career-spanning observations and theoretical conceptualizations into therst of three inuential books on Attachment and loss This foundationalvolume Attachment was groundbreaking for a number of reasons It focusedupon one of the major questions of science specically how and why docertain early ontogenetic events have such an inordinate effect on everything

Attachment amp Human Development Vol 2 No 1 April 2000 23ndash47

Correspondence to Allan N Schore 9817 Sylvia Avenue Northridge CA 91324 USAAn abbreviated version of this article appeared as a Foreword to Basic Bookrsquos reprinting ofJohn Bowlbyrsquos classic volume Attachment

Attachment amp Human Development ISSN 1461-6734 print1469-2988 online copy 2000 Taylor amp Francis Ltdhttpwwwtandfcoukjournals

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 124

that follows Bowlbyrsquos scientically-informed curiosity about this questionenvisioned the center stage of human infancy on which is played the rstchapter of the human drama to be a context in which a mother and her infantexperience connections and disconnections of their vital emotional com-munications Bowlby presented his model in such a way that both a heuris-tic theoretical perspective and a testable experimental methodology could becreated to observe measure and evaluate certain very specic mechanismsby which the early social environment interacts with the maturing organismin order to shape developmental processes (Schore 2000)

But perhaps of even more profound signi cance was his carefully arguedproposition that an interdisciplinary perspective should be applied to thestudy of developmental phenomena as they exist in nature In such anapproach the collaborative knowledge-bases of a spectrum of sciences wouldyield the most powerful models of both the nature of the fundamental onto-genetic processes that mediate the infantrsquos rst attachment to another humanbeing and the essential psychobiological mechanisms by which these pro-cesses indelibly inuence the development of the organism at later points ofthe life-cycle

In response to this classic volume Ainsworth observed that lsquoIn effectwhat Bowlby has attempted is to update psychoanalytic theory in the lightof recent advances in biologyrsquo (1967 p 998) Bowlbyrsquos deep insights intothe potential synergistic effects of combining the literatures of whatappeared on the surface to be distantly related realms may now seem like abrilliant flash of intuition In actuality it represented a natural convergenceof his two most important intellectual influences Charles Darwin andSigmund Freud In order to create a perspective that could describe criticalevents both in the external and in the internal world concepts from bothethology (behavioral biology) and psychoanalysis are presented and inter-woven throughout the volume In essence a central goal of Bowlbyrsquos firstbook is to demonstrate that a mutually enriching dialogue can be organizedbetween the biological and the psychological realms something attemptedby Darwin (1872) in the first scientific treatise on the biology and psy-chology of emotion The Expression of Emotions in Man and Animals andby Freud (1895) in his endeavor to integrate neurobiology and psychologyin order to create a lsquonatural sciencersquo Project for a Scientific Psychology(Schore 1997a)

Although both Darwin and Freud emphasized the centrality of earlydevelopment as an important part of their overall work each primarilyfocused his observational and theoretical lens on the adaptive and maladap-tive functioning of fully matured adult organisms In the Attachment volumeBowlby (1969) argues that clinical observers and experimental scientistsshould intensively focus on the developing organisms that are in the processof maturing More specically he calls for deeper explorations of the funda-mental ontogenetic mechanisms by which an immature organism is criticallyshaped by its primordial relationship with a mature adult member of its

species that is more extensive studies of how an attachment bond formsbetween the infant and the mother In this conception Bowlby asserts thatthese developmental processes are the product of the interaction of a uniquegenetic endowment with a particular environment and that the infantrsquosemerging social psychological and biological capacities cannot be under-stood apart from its relationship with the mother

BOWLBYrsquoS ORIGINAL CHARTINGS OF THEATTACHM EN T LANDSCAPE

Much has transpired since the original publication of Bowlbyrsquos Attachmentand the ensuing explosion of attachment research over the last quarter of acentury is a testament to the power of the concepts it contains And yet a (re-) reading of this classic still continues to reveal more and more subtleinsights into the nature of developmental processes and to shine light uponyet to be fully explored areas of developmental research In fact in thisseminal work of developmental science the pioneering Bowlby presents asurvey of what he sees to be the essential topographic landmarks of theuncharted territory of motherndashinfant relationally driven psychobiologicalprocesses The essential guideposts of this dynamic domain ndash the centralphenomena that must be considered in any overarching model of how theattachment relationship generates both immediate and long-enduring effectson the developing individual ndash are presented by Bowlby in not only thesubject-matter but also the structural organization of the book The readerwill notice that the book is divided into four parts lsquoThe taskrsquo lsquoInstinctivebehaviourrsquo lsquoAttachment behaviourrsquo and lsquoOntogeny of human attachmentrsquoand that Bowlby devotes ten chapters to the rst two parts and seven to thelast two parts

It is now more than 30 years since Bowlbyrsquos call for lsquoa far-reaching pro-gramme of research into the social responses of man from the preverbalperiod of infancy onwardsrsquo (p 174) In the following I want to briey offerfrom a psychoneurobiological perspective not only my views of the originalcontents of Bowlbyrsquos guidebook but also some thoughts about the currentand future directions of the experimental and clinical explorations of attach-ment theory as they pass from one century into the next In doing so I willspecically attend to not so much the quality of attachment research whichhas served as a standard in psychology psychiatry and psychoanalysis as awhole or to the breadth of the research which spans developmental psy-chology developmental psychobiology developmental neurochemistryinfant psychiatry and psychoanalysis but rather to the foci of currentinvestigations as measured against the original prescriptions that are offeredhere by Bowlby And I will suggest that certain uninvestigated areas of thisattachment domain sketched out in Bowlbyrsquos cartographic descriptions inthis book are now ready to be explored by interdisciplinary research

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 25

programs For a broad overview of the eld at the end of century I refer thereader to two excellent edited volumes Attachment theory Social develop-mental and clinical perspectives (Goldberg Muir amp Kerr 1995) and Hand-book of attachment Theory research and clinical applications (Cassidy ampShaver 1999)

In the book most current readers are very familiar (or even perhaps onlyfamiliar) with the latter two sections on attachment and most researcherscontinue to focus their investigation upon the concepts outlined in these laterchapters It is here as well as in the introductory sections that Bowlby pre-sents his essential contributions on the infantrsquos sequential responses to separ-ation from the primary attachment gure ndash protest despair and detachmentIn the context of emphasizing the importance of studying the infantrsquos behav-ior specically during the temporal interval when the mother returnsBowlby introduces the recent methodology of Ainsworth which will soonbecome the major experimental paradigm for attachment research the incre-mentally stress-increasing lsquostrange situationrsquo

But in addition to theorizing on the nature of separation responses stress-ful ruptures of the motherndashinfant bond Bowlby also describes what he seesas the fundamental dynamics of the attachment relationship In stating thatthe infant is active in seeking interaction that the motherrsquos maternal behav-ior is lsquoreciprocalrsquo to the infantrsquos attachment behavior and that the develop-ment of attachment is related both to the sensitivity of the mother inresponding to her babyrsquos cues and to the amount and nature of their inter-action he lays a groundwork that presents attachment dynamics as a lsquorecip-rocal interchangersquo (p 346) a conceptualization that is perfectly compatiblewith recent advances in dynamic systems theory (Schore 1997b in press aLewis 1995 1999 in press)

At the very beginning of the section on lsquoAttachment behaviorrsquo Bowlbyoffers his earliest model of the essential characteristics of attachment ndash it isinstinctive social behavior with a biological function lsquoreadily activatedespecially by the motherrsquos departure or by anything frightening and thestimuli that most ef ciently terminate the systems are sound sight or touchof the motherrsquo and is lsquoa product of the activity of a number of behaviouralsystems that have proximity to mother as a predictable outcomersquo (p 179)Although the rst three postulates remained unaltered in his later writingsin his second volume Bowlby (1973) attempted to dene more precisely theset-goal of the attachment system as seeking not just proximity but access toan attachment gure who is emotionally available and responsive

A further evolution of this concept is now found in transactional theoriesthat emphasize the central role of the primary caregiver in co-regulatingthe childrsquos facially expressed emotional states (Schore 1994 1998a in pressb) and that de ne attachment as the dyadic regulation of emotion (Sroufe1996) and the regulation of biological synchronicity between organisms(Wang 1997) The development of synchronized interactions is fundamentalto the healthy affective development of the infant (Penman Meares amp

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 126

Milgrom-Friedman 1983) Reite and Capitanio (1985) conceptualize affect aslsquoa manifestation of underlying modulating or motivational systems subserv-ing or facilitating social attachmentsrsquo (p 248) and suggest that an essentialattachment function is lsquoto promote the synchrony or regulation of biologicaland behavioral systems on an organismic levelrsquo (p 235) In these rapid regu-lated face-to-face transactions the psychobiologically attuned (Field 1985)caregiver not only minimizes the infantrsquos negative but also maximizes its posi-tive affective states (Schore 1994 1996 1998b) This proximate interpersonalcontext of lsquoaffect synchronyrsquo (Feldman Greenbaum amp Yirmiya 1999) andinterpersonal resonance (Schore 1997b in press b) represents the externalrealm of attachment dynamics

But due to his interests in the inner world Bowlby here presents a modelof events occurring within the internal realm of attachment processes Andso he offers his initial speculations about how the developing child constructsinternal working models lsquoof how the physical world may be expected tobehave how his mother and other signicant persons may be expected tobehave how he himself may be expected to behave and how each interactswith the otherrsquo (p 354) This initial concept has currently evolved intolsquoprocess-orientedrsquo conceptions of internal working models as representationsthat regulate an individualrsquos relationship adaptation through interpre-tiveattributional processes (Bretherton amp Munholland 1999) and encodestrategies of affect regulation (Kobak amp Sceery 1988 Schore 1994) Currentpsychobiological models refer to representations of the infantrsquos affective dia-logue with the mother which can be accessed to regulate its affective state(Polan amp Hofer 1999)

Interestingly Bowlby also describes internal working models in the rstpart of the volume the eight chapters devoted to lsquoinstinctive behaviorrsquo Irepeat my assertion that a deeper explication of the fundamental themes ofthis section of the book represents the frontier of attachment theory andresearch In these opening chapters the aggregate of which represents thefoundation on which the later chapters on attachment are built Bowlbyposits that internal models function as lsquocognitive mapsrsquo in the brain and areaccessed lsquoto transmit store and manipulate information that helps makingpredictions as to how set-goals (of attachment) can be achievedrsquo (p 80)Furthermore he states that lsquothe two working models each individual musthave are referred to respectively as his environmental model and his organ-ismic modelrsquo (p 82) This is because lsquosensory data regarding events reachingan organism via its sense organs are immediately assessed regulated andinterpreted The same is true of sensory data derived from the internal stateof the organismrsquo (p 109) Here Bowlby is pointing to the need for a develop-mental theoretical conception of attachment that can tie together psychologyand biology mind and body

And so at the very onset of his essay he begins lsquoThe taskrsquo by describinga theoretical landscape that includes both the biological and social aspectsof attachment a terrain that must be described in terms of its structural

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 27

organization as well as its functional properties Following the generalperspective of all biological investigators he attempts to elucidate thestructurendashfunction relationships of a living system but with the added per-spective of developmental biology he is specically focusing on the early criti-cal stages within which the system rst self-organizes Thus the form of thebook is rst to outline the general characteristics of the internal structuralsystem and then to describe this systemrsquos central functional role in attachmentprocesses

Bowlby begins the third chapter by quoting Freudrsquos (1925) dictum thatlsquoThere is no more urgent need in psychology than for a securely foundedtheory of the instinctsrsquo The attempt to do so in this book an offering of anlsquoalternative model of instinctive behaviorrsquo in essence represents Bowlbyrsquosconviction that what Freud was calling for was the creation of a model thatcould explicate the biology of unconscious processes Towards that end inthe rst of eight chapters on the topic he proposes that attachment is instinc-tive behavior associated with self-preservation and that it is a product of theinteraction between genetic endowment and the early environment

But immediately after a brief 5-page introduction Bowlby launches into adetailed description of a biological control system that is centrally involvedin instinctive behavior This control system is structured as a hierarchicalmode of organization that acts as lsquoan overall goal-corrected behavioral struc-turersquo Bowlby also gives some hints as to the neurobiological operations ofthis control system ndash its functions must be associated with the organismrsquoslsquostate of arousalrsquo that results from the critical operations of the reticular for-mation and with lsquothe appraisal of organismic states and situations of the mid-brain nuclei and limbic systemrsquo (p 110) He even offers a speculation aboutits anatomical location ndash the prefrontal lobes (p 156)

This control system he says is lsquoopen in some degree to inuence by theenvironment in which development occursrsquo (p 45) More specically itevolves in the infantrsquos interaction with an lsquoenvironment of adaptiveness andespecially of his interaction with the principal gure in that environmentnamely his motherrsquo (p 180) Furthermore Bowlby speculates that thelsquoupgrading of control during individual development from simple to moresophisticated is no doubt in large part a result of the growth of the centralnervous systemrsquo (p 156) In fact he even goes so far as to suggest the tem-poral interval that is critical to the maturation of this control system ndash 9 to18 months (p 180)

In a subsequent chapter on lsquoAppraising and selecting Feeling andemotionrsquo Bowlby quotes Darwinrsquos (1872) observation that the movementsof expression in the face and body serve as the rst means of communicationbetween the mother and the infant Furthering this theme on the communi-cative role of feeling and emotion Bowlby emphasizes the salience of lsquofacialexpression posture tone of voice physiological changes tempo of move-ment and incipient actionrsquo (p 120) The appraisal of this input is experiencedlsquoin terms of value as pleasant or unpleasantrsquo (pp 111ndash112) and the

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 128

movements lsquomay be actively at work even when we are not aware of themrsquo(p 110) in this manner feeling provides a monitoring of both the behavioraland physiological state (p 121) Emotional processes thus he says lie at thefoundation of a model of instinctive behavior

In following chapters Bowlby concludes that the motherndashinfant attach-ment relation is lsquoaccompanied by the strongest of feelings and emotionshappy or the reversersquo (p 242) that the infantrsquos lsquocapacity to cope with stressrsquois correlated with certain maternal behaviors (p 344) and that the instinctivebehavior that emerges from the co-constructed environment of evolutionaryadaptiveness has consequences that are lsquovital to the survival of the speciesrsquo (p 137) He also suggests that the attachment system is readily activated untilthe end of the third year when the childrsquos capacity to cope with maternalseparation lsquoabruptlyrsquo improves due to the fact that lsquosome maturationalthreshold is passedrsquo (p 205)

CONTRIBUTIONS FROM NEUROSCIENCE TOATTACHM ENT THEORY

So the next question is 30 years after the appearance of this volume at theend of the lsquodecade of the brainrsquo how do Bowlbyrsquos original chartings of theattachment domain hold up In a word they were indeed prescient In facthis overall birdrsquos-eye perspective of the internal attachment landscape was socomprehensive that we now need to zoom in not just for close-up views ofthe essential brain structures that mediate attachment processes but also forvisualizations of how these structures dynamically self-organize within thedeveloping brain This includes neurobiological studies of Bowlbyrsquos controlsystem which I suggest may now be identied with the orbitofrontal cortexan area that has been called the lsquosenior executive of the emotional brainrsquo(Joseph 1996) and that has been shown to mediate lsquothe highest level ofcontrol of behavior especially in relation to emotionrsquo (Price Carmichael ampDrevets 1996 p 523) Keeping in mind Bowlbyrsquos previously presentedtheoretical descriptions the following is an extremely brief overview of agrowing body of studies on the neurobiology of attachment (For moreextensive expositions of these concepts and references see Schore 1994 19961997b 1998a 1999 in press a b c d e in preparation)

According to Ainsworth (1967 p 429) attachment is more than overtbehavior it is internal lsquobeing built into the nervous system in the course andas a result of the infantrsquos experience of his transactions with the motherrsquoFollowing Bowlbyrsquos suggestion the limbic system has been suggested to bethe site of developmental changes associated with the rise of attachmentbehaviors (Anders amp Zeanah 1984) Indeed the specic period from 7 to 15months has been shown to be critical for the myelination and therefore thematuration of particular rapidly developing limbic and cortical associationareas (Kinney Brody Kloman amp Gilles 1988) and limbic areas of the human

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 29

cerebral cortex show anatomical maturation at 15 months (Rabinowicz1979) In a number of works I offer evidence to show that attachment experi-ences face-to-face transactions of affect synchrony between caregiver andinfant directly inuence the imprinting the circuit wiring of the orbitalprefrontal cortex a corticolimbic area that is known to begin a major matu-rational change at 10 to 12 months and to complete a critical period of growthfrom the middle to the end of the second year This time-frame is identical toBowlbyrsquos maturation of an attachment control system that is open to in u-ence from the developmental environment

The co-created environment of evolutionary adaptiveness is thus isomor-phic to a growth-facilitating environment for the experience-dependent mat-uration of a regulatory system in the orbitofrontal cortex Indeed thisprefrontal system appraises visual facial information (Scalaidhe Wilson ampGoldman-Rakic 1997) and processes responses to pleasant touch tastesmell (Francis D et al 1999) and music (Blood Zatorre Bermudez ampEvans 1999) as well as to unpleasant images of angry and sad faces (BlairMorris Frith Perrett amp Dolan 1999) But this system is also involved in theregulation of the body state and reects changes taking place in that state(Luria 1980)

This frontolimbic system provides a high-level coding that exibly co-ordinates exteroceptive and interoceptive domains and functions to correctresponses as conditions change (Derryberry amp Tucker 1992) processes feed-back information (Elliott Frith amp Dolan 1997) and thereby monitorsadjusts and corrects emotional responses (Rolls 1986) and modulates themotivational control of goal-directed behavior (Tremblay amp Schultz 1999)So after a rapid evaluation of an environmental stimulus the orbitofrontalsystem monitors feedback about the current internal state in order to makeassessments of coping resources and it updates appropriate response outputsin order to make adaptive adjustments to particular environmental perturba-tions (Schore 1998a) In this manner lsquothe integrity of the orbitofrontal cortexis necessary for acquiring very specic forms of knowledge for regulatinginterpersonal behaviorrsquo (Dolan 1999 p 928)

These functions reect the unique anatomical properties of this area of thebrain Due to its location at the ventral and medial hemispheric surfaces itacts as a convergence zone where cortex and subcortex meet It is thus situ-ated at the apogee of the lsquorostral limbic systemrsquo a hierarchical sequence ofinterconnected limbic areas in orbitofrontal cortex insular cortex anteriorcingulate and amygdala (Schore 1997b in press a in preparation) Thelimbic system is now thought to be centrally involved in the implicit pro-cessing of facial expressions without conscious awareness (Critchley et al2000) and in the capacity lsquoto adapt to a rapidly changing environmentrsquo and inlsquothe organization of new learningrsquo (Mesulam 1998 p 1028) Emotionallyfocused limbic learning underlies the unique and fast-acting processes ofimprinting the learning mechanism associated with attachment as thisdynamic evolves over the rst and second years Hinde (1990 p 162) points

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 130

out that lsquothe development of social behavior can be understood only in termsof a continuing dialectic between an active and changing organism and anactive and changing environmentrsquo

But the orbitofrontal system is also deeply connected into the autonomicnervous system and the arousal-generating reticular formation and due tothe fact that it is the only cortical structure with such direct connections itcan regulate autonomic responses to social stimuli (Zald amp Kim 1996) andmodulate lsquoinstinctual behaviorrsquo (Starkstein amp Robinson 1997) The activityof this frontolimbic system is therefore critical to the modulation of socialand emotional behaviors and the homeostatic regulation of body and moti-vational states affect-regulating functions that are centrally involved inattachment processes The essential aspect of this function is highlighted byWestin (1997 p 542) who asserts that lsquoThe attempt to regulate affect ndash to min-imize unpleasant feelings and to maximize pleasant ones ndash is the driving forcein human motivationrsquo

The orbital prefrontal region is especially expanded in the right hemispherewhich is specialized for lsquoinhibitory controlrsquo (Garavan Ross amp Stein 1999)and it comes to act as an executive control function for the entire right brainThis hemisphere which is dominant for unconscious processes computes ona moment-to-moment basis the affective salience of external stimuli Keepingin mind Bowlbyrsquos earlier descriptions this lateralized system performs alsquovalence taggingrsquo function (Schore 1998a 1999) in which perceptions receivea positive or negative affective charge in accord with a calibration of degreesof pleasurendashunpleasure It also contains a lsquononverbal affect lexiconrsquo a vocabu-lary for nonverbal affective signals such as facial expressions gestures andvocal tone or prosody (Bowers Bauer amp Heilman 1993) The right hemi-sphere is thus faster than the left in performing valence-dependent automaticpre-attentive appraisal of emotional facial expressions (Pizzagalli Regard ampLehmann 1999)

Because the right cortical hemisphere more so than the left contains exten-sive reciprocal connections with limbic and subcortical regions (Tucker 1992Joseph 1996) it is dominant for the processing and expression of lsquoself-relatedmaterialrsquo (Keenan et al 1999) and emotional information and for regulatingpsychobiological states (Schore 1994 1998a 1999 Spence Shapiro amp Zaidel1996) Thus the right hemisphere is centrally involved in what Bowlbydescribed as the social and biological functions of the attachment system(Henry 1993 Schore 1994 Shapiro Jamner amp Spence 1997 Wang 1997Siegel 1999)

Conrming this model Ryan Kuhl and Deci (1997 p 719) using EEGand neuroimaging data conclude that lsquoThe positive emotional exchangeresulting from autonomy-supportive parenting involves participation ofright hemispheric cortical and subcortical systems that participate in globaltonic emotional modulationrsquo And in line with Bowlbyrsquos assertion thatattachment behavior is vital to the survival of the species it is now held thatthe right hemisphere is central to the control of vital functions supporting

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 31

survival and enabling the organism to cope with stresses and challenges(Wittling amp Schweiger 1993)

There is a growing body of studies which shows that the infantrsquos earlymaturing (Geschwind amp Galaburda 1987) right hemisphere is specicallyimpacted by early social experiences (Schore 1994 1998b) This develop-mental principle is now supported in a recent single photon emissioncomputed tomographic (SPECT) study by Chiron et al (1997) whichdemonstrates that the right brain hemisphere is dominant in preverbal humaninfants and indeed for the rst 3 years of life I suggest that the ontogeneticshift of dominance from the right to left hemisphere after this time may expli-cate Bowlbyrsquos description of a diminution of the attachment system at theend of the third year that is due to an lsquoabruptrsquo passage of a lsquomaturationalthresholdrsquo

Current neuropsychological studies indicate that lsquothe emotional experi-ence(s) of the infant are disproportionately stored or processed in theright hemisphere during the formative stages of brain ontogenyrsquo (Semrud-Clikeman amp Hynd 1990 p 198) that lsquothe infant relies primarily on its pro-cedural memory systemsrsquo during lsquothe rst 2ndash3 years of lifersquo (Kandel 1999 p 513) and that the right brain contains the lsquocerebral representation of onersquosown pastrsquo and the substrate of affectively laden autobiographical memory(Fink et al 1996 p 4275) These ndings suggest that early-forming inter-nal working models of the attachment relationship are processed and storedin implicit-procedural memory systems in the right cortex the hemispheredominant for implicit learning (Hugdahl 1995)

In the securely attached individual these models encode an expectationthat lsquohomeostatic disruptions will be set rightrsquo (Pipp amp Harmon 1987 p 650) In discussing these internal models Rutter (1987) notes that lsquochildrenderive a set of expectations about their own relationship capacities and aboutother peoplersquos resources to their social overtures and interactions theseexpectations being created on the basis of their early parentndashchild attach-mentsrsquo (p 449) Such representations are processed by the orbitofrontalsystem which is known to be activated during lsquobreaches of expectationrsquo(Nobre Coull Frith amp Mesulam 1999) and to generate affect-regulatingstrategies for coping with expected negative and positive emotional states thatare inherent in intimate social contexts

The efcient operations of this regulatory system allow for corticallyprocessed information concerning the external environment (such as visualand auditory stimuli emanating from the emotional face of the attachmentobject) to be integrated with subcortically processed information regardingthe internal visceral environment (such as concurrent changes in the childrsquosemotional or bodily self-state) The relaying of sensory information into thelimbic system allows incoming information about the social environment totrigger adjustments in emotional and motivational states and in this mannerthe orbitofrontal system integrates what Bowlby termed environmental andorganismic models Recent ndings that the orbitofrontal cortex generates

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 132

nonconscious biases that guide behavior before conscious knowledge does(Bechara Damasio Tranel amp Damasio 1997) and codes the likely signicanceof future behavioral options (Dolan 1999) and represents an important siteof contact between emotional information and mechanisms of action selec-tion (Rolls 1996) are consonant with Bowlbyrsquos (1981) assertion that internalworking models are used as guides for future action

These mental representations according to Main Kaplan and Cassidy(1985) contain cognitive as well as affective components and act to guideappraisals of experience The orbitofrontal cortex is known to function as anappraisal mechanism (Pribram 1987 Schore 1998a) and to be centrallyinvolved in the generation of lsquocognitive-emotional interactionsrsquo (Barbas1995) It acts to lsquointegrate and assign emotional-motivational signicance tocognitive impressions the association of emotion with ideas and thoughtsrsquo(Joseph 1996 p 427) and in lsquothe processing of affect-related meaningsrsquo (Teas-dale et al 1999)

Orbitofrontal activity is associated with a lower threshold for awarenessof sensations of both external and internal origin (Goldenberg et al 1989)thereby enabling it to act as an lsquointernal re ecting and organizing agencyrsquo(Kaplan-Solms amp Solms 1996) This orbitofrontal role in lsquoself-re ectiveawarenessrsquo (Stuss Gow amp Hetherington 1992) allows an individual to reecton his or her own internal emotional states as well as those of others(Povinelli amp Preuss 1995) According to Fonagy and Target (1997) the reec-tive function is a mental operation that enables the perception of anotherrsquosstate The right hemisphere mediates empathic cognition and the perceptionof the emotional states of other human beings (Voeller 1986) andorbitofrontal function is essential to the capacity of inferring the states ofothers (Baron-Cohen 1995) This adaptive capacity may thus be the outcomeof a secure attachment to a psychobiologically attuned affect-regulating care-giver A recent neuropsychological study indicates that the orbitofrontalcortex is lsquoparticularly involved in theory of mind tasks with an affective com-ponentrsquo (Stone Baron-Cohen amp Knight 1998 p 651)

Furthermore the functioning of the orbitofrontal control system in theregulation of emotion (Baker Frith amp Dolan 1997) and in lsquoacquiring veryspecic forms of knowledge for regulating interpersonal and social behaviorrsquo(Dolan 1999 p 928) is central to self-regulation the ability to exibly regu-late emotional states through interactions with other humans ndash that is inter-active regulation in interconnected contexts ndash and without other humans ndashthat is autoregulation in autonomous contexts The adaptive capacity to shiftbetween these dual regulatory modes depending upon the social contextemerges out of a history of secure attachment interactions of a maturing bio-logical organism and an early attuned social environment

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 33

ATTACH MENT THEORY IS FUNDAMENTALLYA REGULATORY THEORY

Attachment behavior is currently thought to be the output of lsquoa neuro-biologically based biobehavioral system that regulates biological syn-chronicity between organismsrsquo (Wang 1997 p 168) I suggest that thecharacterization of the orbitofrontal system as a frontolimbic structure thatdetermines the regulatory signi cance of stimuli that reach the organism andregulates body state (Luria 1980) bears a striking resemblance to the behav-ioral control system characterized by Bowlby over 30 years ago The OxfordDictionary denes control as lsquothe act or power of directing or regulatingrsquo

Attachment theory as rst propounded in Bowlbyrsquos (1969) denitionalvolume is fundamentally a regulatory theory Attachment can thus be con-ceptualized as the interactive regulation of synchrony between psychobiolog-ically attuned organisms This attachment dynamic which operates at levelsbeneath awareness underlies the dyadic regulation of emotion Emotions arethe highest order direct expression of bioregulation in complex organisms(Damasio 1998) Imprinting the learning process it accesses is described byPetrovich and Gewirtz (1985) as synchrony between sequential infant mater-nal stimuli and behavior (see Schore 1994 and Nelson amp Panksepp 1998 formodels of the neurochemistry of attachment)

According to Feldman et al (1999) lsquoface-to-face synchrony affords infantstheir rst opportunity to practice interpersonal coordination of biologicalrhythmsrsquo (p 223) and acts as an interpersonal context in which lsquointeractantsintegrate into the ow of behavior the ongoing responses of their partner andthe changing inputs of the environmentrsquo (p 224) The visual prosodic-auditory and gestural stimuli embedded in these emotional communicationsare rapidly transmitted back and forth between the infantrsquos and motherrsquos faceand in these transactions the caregiver acts as a regulator of the childrsquos arousallevels

Because arousal levels are known to be associated with changes in meta-bolic energy the caregiver is thus modulating changes in the childrsquos energeticstate (Schore 1994 1997b) These regulated increases in energy metabolismare available for biosynthetic processes in the babyrsquos brain which is in thebrain growth spurt (Dobbing amp Sands 1973) In this manner lsquothe intrinsicregulators of human brain growth in a child are specically adapted to becoupled by emotional communication to the regulators of adult brainsrsquo(Trevarthen 1990 p 357)

In addition the mother also regulates moments of asynchrony that isstressful negative affect Social stressors can be characterized as the occur-rence of an asynchrony in an interactional sequence (Chapple 1970) Stressdescribes both the subjective experience induced by a distressing potentiallythreatening or novel situation and the organismrsquos reactions to a homeosta-tic challenge It is now thought that social stressors are lsquofar more detrimen-talrsquo than non-social aversive stimuli (Sgoifo et al 1999)

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 134

Separation stress in essence is a loss of maternal regulators of the infantrsquosimmature behavioral and physiological systems that results in the attachmentpatterns of protest despair and detachment The principle that lsquoa period ofsynchrony following the period of stress provides a ldquorecoveryrdquo periodrsquo(Chapple 1970 p 631) underlies the mechanism of interactive repair(Tronick 1989 Schore 1994) The primary caregiverrsquos interactive regulationis therefore critical to the infantrsquos maintaining positively charged as well ascoping with stressful negatively charged affects These affect regulatingevents are particularly impacting the organization of the early developingright hemisphere

Bowlbyrsquos control system is located in the right hemisphere that is not onlydominant for lsquoinhibitory controlrsquo (Garavan et al 1999) but also for the pro-cessing of facial information in infants (Deruelle amp de Schonen 1998) andadults (Kim et al 1999) and for the regulation of arousal (Heilman amp VanDen Abell 1979) Because the major coping systems the hypothalamo-pituitary-adrenocortical axis and the sympathetic-adrenomedullary axis areboth under the main control of the right cerebral cortex this hemisphere con-tains lsquoa unique response system preparing the organism to deal efcientlywith external challengesrsquo and so its adaptive functions mediate the humanstress response (Wittling 1997 p 55) Basic research in stress physiologyshows that the behavioral and physiological response of an individual to aspecic stressor is consistent over time (Koolhaas et al 1999)

These attachment transactions are imprinted into implicit-proceduralmemory as enduring internal working models which encode coping strat-egies of affect regulation (Schore 1994) that maintain basic regulation andpositive affect even in the face of environmental challenge (Sroufe 1989)Attachment patterns are now conceptualized as lsquopatterns of mental process-ing of information based on cognition and affect to create models of realityrsquo(Crittenden 1995 p 401) The lsquoanterior limbic prefrontal networkrsquo whichinterconnects the orbital and medial prefrontal cortex with the temporal polecingulate and amygdala lsquois involved in affective responses to events and inthe mnemonic processing and storage of these responsesrsquo (Carmichael ampPrice 1995 p 639) and lsquoconstitutes a mental control system that is essentialfor adjusting thinking and behavior to ongoing realityrsquo (Schnider amp Ptak1999 p 680) An ultimate indicator of secure attachment is resilience in theface of stress (Greenspan 1981) which is expressed in the capacity to ex-ibly regulate emotional states via autoregulation and interactive regulationHowever early social environments that engender insecure attachmentsinhibit the growth of this control system (Schore 1997b) and therefore pre-clude its adaptive coping function in lsquooperations linked to behavioral exi-bilityrsquo (Nobre et al 1999 p 12)

In support of Bowlbyrsquos assertion that the childrsquos capacity to cope withstress is correlated with certain maternal behaviors current developmentalbiological studies are exploring lsquomaternal effectsrsquo the inuence of themotherrsquos experiences on her progenyrsquos development and ability to adapt to

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 35

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

species that is more extensive studies of how an attachment bond formsbetween the infant and the mother In this conception Bowlby asserts thatthese developmental processes are the product of the interaction of a uniquegenetic endowment with a particular environment and that the infantrsquosemerging social psychological and biological capacities cannot be under-stood apart from its relationship with the mother

BOWLBYrsquoS ORIGINAL CHARTINGS OF THEATTACHM EN T LANDSCAPE

Much has transpired since the original publication of Bowlbyrsquos Attachmentand the ensuing explosion of attachment research over the last quarter of acentury is a testament to the power of the concepts it contains And yet a (re-) reading of this classic still continues to reveal more and more subtleinsights into the nature of developmental processes and to shine light uponyet to be fully explored areas of developmental research In fact in thisseminal work of developmental science the pioneering Bowlby presents asurvey of what he sees to be the essential topographic landmarks of theuncharted territory of motherndashinfant relationally driven psychobiologicalprocesses The essential guideposts of this dynamic domain ndash the centralphenomena that must be considered in any overarching model of how theattachment relationship generates both immediate and long-enduring effectson the developing individual ndash are presented by Bowlby in not only thesubject-matter but also the structural organization of the book The readerwill notice that the book is divided into four parts lsquoThe taskrsquo lsquoInstinctivebehaviourrsquo lsquoAttachment behaviourrsquo and lsquoOntogeny of human attachmentrsquoand that Bowlby devotes ten chapters to the rst two parts and seven to thelast two parts

It is now more than 30 years since Bowlbyrsquos call for lsquoa far-reaching pro-gramme of research into the social responses of man from the preverbalperiod of infancy onwardsrsquo (p 174) In the following I want to briey offerfrom a psychoneurobiological perspective not only my views of the originalcontents of Bowlbyrsquos guidebook but also some thoughts about the currentand future directions of the experimental and clinical explorations of attach-ment theory as they pass from one century into the next In doing so I willspecically attend to not so much the quality of attachment research whichhas served as a standard in psychology psychiatry and psychoanalysis as awhole or to the breadth of the research which spans developmental psy-chology developmental psychobiology developmental neurochemistryinfant psychiatry and psychoanalysis but rather to the foci of currentinvestigations as measured against the original prescriptions that are offeredhere by Bowlby And I will suggest that certain uninvestigated areas of thisattachment domain sketched out in Bowlbyrsquos cartographic descriptions inthis book are now ready to be explored by interdisciplinary research

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 25

programs For a broad overview of the eld at the end of century I refer thereader to two excellent edited volumes Attachment theory Social develop-mental and clinical perspectives (Goldberg Muir amp Kerr 1995) and Hand-book of attachment Theory research and clinical applications (Cassidy ampShaver 1999)

In the book most current readers are very familiar (or even perhaps onlyfamiliar) with the latter two sections on attachment and most researcherscontinue to focus their investigation upon the concepts outlined in these laterchapters It is here as well as in the introductory sections that Bowlby pre-sents his essential contributions on the infantrsquos sequential responses to separ-ation from the primary attachment gure ndash protest despair and detachmentIn the context of emphasizing the importance of studying the infantrsquos behav-ior specically during the temporal interval when the mother returnsBowlby introduces the recent methodology of Ainsworth which will soonbecome the major experimental paradigm for attachment research the incre-mentally stress-increasing lsquostrange situationrsquo

But in addition to theorizing on the nature of separation responses stress-ful ruptures of the motherndashinfant bond Bowlby also describes what he seesas the fundamental dynamics of the attachment relationship In stating thatthe infant is active in seeking interaction that the motherrsquos maternal behav-ior is lsquoreciprocalrsquo to the infantrsquos attachment behavior and that the develop-ment of attachment is related both to the sensitivity of the mother inresponding to her babyrsquos cues and to the amount and nature of their inter-action he lays a groundwork that presents attachment dynamics as a lsquorecip-rocal interchangersquo (p 346) a conceptualization that is perfectly compatiblewith recent advances in dynamic systems theory (Schore 1997b in press aLewis 1995 1999 in press)

At the very beginning of the section on lsquoAttachment behaviorrsquo Bowlbyoffers his earliest model of the essential characteristics of attachment ndash it isinstinctive social behavior with a biological function lsquoreadily activatedespecially by the motherrsquos departure or by anything frightening and thestimuli that most ef ciently terminate the systems are sound sight or touchof the motherrsquo and is lsquoa product of the activity of a number of behaviouralsystems that have proximity to mother as a predictable outcomersquo (p 179)Although the rst three postulates remained unaltered in his later writingsin his second volume Bowlby (1973) attempted to dene more precisely theset-goal of the attachment system as seeking not just proximity but access toan attachment gure who is emotionally available and responsive

A further evolution of this concept is now found in transactional theoriesthat emphasize the central role of the primary caregiver in co-regulatingthe childrsquos facially expressed emotional states (Schore 1994 1998a in pressb) and that de ne attachment as the dyadic regulation of emotion (Sroufe1996) and the regulation of biological synchronicity between organisms(Wang 1997) The development of synchronized interactions is fundamentalto the healthy affective development of the infant (Penman Meares amp

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 126

Milgrom-Friedman 1983) Reite and Capitanio (1985) conceptualize affect aslsquoa manifestation of underlying modulating or motivational systems subserv-ing or facilitating social attachmentsrsquo (p 248) and suggest that an essentialattachment function is lsquoto promote the synchrony or regulation of biologicaland behavioral systems on an organismic levelrsquo (p 235) In these rapid regu-lated face-to-face transactions the psychobiologically attuned (Field 1985)caregiver not only minimizes the infantrsquos negative but also maximizes its posi-tive affective states (Schore 1994 1996 1998b) This proximate interpersonalcontext of lsquoaffect synchronyrsquo (Feldman Greenbaum amp Yirmiya 1999) andinterpersonal resonance (Schore 1997b in press b) represents the externalrealm of attachment dynamics

But due to his interests in the inner world Bowlby here presents a modelof events occurring within the internal realm of attachment processes Andso he offers his initial speculations about how the developing child constructsinternal working models lsquoof how the physical world may be expected tobehave how his mother and other signicant persons may be expected tobehave how he himself may be expected to behave and how each interactswith the otherrsquo (p 354) This initial concept has currently evolved intolsquoprocess-orientedrsquo conceptions of internal working models as representationsthat regulate an individualrsquos relationship adaptation through interpre-tiveattributional processes (Bretherton amp Munholland 1999) and encodestrategies of affect regulation (Kobak amp Sceery 1988 Schore 1994) Currentpsychobiological models refer to representations of the infantrsquos affective dia-logue with the mother which can be accessed to regulate its affective state(Polan amp Hofer 1999)

Interestingly Bowlby also describes internal working models in the rstpart of the volume the eight chapters devoted to lsquoinstinctive behaviorrsquo Irepeat my assertion that a deeper explication of the fundamental themes ofthis section of the book represents the frontier of attachment theory andresearch In these opening chapters the aggregate of which represents thefoundation on which the later chapters on attachment are built Bowlbyposits that internal models function as lsquocognitive mapsrsquo in the brain and areaccessed lsquoto transmit store and manipulate information that helps makingpredictions as to how set-goals (of attachment) can be achievedrsquo (p 80)Furthermore he states that lsquothe two working models each individual musthave are referred to respectively as his environmental model and his organ-ismic modelrsquo (p 82) This is because lsquosensory data regarding events reachingan organism via its sense organs are immediately assessed regulated andinterpreted The same is true of sensory data derived from the internal stateof the organismrsquo (p 109) Here Bowlby is pointing to the need for a develop-mental theoretical conception of attachment that can tie together psychologyand biology mind and body

And so at the very onset of his essay he begins lsquoThe taskrsquo by describinga theoretical landscape that includes both the biological and social aspectsof attachment a terrain that must be described in terms of its structural

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 27

organization as well as its functional properties Following the generalperspective of all biological investigators he attempts to elucidate thestructurendashfunction relationships of a living system but with the added per-spective of developmental biology he is specically focusing on the early criti-cal stages within which the system rst self-organizes Thus the form of thebook is rst to outline the general characteristics of the internal structuralsystem and then to describe this systemrsquos central functional role in attachmentprocesses

Bowlby begins the third chapter by quoting Freudrsquos (1925) dictum thatlsquoThere is no more urgent need in psychology than for a securely foundedtheory of the instinctsrsquo The attempt to do so in this book an offering of anlsquoalternative model of instinctive behaviorrsquo in essence represents Bowlbyrsquosconviction that what Freud was calling for was the creation of a model thatcould explicate the biology of unconscious processes Towards that end inthe rst of eight chapters on the topic he proposes that attachment is instinc-tive behavior associated with self-preservation and that it is a product of theinteraction between genetic endowment and the early environment

But immediately after a brief 5-page introduction Bowlby launches into adetailed description of a biological control system that is centrally involvedin instinctive behavior This control system is structured as a hierarchicalmode of organization that acts as lsquoan overall goal-corrected behavioral struc-turersquo Bowlby also gives some hints as to the neurobiological operations ofthis control system ndash its functions must be associated with the organismrsquoslsquostate of arousalrsquo that results from the critical operations of the reticular for-mation and with lsquothe appraisal of organismic states and situations of the mid-brain nuclei and limbic systemrsquo (p 110) He even offers a speculation aboutits anatomical location ndash the prefrontal lobes (p 156)

This control system he says is lsquoopen in some degree to inuence by theenvironment in which development occursrsquo (p 45) More specically itevolves in the infantrsquos interaction with an lsquoenvironment of adaptiveness andespecially of his interaction with the principal gure in that environmentnamely his motherrsquo (p 180) Furthermore Bowlby speculates that thelsquoupgrading of control during individual development from simple to moresophisticated is no doubt in large part a result of the growth of the centralnervous systemrsquo (p 156) In fact he even goes so far as to suggest the tem-poral interval that is critical to the maturation of this control system ndash 9 to18 months (p 180)

In a subsequent chapter on lsquoAppraising and selecting Feeling andemotionrsquo Bowlby quotes Darwinrsquos (1872) observation that the movementsof expression in the face and body serve as the rst means of communicationbetween the mother and the infant Furthering this theme on the communi-cative role of feeling and emotion Bowlby emphasizes the salience of lsquofacialexpression posture tone of voice physiological changes tempo of move-ment and incipient actionrsquo (p 120) The appraisal of this input is experiencedlsquoin terms of value as pleasant or unpleasantrsquo (pp 111ndash112) and the

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 128

movements lsquomay be actively at work even when we are not aware of themrsquo(p 110) in this manner feeling provides a monitoring of both the behavioraland physiological state (p 121) Emotional processes thus he says lie at thefoundation of a model of instinctive behavior

In following chapters Bowlby concludes that the motherndashinfant attach-ment relation is lsquoaccompanied by the strongest of feelings and emotionshappy or the reversersquo (p 242) that the infantrsquos lsquocapacity to cope with stressrsquois correlated with certain maternal behaviors (p 344) and that the instinctivebehavior that emerges from the co-constructed environment of evolutionaryadaptiveness has consequences that are lsquovital to the survival of the speciesrsquo (p 137) He also suggests that the attachment system is readily activated untilthe end of the third year when the childrsquos capacity to cope with maternalseparation lsquoabruptlyrsquo improves due to the fact that lsquosome maturationalthreshold is passedrsquo (p 205)

CONTRIBUTIONS FROM NEUROSCIENCE TOATTACHM ENT THEORY

So the next question is 30 years after the appearance of this volume at theend of the lsquodecade of the brainrsquo how do Bowlbyrsquos original chartings of theattachment domain hold up In a word they were indeed prescient In facthis overall birdrsquos-eye perspective of the internal attachment landscape was socomprehensive that we now need to zoom in not just for close-up views ofthe essential brain structures that mediate attachment processes but also forvisualizations of how these structures dynamically self-organize within thedeveloping brain This includes neurobiological studies of Bowlbyrsquos controlsystem which I suggest may now be identied with the orbitofrontal cortexan area that has been called the lsquosenior executive of the emotional brainrsquo(Joseph 1996) and that has been shown to mediate lsquothe highest level ofcontrol of behavior especially in relation to emotionrsquo (Price Carmichael ampDrevets 1996 p 523) Keeping in mind Bowlbyrsquos previously presentedtheoretical descriptions the following is an extremely brief overview of agrowing body of studies on the neurobiology of attachment (For moreextensive expositions of these concepts and references see Schore 1994 19961997b 1998a 1999 in press a b c d e in preparation)

According to Ainsworth (1967 p 429) attachment is more than overtbehavior it is internal lsquobeing built into the nervous system in the course andas a result of the infantrsquos experience of his transactions with the motherrsquoFollowing Bowlbyrsquos suggestion the limbic system has been suggested to bethe site of developmental changes associated with the rise of attachmentbehaviors (Anders amp Zeanah 1984) Indeed the specic period from 7 to 15months has been shown to be critical for the myelination and therefore thematuration of particular rapidly developing limbic and cortical associationareas (Kinney Brody Kloman amp Gilles 1988) and limbic areas of the human

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 29

cerebral cortex show anatomical maturation at 15 months (Rabinowicz1979) In a number of works I offer evidence to show that attachment experi-ences face-to-face transactions of affect synchrony between caregiver andinfant directly inuence the imprinting the circuit wiring of the orbitalprefrontal cortex a corticolimbic area that is known to begin a major matu-rational change at 10 to 12 months and to complete a critical period of growthfrom the middle to the end of the second year This time-frame is identical toBowlbyrsquos maturation of an attachment control system that is open to in u-ence from the developmental environment

The co-created environment of evolutionary adaptiveness is thus isomor-phic to a growth-facilitating environment for the experience-dependent mat-uration of a regulatory system in the orbitofrontal cortex Indeed thisprefrontal system appraises visual facial information (Scalaidhe Wilson ampGoldman-Rakic 1997) and processes responses to pleasant touch tastesmell (Francis D et al 1999) and music (Blood Zatorre Bermudez ampEvans 1999) as well as to unpleasant images of angry and sad faces (BlairMorris Frith Perrett amp Dolan 1999) But this system is also involved in theregulation of the body state and reects changes taking place in that state(Luria 1980)

This frontolimbic system provides a high-level coding that exibly co-ordinates exteroceptive and interoceptive domains and functions to correctresponses as conditions change (Derryberry amp Tucker 1992) processes feed-back information (Elliott Frith amp Dolan 1997) and thereby monitorsadjusts and corrects emotional responses (Rolls 1986) and modulates themotivational control of goal-directed behavior (Tremblay amp Schultz 1999)So after a rapid evaluation of an environmental stimulus the orbitofrontalsystem monitors feedback about the current internal state in order to makeassessments of coping resources and it updates appropriate response outputsin order to make adaptive adjustments to particular environmental perturba-tions (Schore 1998a) In this manner lsquothe integrity of the orbitofrontal cortexis necessary for acquiring very specic forms of knowledge for regulatinginterpersonal behaviorrsquo (Dolan 1999 p 928)

These functions reect the unique anatomical properties of this area of thebrain Due to its location at the ventral and medial hemispheric surfaces itacts as a convergence zone where cortex and subcortex meet It is thus situ-ated at the apogee of the lsquorostral limbic systemrsquo a hierarchical sequence ofinterconnected limbic areas in orbitofrontal cortex insular cortex anteriorcingulate and amygdala (Schore 1997b in press a in preparation) Thelimbic system is now thought to be centrally involved in the implicit pro-cessing of facial expressions without conscious awareness (Critchley et al2000) and in the capacity lsquoto adapt to a rapidly changing environmentrsquo and inlsquothe organization of new learningrsquo (Mesulam 1998 p 1028) Emotionallyfocused limbic learning underlies the unique and fast-acting processes ofimprinting the learning mechanism associated with attachment as thisdynamic evolves over the rst and second years Hinde (1990 p 162) points

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 130

out that lsquothe development of social behavior can be understood only in termsof a continuing dialectic between an active and changing organism and anactive and changing environmentrsquo

But the orbitofrontal system is also deeply connected into the autonomicnervous system and the arousal-generating reticular formation and due tothe fact that it is the only cortical structure with such direct connections itcan regulate autonomic responses to social stimuli (Zald amp Kim 1996) andmodulate lsquoinstinctual behaviorrsquo (Starkstein amp Robinson 1997) The activityof this frontolimbic system is therefore critical to the modulation of socialand emotional behaviors and the homeostatic regulation of body and moti-vational states affect-regulating functions that are centrally involved inattachment processes The essential aspect of this function is highlighted byWestin (1997 p 542) who asserts that lsquoThe attempt to regulate affect ndash to min-imize unpleasant feelings and to maximize pleasant ones ndash is the driving forcein human motivationrsquo

The orbital prefrontal region is especially expanded in the right hemispherewhich is specialized for lsquoinhibitory controlrsquo (Garavan Ross amp Stein 1999)and it comes to act as an executive control function for the entire right brainThis hemisphere which is dominant for unconscious processes computes ona moment-to-moment basis the affective salience of external stimuli Keepingin mind Bowlbyrsquos earlier descriptions this lateralized system performs alsquovalence taggingrsquo function (Schore 1998a 1999) in which perceptions receivea positive or negative affective charge in accord with a calibration of degreesof pleasurendashunpleasure It also contains a lsquononverbal affect lexiconrsquo a vocabu-lary for nonverbal affective signals such as facial expressions gestures andvocal tone or prosody (Bowers Bauer amp Heilman 1993) The right hemi-sphere is thus faster than the left in performing valence-dependent automaticpre-attentive appraisal of emotional facial expressions (Pizzagalli Regard ampLehmann 1999)

Because the right cortical hemisphere more so than the left contains exten-sive reciprocal connections with limbic and subcortical regions (Tucker 1992Joseph 1996) it is dominant for the processing and expression of lsquoself-relatedmaterialrsquo (Keenan et al 1999) and emotional information and for regulatingpsychobiological states (Schore 1994 1998a 1999 Spence Shapiro amp Zaidel1996) Thus the right hemisphere is centrally involved in what Bowlbydescribed as the social and biological functions of the attachment system(Henry 1993 Schore 1994 Shapiro Jamner amp Spence 1997 Wang 1997Siegel 1999)

Conrming this model Ryan Kuhl and Deci (1997 p 719) using EEGand neuroimaging data conclude that lsquoThe positive emotional exchangeresulting from autonomy-supportive parenting involves participation ofright hemispheric cortical and subcortical systems that participate in globaltonic emotional modulationrsquo And in line with Bowlbyrsquos assertion thatattachment behavior is vital to the survival of the species it is now held thatthe right hemisphere is central to the control of vital functions supporting

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 31

survival and enabling the organism to cope with stresses and challenges(Wittling amp Schweiger 1993)

There is a growing body of studies which shows that the infantrsquos earlymaturing (Geschwind amp Galaburda 1987) right hemisphere is specicallyimpacted by early social experiences (Schore 1994 1998b) This develop-mental principle is now supported in a recent single photon emissioncomputed tomographic (SPECT) study by Chiron et al (1997) whichdemonstrates that the right brain hemisphere is dominant in preverbal humaninfants and indeed for the rst 3 years of life I suggest that the ontogeneticshift of dominance from the right to left hemisphere after this time may expli-cate Bowlbyrsquos description of a diminution of the attachment system at theend of the third year that is due to an lsquoabruptrsquo passage of a lsquomaturationalthresholdrsquo

Current neuropsychological studies indicate that lsquothe emotional experi-ence(s) of the infant are disproportionately stored or processed in theright hemisphere during the formative stages of brain ontogenyrsquo (Semrud-Clikeman amp Hynd 1990 p 198) that lsquothe infant relies primarily on its pro-cedural memory systemsrsquo during lsquothe rst 2ndash3 years of lifersquo (Kandel 1999 p 513) and that the right brain contains the lsquocerebral representation of onersquosown pastrsquo and the substrate of affectively laden autobiographical memory(Fink et al 1996 p 4275) These ndings suggest that early-forming inter-nal working models of the attachment relationship are processed and storedin implicit-procedural memory systems in the right cortex the hemispheredominant for implicit learning (Hugdahl 1995)

In the securely attached individual these models encode an expectationthat lsquohomeostatic disruptions will be set rightrsquo (Pipp amp Harmon 1987 p 650) In discussing these internal models Rutter (1987) notes that lsquochildrenderive a set of expectations about their own relationship capacities and aboutother peoplersquos resources to their social overtures and interactions theseexpectations being created on the basis of their early parentndashchild attach-mentsrsquo (p 449) Such representations are processed by the orbitofrontalsystem which is known to be activated during lsquobreaches of expectationrsquo(Nobre Coull Frith amp Mesulam 1999) and to generate affect-regulatingstrategies for coping with expected negative and positive emotional states thatare inherent in intimate social contexts

The efcient operations of this regulatory system allow for corticallyprocessed information concerning the external environment (such as visualand auditory stimuli emanating from the emotional face of the attachmentobject) to be integrated with subcortically processed information regardingthe internal visceral environment (such as concurrent changes in the childrsquosemotional or bodily self-state) The relaying of sensory information into thelimbic system allows incoming information about the social environment totrigger adjustments in emotional and motivational states and in this mannerthe orbitofrontal system integrates what Bowlby termed environmental andorganismic models Recent ndings that the orbitofrontal cortex generates

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 132

nonconscious biases that guide behavior before conscious knowledge does(Bechara Damasio Tranel amp Damasio 1997) and codes the likely signicanceof future behavioral options (Dolan 1999) and represents an important siteof contact between emotional information and mechanisms of action selec-tion (Rolls 1996) are consonant with Bowlbyrsquos (1981) assertion that internalworking models are used as guides for future action

These mental representations according to Main Kaplan and Cassidy(1985) contain cognitive as well as affective components and act to guideappraisals of experience The orbitofrontal cortex is known to function as anappraisal mechanism (Pribram 1987 Schore 1998a) and to be centrallyinvolved in the generation of lsquocognitive-emotional interactionsrsquo (Barbas1995) It acts to lsquointegrate and assign emotional-motivational signicance tocognitive impressions the association of emotion with ideas and thoughtsrsquo(Joseph 1996 p 427) and in lsquothe processing of affect-related meaningsrsquo (Teas-dale et al 1999)

Orbitofrontal activity is associated with a lower threshold for awarenessof sensations of both external and internal origin (Goldenberg et al 1989)thereby enabling it to act as an lsquointernal re ecting and organizing agencyrsquo(Kaplan-Solms amp Solms 1996) This orbitofrontal role in lsquoself-re ectiveawarenessrsquo (Stuss Gow amp Hetherington 1992) allows an individual to reecton his or her own internal emotional states as well as those of others(Povinelli amp Preuss 1995) According to Fonagy and Target (1997) the reec-tive function is a mental operation that enables the perception of anotherrsquosstate The right hemisphere mediates empathic cognition and the perceptionof the emotional states of other human beings (Voeller 1986) andorbitofrontal function is essential to the capacity of inferring the states ofothers (Baron-Cohen 1995) This adaptive capacity may thus be the outcomeof a secure attachment to a psychobiologically attuned affect-regulating care-giver A recent neuropsychological study indicates that the orbitofrontalcortex is lsquoparticularly involved in theory of mind tasks with an affective com-ponentrsquo (Stone Baron-Cohen amp Knight 1998 p 651)

Furthermore the functioning of the orbitofrontal control system in theregulation of emotion (Baker Frith amp Dolan 1997) and in lsquoacquiring veryspecic forms of knowledge for regulating interpersonal and social behaviorrsquo(Dolan 1999 p 928) is central to self-regulation the ability to exibly regu-late emotional states through interactions with other humans ndash that is inter-active regulation in interconnected contexts ndash and without other humans ndashthat is autoregulation in autonomous contexts The adaptive capacity to shiftbetween these dual regulatory modes depending upon the social contextemerges out of a history of secure attachment interactions of a maturing bio-logical organism and an early attuned social environment

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 33

ATTACH MENT THEORY IS FUNDAMENTALLYA REGULATORY THEORY

Attachment behavior is currently thought to be the output of lsquoa neuro-biologically based biobehavioral system that regulates biological syn-chronicity between organismsrsquo (Wang 1997 p 168) I suggest that thecharacterization of the orbitofrontal system as a frontolimbic structure thatdetermines the regulatory signi cance of stimuli that reach the organism andregulates body state (Luria 1980) bears a striking resemblance to the behav-ioral control system characterized by Bowlby over 30 years ago The OxfordDictionary denes control as lsquothe act or power of directing or regulatingrsquo

Attachment theory as rst propounded in Bowlbyrsquos (1969) denitionalvolume is fundamentally a regulatory theory Attachment can thus be con-ceptualized as the interactive regulation of synchrony between psychobiolog-ically attuned organisms This attachment dynamic which operates at levelsbeneath awareness underlies the dyadic regulation of emotion Emotions arethe highest order direct expression of bioregulation in complex organisms(Damasio 1998) Imprinting the learning process it accesses is described byPetrovich and Gewirtz (1985) as synchrony between sequential infant mater-nal stimuli and behavior (see Schore 1994 and Nelson amp Panksepp 1998 formodels of the neurochemistry of attachment)

According to Feldman et al (1999) lsquoface-to-face synchrony affords infantstheir rst opportunity to practice interpersonal coordination of biologicalrhythmsrsquo (p 223) and acts as an interpersonal context in which lsquointeractantsintegrate into the ow of behavior the ongoing responses of their partner andthe changing inputs of the environmentrsquo (p 224) The visual prosodic-auditory and gestural stimuli embedded in these emotional communicationsare rapidly transmitted back and forth between the infantrsquos and motherrsquos faceand in these transactions the caregiver acts as a regulator of the childrsquos arousallevels

Because arousal levels are known to be associated with changes in meta-bolic energy the caregiver is thus modulating changes in the childrsquos energeticstate (Schore 1994 1997b) These regulated increases in energy metabolismare available for biosynthetic processes in the babyrsquos brain which is in thebrain growth spurt (Dobbing amp Sands 1973) In this manner lsquothe intrinsicregulators of human brain growth in a child are specically adapted to becoupled by emotional communication to the regulators of adult brainsrsquo(Trevarthen 1990 p 357)

In addition the mother also regulates moments of asynchrony that isstressful negative affect Social stressors can be characterized as the occur-rence of an asynchrony in an interactional sequence (Chapple 1970) Stressdescribes both the subjective experience induced by a distressing potentiallythreatening or novel situation and the organismrsquos reactions to a homeosta-tic challenge It is now thought that social stressors are lsquofar more detrimen-talrsquo than non-social aversive stimuli (Sgoifo et al 1999)

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 134

Separation stress in essence is a loss of maternal regulators of the infantrsquosimmature behavioral and physiological systems that results in the attachmentpatterns of protest despair and detachment The principle that lsquoa period ofsynchrony following the period of stress provides a ldquorecoveryrdquo periodrsquo(Chapple 1970 p 631) underlies the mechanism of interactive repair(Tronick 1989 Schore 1994) The primary caregiverrsquos interactive regulationis therefore critical to the infantrsquos maintaining positively charged as well ascoping with stressful negatively charged affects These affect regulatingevents are particularly impacting the organization of the early developingright hemisphere

Bowlbyrsquos control system is located in the right hemisphere that is not onlydominant for lsquoinhibitory controlrsquo (Garavan et al 1999) but also for the pro-cessing of facial information in infants (Deruelle amp de Schonen 1998) andadults (Kim et al 1999) and for the regulation of arousal (Heilman amp VanDen Abell 1979) Because the major coping systems the hypothalamo-pituitary-adrenocortical axis and the sympathetic-adrenomedullary axis areboth under the main control of the right cerebral cortex this hemisphere con-tains lsquoa unique response system preparing the organism to deal efcientlywith external challengesrsquo and so its adaptive functions mediate the humanstress response (Wittling 1997 p 55) Basic research in stress physiologyshows that the behavioral and physiological response of an individual to aspecic stressor is consistent over time (Koolhaas et al 1999)

These attachment transactions are imprinted into implicit-proceduralmemory as enduring internal working models which encode coping strat-egies of affect regulation (Schore 1994) that maintain basic regulation andpositive affect even in the face of environmental challenge (Sroufe 1989)Attachment patterns are now conceptualized as lsquopatterns of mental process-ing of information based on cognition and affect to create models of realityrsquo(Crittenden 1995 p 401) The lsquoanterior limbic prefrontal networkrsquo whichinterconnects the orbital and medial prefrontal cortex with the temporal polecingulate and amygdala lsquois involved in affective responses to events and inthe mnemonic processing and storage of these responsesrsquo (Carmichael ampPrice 1995 p 639) and lsquoconstitutes a mental control system that is essentialfor adjusting thinking and behavior to ongoing realityrsquo (Schnider amp Ptak1999 p 680) An ultimate indicator of secure attachment is resilience in theface of stress (Greenspan 1981) which is expressed in the capacity to ex-ibly regulate emotional states via autoregulation and interactive regulationHowever early social environments that engender insecure attachmentsinhibit the growth of this control system (Schore 1997b) and therefore pre-clude its adaptive coping function in lsquooperations linked to behavioral exi-bilityrsquo (Nobre et al 1999 p 12)

In support of Bowlbyrsquos assertion that the childrsquos capacity to cope withstress is correlated with certain maternal behaviors current developmentalbiological studies are exploring lsquomaternal effectsrsquo the inuence of themotherrsquos experiences on her progenyrsquos development and ability to adapt to

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 35

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

programs For a broad overview of the eld at the end of century I refer thereader to two excellent edited volumes Attachment theory Social develop-mental and clinical perspectives (Goldberg Muir amp Kerr 1995) and Hand-book of attachment Theory research and clinical applications (Cassidy ampShaver 1999)

In the book most current readers are very familiar (or even perhaps onlyfamiliar) with the latter two sections on attachment and most researcherscontinue to focus their investigation upon the concepts outlined in these laterchapters It is here as well as in the introductory sections that Bowlby pre-sents his essential contributions on the infantrsquos sequential responses to separ-ation from the primary attachment gure ndash protest despair and detachmentIn the context of emphasizing the importance of studying the infantrsquos behav-ior specically during the temporal interval when the mother returnsBowlby introduces the recent methodology of Ainsworth which will soonbecome the major experimental paradigm for attachment research the incre-mentally stress-increasing lsquostrange situationrsquo

But in addition to theorizing on the nature of separation responses stress-ful ruptures of the motherndashinfant bond Bowlby also describes what he seesas the fundamental dynamics of the attachment relationship In stating thatthe infant is active in seeking interaction that the motherrsquos maternal behav-ior is lsquoreciprocalrsquo to the infantrsquos attachment behavior and that the develop-ment of attachment is related both to the sensitivity of the mother inresponding to her babyrsquos cues and to the amount and nature of their inter-action he lays a groundwork that presents attachment dynamics as a lsquorecip-rocal interchangersquo (p 346) a conceptualization that is perfectly compatiblewith recent advances in dynamic systems theory (Schore 1997b in press aLewis 1995 1999 in press)

At the very beginning of the section on lsquoAttachment behaviorrsquo Bowlbyoffers his earliest model of the essential characteristics of attachment ndash it isinstinctive social behavior with a biological function lsquoreadily activatedespecially by the motherrsquos departure or by anything frightening and thestimuli that most ef ciently terminate the systems are sound sight or touchof the motherrsquo and is lsquoa product of the activity of a number of behaviouralsystems that have proximity to mother as a predictable outcomersquo (p 179)Although the rst three postulates remained unaltered in his later writingsin his second volume Bowlby (1973) attempted to dene more precisely theset-goal of the attachment system as seeking not just proximity but access toan attachment gure who is emotionally available and responsive

A further evolution of this concept is now found in transactional theoriesthat emphasize the central role of the primary caregiver in co-regulatingthe childrsquos facially expressed emotional states (Schore 1994 1998a in pressb) and that de ne attachment as the dyadic regulation of emotion (Sroufe1996) and the regulation of biological synchronicity between organisms(Wang 1997) The development of synchronized interactions is fundamentalto the healthy affective development of the infant (Penman Meares amp

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 126

Milgrom-Friedman 1983) Reite and Capitanio (1985) conceptualize affect aslsquoa manifestation of underlying modulating or motivational systems subserv-ing or facilitating social attachmentsrsquo (p 248) and suggest that an essentialattachment function is lsquoto promote the synchrony or regulation of biologicaland behavioral systems on an organismic levelrsquo (p 235) In these rapid regu-lated face-to-face transactions the psychobiologically attuned (Field 1985)caregiver not only minimizes the infantrsquos negative but also maximizes its posi-tive affective states (Schore 1994 1996 1998b) This proximate interpersonalcontext of lsquoaffect synchronyrsquo (Feldman Greenbaum amp Yirmiya 1999) andinterpersonal resonance (Schore 1997b in press b) represents the externalrealm of attachment dynamics

But due to his interests in the inner world Bowlby here presents a modelof events occurring within the internal realm of attachment processes Andso he offers his initial speculations about how the developing child constructsinternal working models lsquoof how the physical world may be expected tobehave how his mother and other signicant persons may be expected tobehave how he himself may be expected to behave and how each interactswith the otherrsquo (p 354) This initial concept has currently evolved intolsquoprocess-orientedrsquo conceptions of internal working models as representationsthat regulate an individualrsquos relationship adaptation through interpre-tiveattributional processes (Bretherton amp Munholland 1999) and encodestrategies of affect regulation (Kobak amp Sceery 1988 Schore 1994) Currentpsychobiological models refer to representations of the infantrsquos affective dia-logue with the mother which can be accessed to regulate its affective state(Polan amp Hofer 1999)

Interestingly Bowlby also describes internal working models in the rstpart of the volume the eight chapters devoted to lsquoinstinctive behaviorrsquo Irepeat my assertion that a deeper explication of the fundamental themes ofthis section of the book represents the frontier of attachment theory andresearch In these opening chapters the aggregate of which represents thefoundation on which the later chapters on attachment are built Bowlbyposits that internal models function as lsquocognitive mapsrsquo in the brain and areaccessed lsquoto transmit store and manipulate information that helps makingpredictions as to how set-goals (of attachment) can be achievedrsquo (p 80)Furthermore he states that lsquothe two working models each individual musthave are referred to respectively as his environmental model and his organ-ismic modelrsquo (p 82) This is because lsquosensory data regarding events reachingan organism via its sense organs are immediately assessed regulated andinterpreted The same is true of sensory data derived from the internal stateof the organismrsquo (p 109) Here Bowlby is pointing to the need for a develop-mental theoretical conception of attachment that can tie together psychologyand biology mind and body

And so at the very onset of his essay he begins lsquoThe taskrsquo by describinga theoretical landscape that includes both the biological and social aspectsof attachment a terrain that must be described in terms of its structural

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 27

organization as well as its functional properties Following the generalperspective of all biological investigators he attempts to elucidate thestructurendashfunction relationships of a living system but with the added per-spective of developmental biology he is specically focusing on the early criti-cal stages within which the system rst self-organizes Thus the form of thebook is rst to outline the general characteristics of the internal structuralsystem and then to describe this systemrsquos central functional role in attachmentprocesses

Bowlby begins the third chapter by quoting Freudrsquos (1925) dictum thatlsquoThere is no more urgent need in psychology than for a securely foundedtheory of the instinctsrsquo The attempt to do so in this book an offering of anlsquoalternative model of instinctive behaviorrsquo in essence represents Bowlbyrsquosconviction that what Freud was calling for was the creation of a model thatcould explicate the biology of unconscious processes Towards that end inthe rst of eight chapters on the topic he proposes that attachment is instinc-tive behavior associated with self-preservation and that it is a product of theinteraction between genetic endowment and the early environment

But immediately after a brief 5-page introduction Bowlby launches into adetailed description of a biological control system that is centrally involvedin instinctive behavior This control system is structured as a hierarchicalmode of organization that acts as lsquoan overall goal-corrected behavioral struc-turersquo Bowlby also gives some hints as to the neurobiological operations ofthis control system ndash its functions must be associated with the organismrsquoslsquostate of arousalrsquo that results from the critical operations of the reticular for-mation and with lsquothe appraisal of organismic states and situations of the mid-brain nuclei and limbic systemrsquo (p 110) He even offers a speculation aboutits anatomical location ndash the prefrontal lobes (p 156)

This control system he says is lsquoopen in some degree to inuence by theenvironment in which development occursrsquo (p 45) More specically itevolves in the infantrsquos interaction with an lsquoenvironment of adaptiveness andespecially of his interaction with the principal gure in that environmentnamely his motherrsquo (p 180) Furthermore Bowlby speculates that thelsquoupgrading of control during individual development from simple to moresophisticated is no doubt in large part a result of the growth of the centralnervous systemrsquo (p 156) In fact he even goes so far as to suggest the tem-poral interval that is critical to the maturation of this control system ndash 9 to18 months (p 180)

In a subsequent chapter on lsquoAppraising and selecting Feeling andemotionrsquo Bowlby quotes Darwinrsquos (1872) observation that the movementsof expression in the face and body serve as the rst means of communicationbetween the mother and the infant Furthering this theme on the communi-cative role of feeling and emotion Bowlby emphasizes the salience of lsquofacialexpression posture tone of voice physiological changes tempo of move-ment and incipient actionrsquo (p 120) The appraisal of this input is experiencedlsquoin terms of value as pleasant or unpleasantrsquo (pp 111ndash112) and the

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 128

movements lsquomay be actively at work even when we are not aware of themrsquo(p 110) in this manner feeling provides a monitoring of both the behavioraland physiological state (p 121) Emotional processes thus he says lie at thefoundation of a model of instinctive behavior

In following chapters Bowlby concludes that the motherndashinfant attach-ment relation is lsquoaccompanied by the strongest of feelings and emotionshappy or the reversersquo (p 242) that the infantrsquos lsquocapacity to cope with stressrsquois correlated with certain maternal behaviors (p 344) and that the instinctivebehavior that emerges from the co-constructed environment of evolutionaryadaptiveness has consequences that are lsquovital to the survival of the speciesrsquo (p 137) He also suggests that the attachment system is readily activated untilthe end of the third year when the childrsquos capacity to cope with maternalseparation lsquoabruptlyrsquo improves due to the fact that lsquosome maturationalthreshold is passedrsquo (p 205)

CONTRIBUTIONS FROM NEUROSCIENCE TOATTACHM ENT THEORY

So the next question is 30 years after the appearance of this volume at theend of the lsquodecade of the brainrsquo how do Bowlbyrsquos original chartings of theattachment domain hold up In a word they were indeed prescient In facthis overall birdrsquos-eye perspective of the internal attachment landscape was socomprehensive that we now need to zoom in not just for close-up views ofthe essential brain structures that mediate attachment processes but also forvisualizations of how these structures dynamically self-organize within thedeveloping brain This includes neurobiological studies of Bowlbyrsquos controlsystem which I suggest may now be identied with the orbitofrontal cortexan area that has been called the lsquosenior executive of the emotional brainrsquo(Joseph 1996) and that has been shown to mediate lsquothe highest level ofcontrol of behavior especially in relation to emotionrsquo (Price Carmichael ampDrevets 1996 p 523) Keeping in mind Bowlbyrsquos previously presentedtheoretical descriptions the following is an extremely brief overview of agrowing body of studies on the neurobiology of attachment (For moreextensive expositions of these concepts and references see Schore 1994 19961997b 1998a 1999 in press a b c d e in preparation)

According to Ainsworth (1967 p 429) attachment is more than overtbehavior it is internal lsquobeing built into the nervous system in the course andas a result of the infantrsquos experience of his transactions with the motherrsquoFollowing Bowlbyrsquos suggestion the limbic system has been suggested to bethe site of developmental changes associated with the rise of attachmentbehaviors (Anders amp Zeanah 1984) Indeed the specic period from 7 to 15months has been shown to be critical for the myelination and therefore thematuration of particular rapidly developing limbic and cortical associationareas (Kinney Brody Kloman amp Gilles 1988) and limbic areas of the human

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 29

cerebral cortex show anatomical maturation at 15 months (Rabinowicz1979) In a number of works I offer evidence to show that attachment experi-ences face-to-face transactions of affect synchrony between caregiver andinfant directly inuence the imprinting the circuit wiring of the orbitalprefrontal cortex a corticolimbic area that is known to begin a major matu-rational change at 10 to 12 months and to complete a critical period of growthfrom the middle to the end of the second year This time-frame is identical toBowlbyrsquos maturation of an attachment control system that is open to in u-ence from the developmental environment

The co-created environment of evolutionary adaptiveness is thus isomor-phic to a growth-facilitating environment for the experience-dependent mat-uration of a regulatory system in the orbitofrontal cortex Indeed thisprefrontal system appraises visual facial information (Scalaidhe Wilson ampGoldman-Rakic 1997) and processes responses to pleasant touch tastesmell (Francis D et al 1999) and music (Blood Zatorre Bermudez ampEvans 1999) as well as to unpleasant images of angry and sad faces (BlairMorris Frith Perrett amp Dolan 1999) But this system is also involved in theregulation of the body state and reects changes taking place in that state(Luria 1980)

This frontolimbic system provides a high-level coding that exibly co-ordinates exteroceptive and interoceptive domains and functions to correctresponses as conditions change (Derryberry amp Tucker 1992) processes feed-back information (Elliott Frith amp Dolan 1997) and thereby monitorsadjusts and corrects emotional responses (Rolls 1986) and modulates themotivational control of goal-directed behavior (Tremblay amp Schultz 1999)So after a rapid evaluation of an environmental stimulus the orbitofrontalsystem monitors feedback about the current internal state in order to makeassessments of coping resources and it updates appropriate response outputsin order to make adaptive adjustments to particular environmental perturba-tions (Schore 1998a) In this manner lsquothe integrity of the orbitofrontal cortexis necessary for acquiring very specic forms of knowledge for regulatinginterpersonal behaviorrsquo (Dolan 1999 p 928)

These functions reect the unique anatomical properties of this area of thebrain Due to its location at the ventral and medial hemispheric surfaces itacts as a convergence zone where cortex and subcortex meet It is thus situ-ated at the apogee of the lsquorostral limbic systemrsquo a hierarchical sequence ofinterconnected limbic areas in orbitofrontal cortex insular cortex anteriorcingulate and amygdala (Schore 1997b in press a in preparation) Thelimbic system is now thought to be centrally involved in the implicit pro-cessing of facial expressions without conscious awareness (Critchley et al2000) and in the capacity lsquoto adapt to a rapidly changing environmentrsquo and inlsquothe organization of new learningrsquo (Mesulam 1998 p 1028) Emotionallyfocused limbic learning underlies the unique and fast-acting processes ofimprinting the learning mechanism associated with attachment as thisdynamic evolves over the rst and second years Hinde (1990 p 162) points

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 130

out that lsquothe development of social behavior can be understood only in termsof a continuing dialectic between an active and changing organism and anactive and changing environmentrsquo

But the orbitofrontal system is also deeply connected into the autonomicnervous system and the arousal-generating reticular formation and due tothe fact that it is the only cortical structure with such direct connections itcan regulate autonomic responses to social stimuli (Zald amp Kim 1996) andmodulate lsquoinstinctual behaviorrsquo (Starkstein amp Robinson 1997) The activityof this frontolimbic system is therefore critical to the modulation of socialand emotional behaviors and the homeostatic regulation of body and moti-vational states affect-regulating functions that are centrally involved inattachment processes The essential aspect of this function is highlighted byWestin (1997 p 542) who asserts that lsquoThe attempt to regulate affect ndash to min-imize unpleasant feelings and to maximize pleasant ones ndash is the driving forcein human motivationrsquo

The orbital prefrontal region is especially expanded in the right hemispherewhich is specialized for lsquoinhibitory controlrsquo (Garavan Ross amp Stein 1999)and it comes to act as an executive control function for the entire right brainThis hemisphere which is dominant for unconscious processes computes ona moment-to-moment basis the affective salience of external stimuli Keepingin mind Bowlbyrsquos earlier descriptions this lateralized system performs alsquovalence taggingrsquo function (Schore 1998a 1999) in which perceptions receivea positive or negative affective charge in accord with a calibration of degreesof pleasurendashunpleasure It also contains a lsquononverbal affect lexiconrsquo a vocabu-lary for nonverbal affective signals such as facial expressions gestures andvocal tone or prosody (Bowers Bauer amp Heilman 1993) The right hemi-sphere is thus faster than the left in performing valence-dependent automaticpre-attentive appraisal of emotional facial expressions (Pizzagalli Regard ampLehmann 1999)

Because the right cortical hemisphere more so than the left contains exten-sive reciprocal connections with limbic and subcortical regions (Tucker 1992Joseph 1996) it is dominant for the processing and expression of lsquoself-relatedmaterialrsquo (Keenan et al 1999) and emotional information and for regulatingpsychobiological states (Schore 1994 1998a 1999 Spence Shapiro amp Zaidel1996) Thus the right hemisphere is centrally involved in what Bowlbydescribed as the social and biological functions of the attachment system(Henry 1993 Schore 1994 Shapiro Jamner amp Spence 1997 Wang 1997Siegel 1999)

Conrming this model Ryan Kuhl and Deci (1997 p 719) using EEGand neuroimaging data conclude that lsquoThe positive emotional exchangeresulting from autonomy-supportive parenting involves participation ofright hemispheric cortical and subcortical systems that participate in globaltonic emotional modulationrsquo And in line with Bowlbyrsquos assertion thatattachment behavior is vital to the survival of the species it is now held thatthe right hemisphere is central to the control of vital functions supporting

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 31

survival and enabling the organism to cope with stresses and challenges(Wittling amp Schweiger 1993)

There is a growing body of studies which shows that the infantrsquos earlymaturing (Geschwind amp Galaburda 1987) right hemisphere is specicallyimpacted by early social experiences (Schore 1994 1998b) This develop-mental principle is now supported in a recent single photon emissioncomputed tomographic (SPECT) study by Chiron et al (1997) whichdemonstrates that the right brain hemisphere is dominant in preverbal humaninfants and indeed for the rst 3 years of life I suggest that the ontogeneticshift of dominance from the right to left hemisphere after this time may expli-cate Bowlbyrsquos description of a diminution of the attachment system at theend of the third year that is due to an lsquoabruptrsquo passage of a lsquomaturationalthresholdrsquo

Current neuropsychological studies indicate that lsquothe emotional experi-ence(s) of the infant are disproportionately stored or processed in theright hemisphere during the formative stages of brain ontogenyrsquo (Semrud-Clikeman amp Hynd 1990 p 198) that lsquothe infant relies primarily on its pro-cedural memory systemsrsquo during lsquothe rst 2ndash3 years of lifersquo (Kandel 1999 p 513) and that the right brain contains the lsquocerebral representation of onersquosown pastrsquo and the substrate of affectively laden autobiographical memory(Fink et al 1996 p 4275) These ndings suggest that early-forming inter-nal working models of the attachment relationship are processed and storedin implicit-procedural memory systems in the right cortex the hemispheredominant for implicit learning (Hugdahl 1995)

In the securely attached individual these models encode an expectationthat lsquohomeostatic disruptions will be set rightrsquo (Pipp amp Harmon 1987 p 650) In discussing these internal models Rutter (1987) notes that lsquochildrenderive a set of expectations about their own relationship capacities and aboutother peoplersquos resources to their social overtures and interactions theseexpectations being created on the basis of their early parentndashchild attach-mentsrsquo (p 449) Such representations are processed by the orbitofrontalsystem which is known to be activated during lsquobreaches of expectationrsquo(Nobre Coull Frith amp Mesulam 1999) and to generate affect-regulatingstrategies for coping with expected negative and positive emotional states thatare inherent in intimate social contexts

The efcient operations of this regulatory system allow for corticallyprocessed information concerning the external environment (such as visualand auditory stimuli emanating from the emotional face of the attachmentobject) to be integrated with subcortically processed information regardingthe internal visceral environment (such as concurrent changes in the childrsquosemotional or bodily self-state) The relaying of sensory information into thelimbic system allows incoming information about the social environment totrigger adjustments in emotional and motivational states and in this mannerthe orbitofrontal system integrates what Bowlby termed environmental andorganismic models Recent ndings that the orbitofrontal cortex generates

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 132

nonconscious biases that guide behavior before conscious knowledge does(Bechara Damasio Tranel amp Damasio 1997) and codes the likely signicanceof future behavioral options (Dolan 1999) and represents an important siteof contact between emotional information and mechanisms of action selec-tion (Rolls 1996) are consonant with Bowlbyrsquos (1981) assertion that internalworking models are used as guides for future action

These mental representations according to Main Kaplan and Cassidy(1985) contain cognitive as well as affective components and act to guideappraisals of experience The orbitofrontal cortex is known to function as anappraisal mechanism (Pribram 1987 Schore 1998a) and to be centrallyinvolved in the generation of lsquocognitive-emotional interactionsrsquo (Barbas1995) It acts to lsquointegrate and assign emotional-motivational signicance tocognitive impressions the association of emotion with ideas and thoughtsrsquo(Joseph 1996 p 427) and in lsquothe processing of affect-related meaningsrsquo (Teas-dale et al 1999)

Orbitofrontal activity is associated with a lower threshold for awarenessof sensations of both external and internal origin (Goldenberg et al 1989)thereby enabling it to act as an lsquointernal re ecting and organizing agencyrsquo(Kaplan-Solms amp Solms 1996) This orbitofrontal role in lsquoself-re ectiveawarenessrsquo (Stuss Gow amp Hetherington 1992) allows an individual to reecton his or her own internal emotional states as well as those of others(Povinelli amp Preuss 1995) According to Fonagy and Target (1997) the reec-tive function is a mental operation that enables the perception of anotherrsquosstate The right hemisphere mediates empathic cognition and the perceptionof the emotional states of other human beings (Voeller 1986) andorbitofrontal function is essential to the capacity of inferring the states ofothers (Baron-Cohen 1995) This adaptive capacity may thus be the outcomeof a secure attachment to a psychobiologically attuned affect-regulating care-giver A recent neuropsychological study indicates that the orbitofrontalcortex is lsquoparticularly involved in theory of mind tasks with an affective com-ponentrsquo (Stone Baron-Cohen amp Knight 1998 p 651)

Furthermore the functioning of the orbitofrontal control system in theregulation of emotion (Baker Frith amp Dolan 1997) and in lsquoacquiring veryspecic forms of knowledge for regulating interpersonal and social behaviorrsquo(Dolan 1999 p 928) is central to self-regulation the ability to exibly regu-late emotional states through interactions with other humans ndash that is inter-active regulation in interconnected contexts ndash and without other humans ndashthat is autoregulation in autonomous contexts The adaptive capacity to shiftbetween these dual regulatory modes depending upon the social contextemerges out of a history of secure attachment interactions of a maturing bio-logical organism and an early attuned social environment

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 33

ATTACH MENT THEORY IS FUNDAMENTALLYA REGULATORY THEORY

Attachment behavior is currently thought to be the output of lsquoa neuro-biologically based biobehavioral system that regulates biological syn-chronicity between organismsrsquo (Wang 1997 p 168) I suggest that thecharacterization of the orbitofrontal system as a frontolimbic structure thatdetermines the regulatory signi cance of stimuli that reach the organism andregulates body state (Luria 1980) bears a striking resemblance to the behav-ioral control system characterized by Bowlby over 30 years ago The OxfordDictionary denes control as lsquothe act or power of directing or regulatingrsquo

Attachment theory as rst propounded in Bowlbyrsquos (1969) denitionalvolume is fundamentally a regulatory theory Attachment can thus be con-ceptualized as the interactive regulation of synchrony between psychobiolog-ically attuned organisms This attachment dynamic which operates at levelsbeneath awareness underlies the dyadic regulation of emotion Emotions arethe highest order direct expression of bioregulation in complex organisms(Damasio 1998) Imprinting the learning process it accesses is described byPetrovich and Gewirtz (1985) as synchrony between sequential infant mater-nal stimuli and behavior (see Schore 1994 and Nelson amp Panksepp 1998 formodels of the neurochemistry of attachment)

According to Feldman et al (1999) lsquoface-to-face synchrony affords infantstheir rst opportunity to practice interpersonal coordination of biologicalrhythmsrsquo (p 223) and acts as an interpersonal context in which lsquointeractantsintegrate into the ow of behavior the ongoing responses of their partner andthe changing inputs of the environmentrsquo (p 224) The visual prosodic-auditory and gestural stimuli embedded in these emotional communicationsare rapidly transmitted back and forth between the infantrsquos and motherrsquos faceand in these transactions the caregiver acts as a regulator of the childrsquos arousallevels

Because arousal levels are known to be associated with changes in meta-bolic energy the caregiver is thus modulating changes in the childrsquos energeticstate (Schore 1994 1997b) These regulated increases in energy metabolismare available for biosynthetic processes in the babyrsquos brain which is in thebrain growth spurt (Dobbing amp Sands 1973) In this manner lsquothe intrinsicregulators of human brain growth in a child are specically adapted to becoupled by emotional communication to the regulators of adult brainsrsquo(Trevarthen 1990 p 357)

In addition the mother also regulates moments of asynchrony that isstressful negative affect Social stressors can be characterized as the occur-rence of an asynchrony in an interactional sequence (Chapple 1970) Stressdescribes both the subjective experience induced by a distressing potentiallythreatening or novel situation and the organismrsquos reactions to a homeosta-tic challenge It is now thought that social stressors are lsquofar more detrimen-talrsquo than non-social aversive stimuli (Sgoifo et al 1999)

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 134

Separation stress in essence is a loss of maternal regulators of the infantrsquosimmature behavioral and physiological systems that results in the attachmentpatterns of protest despair and detachment The principle that lsquoa period ofsynchrony following the period of stress provides a ldquorecoveryrdquo periodrsquo(Chapple 1970 p 631) underlies the mechanism of interactive repair(Tronick 1989 Schore 1994) The primary caregiverrsquos interactive regulationis therefore critical to the infantrsquos maintaining positively charged as well ascoping with stressful negatively charged affects These affect regulatingevents are particularly impacting the organization of the early developingright hemisphere

Bowlbyrsquos control system is located in the right hemisphere that is not onlydominant for lsquoinhibitory controlrsquo (Garavan et al 1999) but also for the pro-cessing of facial information in infants (Deruelle amp de Schonen 1998) andadults (Kim et al 1999) and for the regulation of arousal (Heilman amp VanDen Abell 1979) Because the major coping systems the hypothalamo-pituitary-adrenocortical axis and the sympathetic-adrenomedullary axis areboth under the main control of the right cerebral cortex this hemisphere con-tains lsquoa unique response system preparing the organism to deal efcientlywith external challengesrsquo and so its adaptive functions mediate the humanstress response (Wittling 1997 p 55) Basic research in stress physiologyshows that the behavioral and physiological response of an individual to aspecic stressor is consistent over time (Koolhaas et al 1999)

These attachment transactions are imprinted into implicit-proceduralmemory as enduring internal working models which encode coping strat-egies of affect regulation (Schore 1994) that maintain basic regulation andpositive affect even in the face of environmental challenge (Sroufe 1989)Attachment patterns are now conceptualized as lsquopatterns of mental process-ing of information based on cognition and affect to create models of realityrsquo(Crittenden 1995 p 401) The lsquoanterior limbic prefrontal networkrsquo whichinterconnects the orbital and medial prefrontal cortex with the temporal polecingulate and amygdala lsquois involved in affective responses to events and inthe mnemonic processing and storage of these responsesrsquo (Carmichael ampPrice 1995 p 639) and lsquoconstitutes a mental control system that is essentialfor adjusting thinking and behavior to ongoing realityrsquo (Schnider amp Ptak1999 p 680) An ultimate indicator of secure attachment is resilience in theface of stress (Greenspan 1981) which is expressed in the capacity to ex-ibly regulate emotional states via autoregulation and interactive regulationHowever early social environments that engender insecure attachmentsinhibit the growth of this control system (Schore 1997b) and therefore pre-clude its adaptive coping function in lsquooperations linked to behavioral exi-bilityrsquo (Nobre et al 1999 p 12)

In support of Bowlbyrsquos assertion that the childrsquos capacity to cope withstress is correlated with certain maternal behaviors current developmentalbiological studies are exploring lsquomaternal effectsrsquo the inuence of themotherrsquos experiences on her progenyrsquos development and ability to adapt to

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 35

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

Milgrom-Friedman 1983) Reite and Capitanio (1985) conceptualize affect aslsquoa manifestation of underlying modulating or motivational systems subserv-ing or facilitating social attachmentsrsquo (p 248) and suggest that an essentialattachment function is lsquoto promote the synchrony or regulation of biologicaland behavioral systems on an organismic levelrsquo (p 235) In these rapid regu-lated face-to-face transactions the psychobiologically attuned (Field 1985)caregiver not only minimizes the infantrsquos negative but also maximizes its posi-tive affective states (Schore 1994 1996 1998b) This proximate interpersonalcontext of lsquoaffect synchronyrsquo (Feldman Greenbaum amp Yirmiya 1999) andinterpersonal resonance (Schore 1997b in press b) represents the externalrealm of attachment dynamics

But due to his interests in the inner world Bowlby here presents a modelof events occurring within the internal realm of attachment processes Andso he offers his initial speculations about how the developing child constructsinternal working models lsquoof how the physical world may be expected tobehave how his mother and other signicant persons may be expected tobehave how he himself may be expected to behave and how each interactswith the otherrsquo (p 354) This initial concept has currently evolved intolsquoprocess-orientedrsquo conceptions of internal working models as representationsthat regulate an individualrsquos relationship adaptation through interpre-tiveattributional processes (Bretherton amp Munholland 1999) and encodestrategies of affect regulation (Kobak amp Sceery 1988 Schore 1994) Currentpsychobiological models refer to representations of the infantrsquos affective dia-logue with the mother which can be accessed to regulate its affective state(Polan amp Hofer 1999)

Interestingly Bowlby also describes internal working models in the rstpart of the volume the eight chapters devoted to lsquoinstinctive behaviorrsquo Irepeat my assertion that a deeper explication of the fundamental themes ofthis section of the book represents the frontier of attachment theory andresearch In these opening chapters the aggregate of which represents thefoundation on which the later chapters on attachment are built Bowlbyposits that internal models function as lsquocognitive mapsrsquo in the brain and areaccessed lsquoto transmit store and manipulate information that helps makingpredictions as to how set-goals (of attachment) can be achievedrsquo (p 80)Furthermore he states that lsquothe two working models each individual musthave are referred to respectively as his environmental model and his organ-ismic modelrsquo (p 82) This is because lsquosensory data regarding events reachingan organism via its sense organs are immediately assessed regulated andinterpreted The same is true of sensory data derived from the internal stateof the organismrsquo (p 109) Here Bowlby is pointing to the need for a develop-mental theoretical conception of attachment that can tie together psychologyand biology mind and body

And so at the very onset of his essay he begins lsquoThe taskrsquo by describinga theoretical landscape that includes both the biological and social aspectsof attachment a terrain that must be described in terms of its structural

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 27

organization as well as its functional properties Following the generalperspective of all biological investigators he attempts to elucidate thestructurendashfunction relationships of a living system but with the added per-spective of developmental biology he is specically focusing on the early criti-cal stages within which the system rst self-organizes Thus the form of thebook is rst to outline the general characteristics of the internal structuralsystem and then to describe this systemrsquos central functional role in attachmentprocesses

Bowlby begins the third chapter by quoting Freudrsquos (1925) dictum thatlsquoThere is no more urgent need in psychology than for a securely foundedtheory of the instinctsrsquo The attempt to do so in this book an offering of anlsquoalternative model of instinctive behaviorrsquo in essence represents Bowlbyrsquosconviction that what Freud was calling for was the creation of a model thatcould explicate the biology of unconscious processes Towards that end inthe rst of eight chapters on the topic he proposes that attachment is instinc-tive behavior associated with self-preservation and that it is a product of theinteraction between genetic endowment and the early environment

But immediately after a brief 5-page introduction Bowlby launches into adetailed description of a biological control system that is centrally involvedin instinctive behavior This control system is structured as a hierarchicalmode of organization that acts as lsquoan overall goal-corrected behavioral struc-turersquo Bowlby also gives some hints as to the neurobiological operations ofthis control system ndash its functions must be associated with the organismrsquoslsquostate of arousalrsquo that results from the critical operations of the reticular for-mation and with lsquothe appraisal of organismic states and situations of the mid-brain nuclei and limbic systemrsquo (p 110) He even offers a speculation aboutits anatomical location ndash the prefrontal lobes (p 156)

This control system he says is lsquoopen in some degree to inuence by theenvironment in which development occursrsquo (p 45) More specically itevolves in the infantrsquos interaction with an lsquoenvironment of adaptiveness andespecially of his interaction with the principal gure in that environmentnamely his motherrsquo (p 180) Furthermore Bowlby speculates that thelsquoupgrading of control during individual development from simple to moresophisticated is no doubt in large part a result of the growth of the centralnervous systemrsquo (p 156) In fact he even goes so far as to suggest the tem-poral interval that is critical to the maturation of this control system ndash 9 to18 months (p 180)

In a subsequent chapter on lsquoAppraising and selecting Feeling andemotionrsquo Bowlby quotes Darwinrsquos (1872) observation that the movementsof expression in the face and body serve as the rst means of communicationbetween the mother and the infant Furthering this theme on the communi-cative role of feeling and emotion Bowlby emphasizes the salience of lsquofacialexpression posture tone of voice physiological changes tempo of move-ment and incipient actionrsquo (p 120) The appraisal of this input is experiencedlsquoin terms of value as pleasant or unpleasantrsquo (pp 111ndash112) and the

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 128

movements lsquomay be actively at work even when we are not aware of themrsquo(p 110) in this manner feeling provides a monitoring of both the behavioraland physiological state (p 121) Emotional processes thus he says lie at thefoundation of a model of instinctive behavior

In following chapters Bowlby concludes that the motherndashinfant attach-ment relation is lsquoaccompanied by the strongest of feelings and emotionshappy or the reversersquo (p 242) that the infantrsquos lsquocapacity to cope with stressrsquois correlated with certain maternal behaviors (p 344) and that the instinctivebehavior that emerges from the co-constructed environment of evolutionaryadaptiveness has consequences that are lsquovital to the survival of the speciesrsquo (p 137) He also suggests that the attachment system is readily activated untilthe end of the third year when the childrsquos capacity to cope with maternalseparation lsquoabruptlyrsquo improves due to the fact that lsquosome maturationalthreshold is passedrsquo (p 205)

CONTRIBUTIONS FROM NEUROSCIENCE TOATTACHM ENT THEORY

So the next question is 30 years after the appearance of this volume at theend of the lsquodecade of the brainrsquo how do Bowlbyrsquos original chartings of theattachment domain hold up In a word they were indeed prescient In facthis overall birdrsquos-eye perspective of the internal attachment landscape was socomprehensive that we now need to zoom in not just for close-up views ofthe essential brain structures that mediate attachment processes but also forvisualizations of how these structures dynamically self-organize within thedeveloping brain This includes neurobiological studies of Bowlbyrsquos controlsystem which I suggest may now be identied with the orbitofrontal cortexan area that has been called the lsquosenior executive of the emotional brainrsquo(Joseph 1996) and that has been shown to mediate lsquothe highest level ofcontrol of behavior especially in relation to emotionrsquo (Price Carmichael ampDrevets 1996 p 523) Keeping in mind Bowlbyrsquos previously presentedtheoretical descriptions the following is an extremely brief overview of agrowing body of studies on the neurobiology of attachment (For moreextensive expositions of these concepts and references see Schore 1994 19961997b 1998a 1999 in press a b c d e in preparation)

According to Ainsworth (1967 p 429) attachment is more than overtbehavior it is internal lsquobeing built into the nervous system in the course andas a result of the infantrsquos experience of his transactions with the motherrsquoFollowing Bowlbyrsquos suggestion the limbic system has been suggested to bethe site of developmental changes associated with the rise of attachmentbehaviors (Anders amp Zeanah 1984) Indeed the specic period from 7 to 15months has been shown to be critical for the myelination and therefore thematuration of particular rapidly developing limbic and cortical associationareas (Kinney Brody Kloman amp Gilles 1988) and limbic areas of the human

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 29

cerebral cortex show anatomical maturation at 15 months (Rabinowicz1979) In a number of works I offer evidence to show that attachment experi-ences face-to-face transactions of affect synchrony between caregiver andinfant directly inuence the imprinting the circuit wiring of the orbitalprefrontal cortex a corticolimbic area that is known to begin a major matu-rational change at 10 to 12 months and to complete a critical period of growthfrom the middle to the end of the second year This time-frame is identical toBowlbyrsquos maturation of an attachment control system that is open to in u-ence from the developmental environment

The co-created environment of evolutionary adaptiveness is thus isomor-phic to a growth-facilitating environment for the experience-dependent mat-uration of a regulatory system in the orbitofrontal cortex Indeed thisprefrontal system appraises visual facial information (Scalaidhe Wilson ampGoldman-Rakic 1997) and processes responses to pleasant touch tastesmell (Francis D et al 1999) and music (Blood Zatorre Bermudez ampEvans 1999) as well as to unpleasant images of angry and sad faces (BlairMorris Frith Perrett amp Dolan 1999) But this system is also involved in theregulation of the body state and reects changes taking place in that state(Luria 1980)

This frontolimbic system provides a high-level coding that exibly co-ordinates exteroceptive and interoceptive domains and functions to correctresponses as conditions change (Derryberry amp Tucker 1992) processes feed-back information (Elliott Frith amp Dolan 1997) and thereby monitorsadjusts and corrects emotional responses (Rolls 1986) and modulates themotivational control of goal-directed behavior (Tremblay amp Schultz 1999)So after a rapid evaluation of an environmental stimulus the orbitofrontalsystem monitors feedback about the current internal state in order to makeassessments of coping resources and it updates appropriate response outputsin order to make adaptive adjustments to particular environmental perturba-tions (Schore 1998a) In this manner lsquothe integrity of the orbitofrontal cortexis necessary for acquiring very specic forms of knowledge for regulatinginterpersonal behaviorrsquo (Dolan 1999 p 928)

These functions reect the unique anatomical properties of this area of thebrain Due to its location at the ventral and medial hemispheric surfaces itacts as a convergence zone where cortex and subcortex meet It is thus situ-ated at the apogee of the lsquorostral limbic systemrsquo a hierarchical sequence ofinterconnected limbic areas in orbitofrontal cortex insular cortex anteriorcingulate and amygdala (Schore 1997b in press a in preparation) Thelimbic system is now thought to be centrally involved in the implicit pro-cessing of facial expressions without conscious awareness (Critchley et al2000) and in the capacity lsquoto adapt to a rapidly changing environmentrsquo and inlsquothe organization of new learningrsquo (Mesulam 1998 p 1028) Emotionallyfocused limbic learning underlies the unique and fast-acting processes ofimprinting the learning mechanism associated with attachment as thisdynamic evolves over the rst and second years Hinde (1990 p 162) points

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 130

out that lsquothe development of social behavior can be understood only in termsof a continuing dialectic between an active and changing organism and anactive and changing environmentrsquo

But the orbitofrontal system is also deeply connected into the autonomicnervous system and the arousal-generating reticular formation and due tothe fact that it is the only cortical structure with such direct connections itcan regulate autonomic responses to social stimuli (Zald amp Kim 1996) andmodulate lsquoinstinctual behaviorrsquo (Starkstein amp Robinson 1997) The activityof this frontolimbic system is therefore critical to the modulation of socialand emotional behaviors and the homeostatic regulation of body and moti-vational states affect-regulating functions that are centrally involved inattachment processes The essential aspect of this function is highlighted byWestin (1997 p 542) who asserts that lsquoThe attempt to regulate affect ndash to min-imize unpleasant feelings and to maximize pleasant ones ndash is the driving forcein human motivationrsquo

The orbital prefrontal region is especially expanded in the right hemispherewhich is specialized for lsquoinhibitory controlrsquo (Garavan Ross amp Stein 1999)and it comes to act as an executive control function for the entire right brainThis hemisphere which is dominant for unconscious processes computes ona moment-to-moment basis the affective salience of external stimuli Keepingin mind Bowlbyrsquos earlier descriptions this lateralized system performs alsquovalence taggingrsquo function (Schore 1998a 1999) in which perceptions receivea positive or negative affective charge in accord with a calibration of degreesof pleasurendashunpleasure It also contains a lsquononverbal affect lexiconrsquo a vocabu-lary for nonverbal affective signals such as facial expressions gestures andvocal tone or prosody (Bowers Bauer amp Heilman 1993) The right hemi-sphere is thus faster than the left in performing valence-dependent automaticpre-attentive appraisal of emotional facial expressions (Pizzagalli Regard ampLehmann 1999)

Because the right cortical hemisphere more so than the left contains exten-sive reciprocal connections with limbic and subcortical regions (Tucker 1992Joseph 1996) it is dominant for the processing and expression of lsquoself-relatedmaterialrsquo (Keenan et al 1999) and emotional information and for regulatingpsychobiological states (Schore 1994 1998a 1999 Spence Shapiro amp Zaidel1996) Thus the right hemisphere is centrally involved in what Bowlbydescribed as the social and biological functions of the attachment system(Henry 1993 Schore 1994 Shapiro Jamner amp Spence 1997 Wang 1997Siegel 1999)

Conrming this model Ryan Kuhl and Deci (1997 p 719) using EEGand neuroimaging data conclude that lsquoThe positive emotional exchangeresulting from autonomy-supportive parenting involves participation ofright hemispheric cortical and subcortical systems that participate in globaltonic emotional modulationrsquo And in line with Bowlbyrsquos assertion thatattachment behavior is vital to the survival of the species it is now held thatthe right hemisphere is central to the control of vital functions supporting

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 31

survival and enabling the organism to cope with stresses and challenges(Wittling amp Schweiger 1993)

There is a growing body of studies which shows that the infantrsquos earlymaturing (Geschwind amp Galaburda 1987) right hemisphere is specicallyimpacted by early social experiences (Schore 1994 1998b) This develop-mental principle is now supported in a recent single photon emissioncomputed tomographic (SPECT) study by Chiron et al (1997) whichdemonstrates that the right brain hemisphere is dominant in preverbal humaninfants and indeed for the rst 3 years of life I suggest that the ontogeneticshift of dominance from the right to left hemisphere after this time may expli-cate Bowlbyrsquos description of a diminution of the attachment system at theend of the third year that is due to an lsquoabruptrsquo passage of a lsquomaturationalthresholdrsquo

Current neuropsychological studies indicate that lsquothe emotional experi-ence(s) of the infant are disproportionately stored or processed in theright hemisphere during the formative stages of brain ontogenyrsquo (Semrud-Clikeman amp Hynd 1990 p 198) that lsquothe infant relies primarily on its pro-cedural memory systemsrsquo during lsquothe rst 2ndash3 years of lifersquo (Kandel 1999 p 513) and that the right brain contains the lsquocerebral representation of onersquosown pastrsquo and the substrate of affectively laden autobiographical memory(Fink et al 1996 p 4275) These ndings suggest that early-forming inter-nal working models of the attachment relationship are processed and storedin implicit-procedural memory systems in the right cortex the hemispheredominant for implicit learning (Hugdahl 1995)

In the securely attached individual these models encode an expectationthat lsquohomeostatic disruptions will be set rightrsquo (Pipp amp Harmon 1987 p 650) In discussing these internal models Rutter (1987) notes that lsquochildrenderive a set of expectations about their own relationship capacities and aboutother peoplersquos resources to their social overtures and interactions theseexpectations being created on the basis of their early parentndashchild attach-mentsrsquo (p 449) Such representations are processed by the orbitofrontalsystem which is known to be activated during lsquobreaches of expectationrsquo(Nobre Coull Frith amp Mesulam 1999) and to generate affect-regulatingstrategies for coping with expected negative and positive emotional states thatare inherent in intimate social contexts

The efcient operations of this regulatory system allow for corticallyprocessed information concerning the external environment (such as visualand auditory stimuli emanating from the emotional face of the attachmentobject) to be integrated with subcortically processed information regardingthe internal visceral environment (such as concurrent changes in the childrsquosemotional or bodily self-state) The relaying of sensory information into thelimbic system allows incoming information about the social environment totrigger adjustments in emotional and motivational states and in this mannerthe orbitofrontal system integrates what Bowlby termed environmental andorganismic models Recent ndings that the orbitofrontal cortex generates

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 132

nonconscious biases that guide behavior before conscious knowledge does(Bechara Damasio Tranel amp Damasio 1997) and codes the likely signicanceof future behavioral options (Dolan 1999) and represents an important siteof contact between emotional information and mechanisms of action selec-tion (Rolls 1996) are consonant with Bowlbyrsquos (1981) assertion that internalworking models are used as guides for future action

These mental representations according to Main Kaplan and Cassidy(1985) contain cognitive as well as affective components and act to guideappraisals of experience The orbitofrontal cortex is known to function as anappraisal mechanism (Pribram 1987 Schore 1998a) and to be centrallyinvolved in the generation of lsquocognitive-emotional interactionsrsquo (Barbas1995) It acts to lsquointegrate and assign emotional-motivational signicance tocognitive impressions the association of emotion with ideas and thoughtsrsquo(Joseph 1996 p 427) and in lsquothe processing of affect-related meaningsrsquo (Teas-dale et al 1999)

Orbitofrontal activity is associated with a lower threshold for awarenessof sensations of both external and internal origin (Goldenberg et al 1989)thereby enabling it to act as an lsquointernal re ecting and organizing agencyrsquo(Kaplan-Solms amp Solms 1996) This orbitofrontal role in lsquoself-re ectiveawarenessrsquo (Stuss Gow amp Hetherington 1992) allows an individual to reecton his or her own internal emotional states as well as those of others(Povinelli amp Preuss 1995) According to Fonagy and Target (1997) the reec-tive function is a mental operation that enables the perception of anotherrsquosstate The right hemisphere mediates empathic cognition and the perceptionof the emotional states of other human beings (Voeller 1986) andorbitofrontal function is essential to the capacity of inferring the states ofothers (Baron-Cohen 1995) This adaptive capacity may thus be the outcomeof a secure attachment to a psychobiologically attuned affect-regulating care-giver A recent neuropsychological study indicates that the orbitofrontalcortex is lsquoparticularly involved in theory of mind tasks with an affective com-ponentrsquo (Stone Baron-Cohen amp Knight 1998 p 651)

Furthermore the functioning of the orbitofrontal control system in theregulation of emotion (Baker Frith amp Dolan 1997) and in lsquoacquiring veryspecic forms of knowledge for regulating interpersonal and social behaviorrsquo(Dolan 1999 p 928) is central to self-regulation the ability to exibly regu-late emotional states through interactions with other humans ndash that is inter-active regulation in interconnected contexts ndash and without other humans ndashthat is autoregulation in autonomous contexts The adaptive capacity to shiftbetween these dual regulatory modes depending upon the social contextemerges out of a history of secure attachment interactions of a maturing bio-logical organism and an early attuned social environment

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 33

ATTACH MENT THEORY IS FUNDAMENTALLYA REGULATORY THEORY

Attachment behavior is currently thought to be the output of lsquoa neuro-biologically based biobehavioral system that regulates biological syn-chronicity between organismsrsquo (Wang 1997 p 168) I suggest that thecharacterization of the orbitofrontal system as a frontolimbic structure thatdetermines the regulatory signi cance of stimuli that reach the organism andregulates body state (Luria 1980) bears a striking resemblance to the behav-ioral control system characterized by Bowlby over 30 years ago The OxfordDictionary denes control as lsquothe act or power of directing or regulatingrsquo

Attachment theory as rst propounded in Bowlbyrsquos (1969) denitionalvolume is fundamentally a regulatory theory Attachment can thus be con-ceptualized as the interactive regulation of synchrony between psychobiolog-ically attuned organisms This attachment dynamic which operates at levelsbeneath awareness underlies the dyadic regulation of emotion Emotions arethe highest order direct expression of bioregulation in complex organisms(Damasio 1998) Imprinting the learning process it accesses is described byPetrovich and Gewirtz (1985) as synchrony between sequential infant mater-nal stimuli and behavior (see Schore 1994 and Nelson amp Panksepp 1998 formodels of the neurochemistry of attachment)

According to Feldman et al (1999) lsquoface-to-face synchrony affords infantstheir rst opportunity to practice interpersonal coordination of biologicalrhythmsrsquo (p 223) and acts as an interpersonal context in which lsquointeractantsintegrate into the ow of behavior the ongoing responses of their partner andthe changing inputs of the environmentrsquo (p 224) The visual prosodic-auditory and gestural stimuli embedded in these emotional communicationsare rapidly transmitted back and forth between the infantrsquos and motherrsquos faceand in these transactions the caregiver acts as a regulator of the childrsquos arousallevels

Because arousal levels are known to be associated with changes in meta-bolic energy the caregiver is thus modulating changes in the childrsquos energeticstate (Schore 1994 1997b) These regulated increases in energy metabolismare available for biosynthetic processes in the babyrsquos brain which is in thebrain growth spurt (Dobbing amp Sands 1973) In this manner lsquothe intrinsicregulators of human brain growth in a child are specically adapted to becoupled by emotional communication to the regulators of adult brainsrsquo(Trevarthen 1990 p 357)

In addition the mother also regulates moments of asynchrony that isstressful negative affect Social stressors can be characterized as the occur-rence of an asynchrony in an interactional sequence (Chapple 1970) Stressdescribes both the subjective experience induced by a distressing potentiallythreatening or novel situation and the organismrsquos reactions to a homeosta-tic challenge It is now thought that social stressors are lsquofar more detrimen-talrsquo than non-social aversive stimuli (Sgoifo et al 1999)

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 134

Separation stress in essence is a loss of maternal regulators of the infantrsquosimmature behavioral and physiological systems that results in the attachmentpatterns of protest despair and detachment The principle that lsquoa period ofsynchrony following the period of stress provides a ldquorecoveryrdquo periodrsquo(Chapple 1970 p 631) underlies the mechanism of interactive repair(Tronick 1989 Schore 1994) The primary caregiverrsquos interactive regulationis therefore critical to the infantrsquos maintaining positively charged as well ascoping with stressful negatively charged affects These affect regulatingevents are particularly impacting the organization of the early developingright hemisphere

Bowlbyrsquos control system is located in the right hemisphere that is not onlydominant for lsquoinhibitory controlrsquo (Garavan et al 1999) but also for the pro-cessing of facial information in infants (Deruelle amp de Schonen 1998) andadults (Kim et al 1999) and for the regulation of arousal (Heilman amp VanDen Abell 1979) Because the major coping systems the hypothalamo-pituitary-adrenocortical axis and the sympathetic-adrenomedullary axis areboth under the main control of the right cerebral cortex this hemisphere con-tains lsquoa unique response system preparing the organism to deal efcientlywith external challengesrsquo and so its adaptive functions mediate the humanstress response (Wittling 1997 p 55) Basic research in stress physiologyshows that the behavioral and physiological response of an individual to aspecic stressor is consistent over time (Koolhaas et al 1999)

These attachment transactions are imprinted into implicit-proceduralmemory as enduring internal working models which encode coping strat-egies of affect regulation (Schore 1994) that maintain basic regulation andpositive affect even in the face of environmental challenge (Sroufe 1989)Attachment patterns are now conceptualized as lsquopatterns of mental process-ing of information based on cognition and affect to create models of realityrsquo(Crittenden 1995 p 401) The lsquoanterior limbic prefrontal networkrsquo whichinterconnects the orbital and medial prefrontal cortex with the temporal polecingulate and amygdala lsquois involved in affective responses to events and inthe mnemonic processing and storage of these responsesrsquo (Carmichael ampPrice 1995 p 639) and lsquoconstitutes a mental control system that is essentialfor adjusting thinking and behavior to ongoing realityrsquo (Schnider amp Ptak1999 p 680) An ultimate indicator of secure attachment is resilience in theface of stress (Greenspan 1981) which is expressed in the capacity to ex-ibly regulate emotional states via autoregulation and interactive regulationHowever early social environments that engender insecure attachmentsinhibit the growth of this control system (Schore 1997b) and therefore pre-clude its adaptive coping function in lsquooperations linked to behavioral exi-bilityrsquo (Nobre et al 1999 p 12)

In support of Bowlbyrsquos assertion that the childrsquos capacity to cope withstress is correlated with certain maternal behaviors current developmentalbiological studies are exploring lsquomaternal effectsrsquo the inuence of themotherrsquos experiences on her progenyrsquos development and ability to adapt to

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 35

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

organization as well as its functional properties Following the generalperspective of all biological investigators he attempts to elucidate thestructurendashfunction relationships of a living system but with the added per-spective of developmental biology he is specically focusing on the early criti-cal stages within which the system rst self-organizes Thus the form of thebook is rst to outline the general characteristics of the internal structuralsystem and then to describe this systemrsquos central functional role in attachmentprocesses

Bowlby begins the third chapter by quoting Freudrsquos (1925) dictum thatlsquoThere is no more urgent need in psychology than for a securely foundedtheory of the instinctsrsquo The attempt to do so in this book an offering of anlsquoalternative model of instinctive behaviorrsquo in essence represents Bowlbyrsquosconviction that what Freud was calling for was the creation of a model thatcould explicate the biology of unconscious processes Towards that end inthe rst of eight chapters on the topic he proposes that attachment is instinc-tive behavior associated with self-preservation and that it is a product of theinteraction between genetic endowment and the early environment

But immediately after a brief 5-page introduction Bowlby launches into adetailed description of a biological control system that is centrally involvedin instinctive behavior This control system is structured as a hierarchicalmode of organization that acts as lsquoan overall goal-corrected behavioral struc-turersquo Bowlby also gives some hints as to the neurobiological operations ofthis control system ndash its functions must be associated with the organismrsquoslsquostate of arousalrsquo that results from the critical operations of the reticular for-mation and with lsquothe appraisal of organismic states and situations of the mid-brain nuclei and limbic systemrsquo (p 110) He even offers a speculation aboutits anatomical location ndash the prefrontal lobes (p 156)

This control system he says is lsquoopen in some degree to inuence by theenvironment in which development occursrsquo (p 45) More specically itevolves in the infantrsquos interaction with an lsquoenvironment of adaptiveness andespecially of his interaction with the principal gure in that environmentnamely his motherrsquo (p 180) Furthermore Bowlby speculates that thelsquoupgrading of control during individual development from simple to moresophisticated is no doubt in large part a result of the growth of the centralnervous systemrsquo (p 156) In fact he even goes so far as to suggest the tem-poral interval that is critical to the maturation of this control system ndash 9 to18 months (p 180)

In a subsequent chapter on lsquoAppraising and selecting Feeling andemotionrsquo Bowlby quotes Darwinrsquos (1872) observation that the movementsof expression in the face and body serve as the rst means of communicationbetween the mother and the infant Furthering this theme on the communi-cative role of feeling and emotion Bowlby emphasizes the salience of lsquofacialexpression posture tone of voice physiological changes tempo of move-ment and incipient actionrsquo (p 120) The appraisal of this input is experiencedlsquoin terms of value as pleasant or unpleasantrsquo (pp 111ndash112) and the

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 128

movements lsquomay be actively at work even when we are not aware of themrsquo(p 110) in this manner feeling provides a monitoring of both the behavioraland physiological state (p 121) Emotional processes thus he says lie at thefoundation of a model of instinctive behavior

In following chapters Bowlby concludes that the motherndashinfant attach-ment relation is lsquoaccompanied by the strongest of feelings and emotionshappy or the reversersquo (p 242) that the infantrsquos lsquocapacity to cope with stressrsquois correlated with certain maternal behaviors (p 344) and that the instinctivebehavior that emerges from the co-constructed environment of evolutionaryadaptiveness has consequences that are lsquovital to the survival of the speciesrsquo (p 137) He also suggests that the attachment system is readily activated untilthe end of the third year when the childrsquos capacity to cope with maternalseparation lsquoabruptlyrsquo improves due to the fact that lsquosome maturationalthreshold is passedrsquo (p 205)

CONTRIBUTIONS FROM NEUROSCIENCE TOATTACHM ENT THEORY

So the next question is 30 years after the appearance of this volume at theend of the lsquodecade of the brainrsquo how do Bowlbyrsquos original chartings of theattachment domain hold up In a word they were indeed prescient In facthis overall birdrsquos-eye perspective of the internal attachment landscape was socomprehensive that we now need to zoom in not just for close-up views ofthe essential brain structures that mediate attachment processes but also forvisualizations of how these structures dynamically self-organize within thedeveloping brain This includes neurobiological studies of Bowlbyrsquos controlsystem which I suggest may now be identied with the orbitofrontal cortexan area that has been called the lsquosenior executive of the emotional brainrsquo(Joseph 1996) and that has been shown to mediate lsquothe highest level ofcontrol of behavior especially in relation to emotionrsquo (Price Carmichael ampDrevets 1996 p 523) Keeping in mind Bowlbyrsquos previously presentedtheoretical descriptions the following is an extremely brief overview of agrowing body of studies on the neurobiology of attachment (For moreextensive expositions of these concepts and references see Schore 1994 19961997b 1998a 1999 in press a b c d e in preparation)

According to Ainsworth (1967 p 429) attachment is more than overtbehavior it is internal lsquobeing built into the nervous system in the course andas a result of the infantrsquos experience of his transactions with the motherrsquoFollowing Bowlbyrsquos suggestion the limbic system has been suggested to bethe site of developmental changes associated with the rise of attachmentbehaviors (Anders amp Zeanah 1984) Indeed the specic period from 7 to 15months has been shown to be critical for the myelination and therefore thematuration of particular rapidly developing limbic and cortical associationareas (Kinney Brody Kloman amp Gilles 1988) and limbic areas of the human

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 29

cerebral cortex show anatomical maturation at 15 months (Rabinowicz1979) In a number of works I offer evidence to show that attachment experi-ences face-to-face transactions of affect synchrony between caregiver andinfant directly inuence the imprinting the circuit wiring of the orbitalprefrontal cortex a corticolimbic area that is known to begin a major matu-rational change at 10 to 12 months and to complete a critical period of growthfrom the middle to the end of the second year This time-frame is identical toBowlbyrsquos maturation of an attachment control system that is open to in u-ence from the developmental environment

The co-created environment of evolutionary adaptiveness is thus isomor-phic to a growth-facilitating environment for the experience-dependent mat-uration of a regulatory system in the orbitofrontal cortex Indeed thisprefrontal system appraises visual facial information (Scalaidhe Wilson ampGoldman-Rakic 1997) and processes responses to pleasant touch tastesmell (Francis D et al 1999) and music (Blood Zatorre Bermudez ampEvans 1999) as well as to unpleasant images of angry and sad faces (BlairMorris Frith Perrett amp Dolan 1999) But this system is also involved in theregulation of the body state and reects changes taking place in that state(Luria 1980)

This frontolimbic system provides a high-level coding that exibly co-ordinates exteroceptive and interoceptive domains and functions to correctresponses as conditions change (Derryberry amp Tucker 1992) processes feed-back information (Elliott Frith amp Dolan 1997) and thereby monitorsadjusts and corrects emotional responses (Rolls 1986) and modulates themotivational control of goal-directed behavior (Tremblay amp Schultz 1999)So after a rapid evaluation of an environmental stimulus the orbitofrontalsystem monitors feedback about the current internal state in order to makeassessments of coping resources and it updates appropriate response outputsin order to make adaptive adjustments to particular environmental perturba-tions (Schore 1998a) In this manner lsquothe integrity of the orbitofrontal cortexis necessary for acquiring very specic forms of knowledge for regulatinginterpersonal behaviorrsquo (Dolan 1999 p 928)

These functions reect the unique anatomical properties of this area of thebrain Due to its location at the ventral and medial hemispheric surfaces itacts as a convergence zone where cortex and subcortex meet It is thus situ-ated at the apogee of the lsquorostral limbic systemrsquo a hierarchical sequence ofinterconnected limbic areas in orbitofrontal cortex insular cortex anteriorcingulate and amygdala (Schore 1997b in press a in preparation) Thelimbic system is now thought to be centrally involved in the implicit pro-cessing of facial expressions without conscious awareness (Critchley et al2000) and in the capacity lsquoto adapt to a rapidly changing environmentrsquo and inlsquothe organization of new learningrsquo (Mesulam 1998 p 1028) Emotionallyfocused limbic learning underlies the unique and fast-acting processes ofimprinting the learning mechanism associated with attachment as thisdynamic evolves over the rst and second years Hinde (1990 p 162) points

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 130

out that lsquothe development of social behavior can be understood only in termsof a continuing dialectic between an active and changing organism and anactive and changing environmentrsquo

But the orbitofrontal system is also deeply connected into the autonomicnervous system and the arousal-generating reticular formation and due tothe fact that it is the only cortical structure with such direct connections itcan regulate autonomic responses to social stimuli (Zald amp Kim 1996) andmodulate lsquoinstinctual behaviorrsquo (Starkstein amp Robinson 1997) The activityof this frontolimbic system is therefore critical to the modulation of socialand emotional behaviors and the homeostatic regulation of body and moti-vational states affect-regulating functions that are centrally involved inattachment processes The essential aspect of this function is highlighted byWestin (1997 p 542) who asserts that lsquoThe attempt to regulate affect ndash to min-imize unpleasant feelings and to maximize pleasant ones ndash is the driving forcein human motivationrsquo

The orbital prefrontal region is especially expanded in the right hemispherewhich is specialized for lsquoinhibitory controlrsquo (Garavan Ross amp Stein 1999)and it comes to act as an executive control function for the entire right brainThis hemisphere which is dominant for unconscious processes computes ona moment-to-moment basis the affective salience of external stimuli Keepingin mind Bowlbyrsquos earlier descriptions this lateralized system performs alsquovalence taggingrsquo function (Schore 1998a 1999) in which perceptions receivea positive or negative affective charge in accord with a calibration of degreesof pleasurendashunpleasure It also contains a lsquononverbal affect lexiconrsquo a vocabu-lary for nonverbal affective signals such as facial expressions gestures andvocal tone or prosody (Bowers Bauer amp Heilman 1993) The right hemi-sphere is thus faster than the left in performing valence-dependent automaticpre-attentive appraisal of emotional facial expressions (Pizzagalli Regard ampLehmann 1999)

Because the right cortical hemisphere more so than the left contains exten-sive reciprocal connections with limbic and subcortical regions (Tucker 1992Joseph 1996) it is dominant for the processing and expression of lsquoself-relatedmaterialrsquo (Keenan et al 1999) and emotional information and for regulatingpsychobiological states (Schore 1994 1998a 1999 Spence Shapiro amp Zaidel1996) Thus the right hemisphere is centrally involved in what Bowlbydescribed as the social and biological functions of the attachment system(Henry 1993 Schore 1994 Shapiro Jamner amp Spence 1997 Wang 1997Siegel 1999)

Conrming this model Ryan Kuhl and Deci (1997 p 719) using EEGand neuroimaging data conclude that lsquoThe positive emotional exchangeresulting from autonomy-supportive parenting involves participation ofright hemispheric cortical and subcortical systems that participate in globaltonic emotional modulationrsquo And in line with Bowlbyrsquos assertion thatattachment behavior is vital to the survival of the species it is now held thatthe right hemisphere is central to the control of vital functions supporting

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 31

survival and enabling the organism to cope with stresses and challenges(Wittling amp Schweiger 1993)

There is a growing body of studies which shows that the infantrsquos earlymaturing (Geschwind amp Galaburda 1987) right hemisphere is specicallyimpacted by early social experiences (Schore 1994 1998b) This develop-mental principle is now supported in a recent single photon emissioncomputed tomographic (SPECT) study by Chiron et al (1997) whichdemonstrates that the right brain hemisphere is dominant in preverbal humaninfants and indeed for the rst 3 years of life I suggest that the ontogeneticshift of dominance from the right to left hemisphere after this time may expli-cate Bowlbyrsquos description of a diminution of the attachment system at theend of the third year that is due to an lsquoabruptrsquo passage of a lsquomaturationalthresholdrsquo

Current neuropsychological studies indicate that lsquothe emotional experi-ence(s) of the infant are disproportionately stored or processed in theright hemisphere during the formative stages of brain ontogenyrsquo (Semrud-Clikeman amp Hynd 1990 p 198) that lsquothe infant relies primarily on its pro-cedural memory systemsrsquo during lsquothe rst 2ndash3 years of lifersquo (Kandel 1999 p 513) and that the right brain contains the lsquocerebral representation of onersquosown pastrsquo and the substrate of affectively laden autobiographical memory(Fink et al 1996 p 4275) These ndings suggest that early-forming inter-nal working models of the attachment relationship are processed and storedin implicit-procedural memory systems in the right cortex the hemispheredominant for implicit learning (Hugdahl 1995)

In the securely attached individual these models encode an expectationthat lsquohomeostatic disruptions will be set rightrsquo (Pipp amp Harmon 1987 p 650) In discussing these internal models Rutter (1987) notes that lsquochildrenderive a set of expectations about their own relationship capacities and aboutother peoplersquos resources to their social overtures and interactions theseexpectations being created on the basis of their early parentndashchild attach-mentsrsquo (p 449) Such representations are processed by the orbitofrontalsystem which is known to be activated during lsquobreaches of expectationrsquo(Nobre Coull Frith amp Mesulam 1999) and to generate affect-regulatingstrategies for coping with expected negative and positive emotional states thatare inherent in intimate social contexts

The efcient operations of this regulatory system allow for corticallyprocessed information concerning the external environment (such as visualand auditory stimuli emanating from the emotional face of the attachmentobject) to be integrated with subcortically processed information regardingthe internal visceral environment (such as concurrent changes in the childrsquosemotional or bodily self-state) The relaying of sensory information into thelimbic system allows incoming information about the social environment totrigger adjustments in emotional and motivational states and in this mannerthe orbitofrontal system integrates what Bowlby termed environmental andorganismic models Recent ndings that the orbitofrontal cortex generates

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 132

nonconscious biases that guide behavior before conscious knowledge does(Bechara Damasio Tranel amp Damasio 1997) and codes the likely signicanceof future behavioral options (Dolan 1999) and represents an important siteof contact between emotional information and mechanisms of action selec-tion (Rolls 1996) are consonant with Bowlbyrsquos (1981) assertion that internalworking models are used as guides for future action

These mental representations according to Main Kaplan and Cassidy(1985) contain cognitive as well as affective components and act to guideappraisals of experience The orbitofrontal cortex is known to function as anappraisal mechanism (Pribram 1987 Schore 1998a) and to be centrallyinvolved in the generation of lsquocognitive-emotional interactionsrsquo (Barbas1995) It acts to lsquointegrate and assign emotional-motivational signicance tocognitive impressions the association of emotion with ideas and thoughtsrsquo(Joseph 1996 p 427) and in lsquothe processing of affect-related meaningsrsquo (Teas-dale et al 1999)

Orbitofrontal activity is associated with a lower threshold for awarenessof sensations of both external and internal origin (Goldenberg et al 1989)thereby enabling it to act as an lsquointernal re ecting and organizing agencyrsquo(Kaplan-Solms amp Solms 1996) This orbitofrontal role in lsquoself-re ectiveawarenessrsquo (Stuss Gow amp Hetherington 1992) allows an individual to reecton his or her own internal emotional states as well as those of others(Povinelli amp Preuss 1995) According to Fonagy and Target (1997) the reec-tive function is a mental operation that enables the perception of anotherrsquosstate The right hemisphere mediates empathic cognition and the perceptionof the emotional states of other human beings (Voeller 1986) andorbitofrontal function is essential to the capacity of inferring the states ofothers (Baron-Cohen 1995) This adaptive capacity may thus be the outcomeof a secure attachment to a psychobiologically attuned affect-regulating care-giver A recent neuropsychological study indicates that the orbitofrontalcortex is lsquoparticularly involved in theory of mind tasks with an affective com-ponentrsquo (Stone Baron-Cohen amp Knight 1998 p 651)

Furthermore the functioning of the orbitofrontal control system in theregulation of emotion (Baker Frith amp Dolan 1997) and in lsquoacquiring veryspecic forms of knowledge for regulating interpersonal and social behaviorrsquo(Dolan 1999 p 928) is central to self-regulation the ability to exibly regu-late emotional states through interactions with other humans ndash that is inter-active regulation in interconnected contexts ndash and without other humans ndashthat is autoregulation in autonomous contexts The adaptive capacity to shiftbetween these dual regulatory modes depending upon the social contextemerges out of a history of secure attachment interactions of a maturing bio-logical organism and an early attuned social environment

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 33

ATTACH MENT THEORY IS FUNDAMENTALLYA REGULATORY THEORY

Attachment behavior is currently thought to be the output of lsquoa neuro-biologically based biobehavioral system that regulates biological syn-chronicity between organismsrsquo (Wang 1997 p 168) I suggest that thecharacterization of the orbitofrontal system as a frontolimbic structure thatdetermines the regulatory signi cance of stimuli that reach the organism andregulates body state (Luria 1980) bears a striking resemblance to the behav-ioral control system characterized by Bowlby over 30 years ago The OxfordDictionary denes control as lsquothe act or power of directing or regulatingrsquo

Attachment theory as rst propounded in Bowlbyrsquos (1969) denitionalvolume is fundamentally a regulatory theory Attachment can thus be con-ceptualized as the interactive regulation of synchrony between psychobiolog-ically attuned organisms This attachment dynamic which operates at levelsbeneath awareness underlies the dyadic regulation of emotion Emotions arethe highest order direct expression of bioregulation in complex organisms(Damasio 1998) Imprinting the learning process it accesses is described byPetrovich and Gewirtz (1985) as synchrony between sequential infant mater-nal stimuli and behavior (see Schore 1994 and Nelson amp Panksepp 1998 formodels of the neurochemistry of attachment)

According to Feldman et al (1999) lsquoface-to-face synchrony affords infantstheir rst opportunity to practice interpersonal coordination of biologicalrhythmsrsquo (p 223) and acts as an interpersonal context in which lsquointeractantsintegrate into the ow of behavior the ongoing responses of their partner andthe changing inputs of the environmentrsquo (p 224) The visual prosodic-auditory and gestural stimuli embedded in these emotional communicationsare rapidly transmitted back and forth between the infantrsquos and motherrsquos faceand in these transactions the caregiver acts as a regulator of the childrsquos arousallevels

Because arousal levels are known to be associated with changes in meta-bolic energy the caregiver is thus modulating changes in the childrsquos energeticstate (Schore 1994 1997b) These regulated increases in energy metabolismare available for biosynthetic processes in the babyrsquos brain which is in thebrain growth spurt (Dobbing amp Sands 1973) In this manner lsquothe intrinsicregulators of human brain growth in a child are specically adapted to becoupled by emotional communication to the regulators of adult brainsrsquo(Trevarthen 1990 p 357)

In addition the mother also regulates moments of asynchrony that isstressful negative affect Social stressors can be characterized as the occur-rence of an asynchrony in an interactional sequence (Chapple 1970) Stressdescribes both the subjective experience induced by a distressing potentiallythreatening or novel situation and the organismrsquos reactions to a homeosta-tic challenge It is now thought that social stressors are lsquofar more detrimen-talrsquo than non-social aversive stimuli (Sgoifo et al 1999)

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 134

Separation stress in essence is a loss of maternal regulators of the infantrsquosimmature behavioral and physiological systems that results in the attachmentpatterns of protest despair and detachment The principle that lsquoa period ofsynchrony following the period of stress provides a ldquorecoveryrdquo periodrsquo(Chapple 1970 p 631) underlies the mechanism of interactive repair(Tronick 1989 Schore 1994) The primary caregiverrsquos interactive regulationis therefore critical to the infantrsquos maintaining positively charged as well ascoping with stressful negatively charged affects These affect regulatingevents are particularly impacting the organization of the early developingright hemisphere

Bowlbyrsquos control system is located in the right hemisphere that is not onlydominant for lsquoinhibitory controlrsquo (Garavan et al 1999) but also for the pro-cessing of facial information in infants (Deruelle amp de Schonen 1998) andadults (Kim et al 1999) and for the regulation of arousal (Heilman amp VanDen Abell 1979) Because the major coping systems the hypothalamo-pituitary-adrenocortical axis and the sympathetic-adrenomedullary axis areboth under the main control of the right cerebral cortex this hemisphere con-tains lsquoa unique response system preparing the organism to deal efcientlywith external challengesrsquo and so its adaptive functions mediate the humanstress response (Wittling 1997 p 55) Basic research in stress physiologyshows that the behavioral and physiological response of an individual to aspecic stressor is consistent over time (Koolhaas et al 1999)

These attachment transactions are imprinted into implicit-proceduralmemory as enduring internal working models which encode coping strat-egies of affect regulation (Schore 1994) that maintain basic regulation andpositive affect even in the face of environmental challenge (Sroufe 1989)Attachment patterns are now conceptualized as lsquopatterns of mental process-ing of information based on cognition and affect to create models of realityrsquo(Crittenden 1995 p 401) The lsquoanterior limbic prefrontal networkrsquo whichinterconnects the orbital and medial prefrontal cortex with the temporal polecingulate and amygdala lsquois involved in affective responses to events and inthe mnemonic processing and storage of these responsesrsquo (Carmichael ampPrice 1995 p 639) and lsquoconstitutes a mental control system that is essentialfor adjusting thinking and behavior to ongoing realityrsquo (Schnider amp Ptak1999 p 680) An ultimate indicator of secure attachment is resilience in theface of stress (Greenspan 1981) which is expressed in the capacity to ex-ibly regulate emotional states via autoregulation and interactive regulationHowever early social environments that engender insecure attachmentsinhibit the growth of this control system (Schore 1997b) and therefore pre-clude its adaptive coping function in lsquooperations linked to behavioral exi-bilityrsquo (Nobre et al 1999 p 12)

In support of Bowlbyrsquos assertion that the childrsquos capacity to cope withstress is correlated with certain maternal behaviors current developmentalbiological studies are exploring lsquomaternal effectsrsquo the inuence of themotherrsquos experiences on her progenyrsquos development and ability to adapt to

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 35

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

movements lsquomay be actively at work even when we are not aware of themrsquo(p 110) in this manner feeling provides a monitoring of both the behavioraland physiological state (p 121) Emotional processes thus he says lie at thefoundation of a model of instinctive behavior

In following chapters Bowlby concludes that the motherndashinfant attach-ment relation is lsquoaccompanied by the strongest of feelings and emotionshappy or the reversersquo (p 242) that the infantrsquos lsquocapacity to cope with stressrsquois correlated with certain maternal behaviors (p 344) and that the instinctivebehavior that emerges from the co-constructed environment of evolutionaryadaptiveness has consequences that are lsquovital to the survival of the speciesrsquo (p 137) He also suggests that the attachment system is readily activated untilthe end of the third year when the childrsquos capacity to cope with maternalseparation lsquoabruptlyrsquo improves due to the fact that lsquosome maturationalthreshold is passedrsquo (p 205)

CONTRIBUTIONS FROM NEUROSCIENCE TOATTACHM ENT THEORY

So the next question is 30 years after the appearance of this volume at theend of the lsquodecade of the brainrsquo how do Bowlbyrsquos original chartings of theattachment domain hold up In a word they were indeed prescient In facthis overall birdrsquos-eye perspective of the internal attachment landscape was socomprehensive that we now need to zoom in not just for close-up views ofthe essential brain structures that mediate attachment processes but also forvisualizations of how these structures dynamically self-organize within thedeveloping brain This includes neurobiological studies of Bowlbyrsquos controlsystem which I suggest may now be identied with the orbitofrontal cortexan area that has been called the lsquosenior executive of the emotional brainrsquo(Joseph 1996) and that has been shown to mediate lsquothe highest level ofcontrol of behavior especially in relation to emotionrsquo (Price Carmichael ampDrevets 1996 p 523) Keeping in mind Bowlbyrsquos previously presentedtheoretical descriptions the following is an extremely brief overview of agrowing body of studies on the neurobiology of attachment (For moreextensive expositions of these concepts and references see Schore 1994 19961997b 1998a 1999 in press a b c d e in preparation)

According to Ainsworth (1967 p 429) attachment is more than overtbehavior it is internal lsquobeing built into the nervous system in the course andas a result of the infantrsquos experience of his transactions with the motherrsquoFollowing Bowlbyrsquos suggestion the limbic system has been suggested to bethe site of developmental changes associated with the rise of attachmentbehaviors (Anders amp Zeanah 1984) Indeed the specic period from 7 to 15months has been shown to be critical for the myelination and therefore thematuration of particular rapidly developing limbic and cortical associationareas (Kinney Brody Kloman amp Gilles 1988) and limbic areas of the human

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 29

cerebral cortex show anatomical maturation at 15 months (Rabinowicz1979) In a number of works I offer evidence to show that attachment experi-ences face-to-face transactions of affect synchrony between caregiver andinfant directly inuence the imprinting the circuit wiring of the orbitalprefrontal cortex a corticolimbic area that is known to begin a major matu-rational change at 10 to 12 months and to complete a critical period of growthfrom the middle to the end of the second year This time-frame is identical toBowlbyrsquos maturation of an attachment control system that is open to in u-ence from the developmental environment

The co-created environment of evolutionary adaptiveness is thus isomor-phic to a growth-facilitating environment for the experience-dependent mat-uration of a regulatory system in the orbitofrontal cortex Indeed thisprefrontal system appraises visual facial information (Scalaidhe Wilson ampGoldman-Rakic 1997) and processes responses to pleasant touch tastesmell (Francis D et al 1999) and music (Blood Zatorre Bermudez ampEvans 1999) as well as to unpleasant images of angry and sad faces (BlairMorris Frith Perrett amp Dolan 1999) But this system is also involved in theregulation of the body state and reects changes taking place in that state(Luria 1980)

This frontolimbic system provides a high-level coding that exibly co-ordinates exteroceptive and interoceptive domains and functions to correctresponses as conditions change (Derryberry amp Tucker 1992) processes feed-back information (Elliott Frith amp Dolan 1997) and thereby monitorsadjusts and corrects emotional responses (Rolls 1986) and modulates themotivational control of goal-directed behavior (Tremblay amp Schultz 1999)So after a rapid evaluation of an environmental stimulus the orbitofrontalsystem monitors feedback about the current internal state in order to makeassessments of coping resources and it updates appropriate response outputsin order to make adaptive adjustments to particular environmental perturba-tions (Schore 1998a) In this manner lsquothe integrity of the orbitofrontal cortexis necessary for acquiring very specic forms of knowledge for regulatinginterpersonal behaviorrsquo (Dolan 1999 p 928)

These functions reect the unique anatomical properties of this area of thebrain Due to its location at the ventral and medial hemispheric surfaces itacts as a convergence zone where cortex and subcortex meet It is thus situ-ated at the apogee of the lsquorostral limbic systemrsquo a hierarchical sequence ofinterconnected limbic areas in orbitofrontal cortex insular cortex anteriorcingulate and amygdala (Schore 1997b in press a in preparation) Thelimbic system is now thought to be centrally involved in the implicit pro-cessing of facial expressions without conscious awareness (Critchley et al2000) and in the capacity lsquoto adapt to a rapidly changing environmentrsquo and inlsquothe organization of new learningrsquo (Mesulam 1998 p 1028) Emotionallyfocused limbic learning underlies the unique and fast-acting processes ofimprinting the learning mechanism associated with attachment as thisdynamic evolves over the rst and second years Hinde (1990 p 162) points

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 130

out that lsquothe development of social behavior can be understood only in termsof a continuing dialectic between an active and changing organism and anactive and changing environmentrsquo

But the orbitofrontal system is also deeply connected into the autonomicnervous system and the arousal-generating reticular formation and due tothe fact that it is the only cortical structure with such direct connections itcan regulate autonomic responses to social stimuli (Zald amp Kim 1996) andmodulate lsquoinstinctual behaviorrsquo (Starkstein amp Robinson 1997) The activityof this frontolimbic system is therefore critical to the modulation of socialand emotional behaviors and the homeostatic regulation of body and moti-vational states affect-regulating functions that are centrally involved inattachment processes The essential aspect of this function is highlighted byWestin (1997 p 542) who asserts that lsquoThe attempt to regulate affect ndash to min-imize unpleasant feelings and to maximize pleasant ones ndash is the driving forcein human motivationrsquo

The orbital prefrontal region is especially expanded in the right hemispherewhich is specialized for lsquoinhibitory controlrsquo (Garavan Ross amp Stein 1999)and it comes to act as an executive control function for the entire right brainThis hemisphere which is dominant for unconscious processes computes ona moment-to-moment basis the affective salience of external stimuli Keepingin mind Bowlbyrsquos earlier descriptions this lateralized system performs alsquovalence taggingrsquo function (Schore 1998a 1999) in which perceptions receivea positive or negative affective charge in accord with a calibration of degreesof pleasurendashunpleasure It also contains a lsquononverbal affect lexiconrsquo a vocabu-lary for nonverbal affective signals such as facial expressions gestures andvocal tone or prosody (Bowers Bauer amp Heilman 1993) The right hemi-sphere is thus faster than the left in performing valence-dependent automaticpre-attentive appraisal of emotional facial expressions (Pizzagalli Regard ampLehmann 1999)

Because the right cortical hemisphere more so than the left contains exten-sive reciprocal connections with limbic and subcortical regions (Tucker 1992Joseph 1996) it is dominant for the processing and expression of lsquoself-relatedmaterialrsquo (Keenan et al 1999) and emotional information and for regulatingpsychobiological states (Schore 1994 1998a 1999 Spence Shapiro amp Zaidel1996) Thus the right hemisphere is centrally involved in what Bowlbydescribed as the social and biological functions of the attachment system(Henry 1993 Schore 1994 Shapiro Jamner amp Spence 1997 Wang 1997Siegel 1999)

Conrming this model Ryan Kuhl and Deci (1997 p 719) using EEGand neuroimaging data conclude that lsquoThe positive emotional exchangeresulting from autonomy-supportive parenting involves participation ofright hemispheric cortical and subcortical systems that participate in globaltonic emotional modulationrsquo And in line with Bowlbyrsquos assertion thatattachment behavior is vital to the survival of the species it is now held thatthe right hemisphere is central to the control of vital functions supporting

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 31

survival and enabling the organism to cope with stresses and challenges(Wittling amp Schweiger 1993)

There is a growing body of studies which shows that the infantrsquos earlymaturing (Geschwind amp Galaburda 1987) right hemisphere is specicallyimpacted by early social experiences (Schore 1994 1998b) This develop-mental principle is now supported in a recent single photon emissioncomputed tomographic (SPECT) study by Chiron et al (1997) whichdemonstrates that the right brain hemisphere is dominant in preverbal humaninfants and indeed for the rst 3 years of life I suggest that the ontogeneticshift of dominance from the right to left hemisphere after this time may expli-cate Bowlbyrsquos description of a diminution of the attachment system at theend of the third year that is due to an lsquoabruptrsquo passage of a lsquomaturationalthresholdrsquo

Current neuropsychological studies indicate that lsquothe emotional experi-ence(s) of the infant are disproportionately stored or processed in theright hemisphere during the formative stages of brain ontogenyrsquo (Semrud-Clikeman amp Hynd 1990 p 198) that lsquothe infant relies primarily on its pro-cedural memory systemsrsquo during lsquothe rst 2ndash3 years of lifersquo (Kandel 1999 p 513) and that the right brain contains the lsquocerebral representation of onersquosown pastrsquo and the substrate of affectively laden autobiographical memory(Fink et al 1996 p 4275) These ndings suggest that early-forming inter-nal working models of the attachment relationship are processed and storedin implicit-procedural memory systems in the right cortex the hemispheredominant for implicit learning (Hugdahl 1995)

In the securely attached individual these models encode an expectationthat lsquohomeostatic disruptions will be set rightrsquo (Pipp amp Harmon 1987 p 650) In discussing these internal models Rutter (1987) notes that lsquochildrenderive a set of expectations about their own relationship capacities and aboutother peoplersquos resources to their social overtures and interactions theseexpectations being created on the basis of their early parentndashchild attach-mentsrsquo (p 449) Such representations are processed by the orbitofrontalsystem which is known to be activated during lsquobreaches of expectationrsquo(Nobre Coull Frith amp Mesulam 1999) and to generate affect-regulatingstrategies for coping with expected negative and positive emotional states thatare inherent in intimate social contexts

The efcient operations of this regulatory system allow for corticallyprocessed information concerning the external environment (such as visualand auditory stimuli emanating from the emotional face of the attachmentobject) to be integrated with subcortically processed information regardingthe internal visceral environment (such as concurrent changes in the childrsquosemotional or bodily self-state) The relaying of sensory information into thelimbic system allows incoming information about the social environment totrigger adjustments in emotional and motivational states and in this mannerthe orbitofrontal system integrates what Bowlby termed environmental andorganismic models Recent ndings that the orbitofrontal cortex generates

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 132

nonconscious biases that guide behavior before conscious knowledge does(Bechara Damasio Tranel amp Damasio 1997) and codes the likely signicanceof future behavioral options (Dolan 1999) and represents an important siteof contact between emotional information and mechanisms of action selec-tion (Rolls 1996) are consonant with Bowlbyrsquos (1981) assertion that internalworking models are used as guides for future action

These mental representations according to Main Kaplan and Cassidy(1985) contain cognitive as well as affective components and act to guideappraisals of experience The orbitofrontal cortex is known to function as anappraisal mechanism (Pribram 1987 Schore 1998a) and to be centrallyinvolved in the generation of lsquocognitive-emotional interactionsrsquo (Barbas1995) It acts to lsquointegrate and assign emotional-motivational signicance tocognitive impressions the association of emotion with ideas and thoughtsrsquo(Joseph 1996 p 427) and in lsquothe processing of affect-related meaningsrsquo (Teas-dale et al 1999)

Orbitofrontal activity is associated with a lower threshold for awarenessof sensations of both external and internal origin (Goldenberg et al 1989)thereby enabling it to act as an lsquointernal re ecting and organizing agencyrsquo(Kaplan-Solms amp Solms 1996) This orbitofrontal role in lsquoself-re ectiveawarenessrsquo (Stuss Gow amp Hetherington 1992) allows an individual to reecton his or her own internal emotional states as well as those of others(Povinelli amp Preuss 1995) According to Fonagy and Target (1997) the reec-tive function is a mental operation that enables the perception of anotherrsquosstate The right hemisphere mediates empathic cognition and the perceptionof the emotional states of other human beings (Voeller 1986) andorbitofrontal function is essential to the capacity of inferring the states ofothers (Baron-Cohen 1995) This adaptive capacity may thus be the outcomeof a secure attachment to a psychobiologically attuned affect-regulating care-giver A recent neuropsychological study indicates that the orbitofrontalcortex is lsquoparticularly involved in theory of mind tasks with an affective com-ponentrsquo (Stone Baron-Cohen amp Knight 1998 p 651)

Furthermore the functioning of the orbitofrontal control system in theregulation of emotion (Baker Frith amp Dolan 1997) and in lsquoacquiring veryspecic forms of knowledge for regulating interpersonal and social behaviorrsquo(Dolan 1999 p 928) is central to self-regulation the ability to exibly regu-late emotional states through interactions with other humans ndash that is inter-active regulation in interconnected contexts ndash and without other humans ndashthat is autoregulation in autonomous contexts The adaptive capacity to shiftbetween these dual regulatory modes depending upon the social contextemerges out of a history of secure attachment interactions of a maturing bio-logical organism and an early attuned social environment

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 33

ATTACH MENT THEORY IS FUNDAMENTALLYA REGULATORY THEORY

Attachment behavior is currently thought to be the output of lsquoa neuro-biologically based biobehavioral system that regulates biological syn-chronicity between organismsrsquo (Wang 1997 p 168) I suggest that thecharacterization of the orbitofrontal system as a frontolimbic structure thatdetermines the regulatory signi cance of stimuli that reach the organism andregulates body state (Luria 1980) bears a striking resemblance to the behav-ioral control system characterized by Bowlby over 30 years ago The OxfordDictionary denes control as lsquothe act or power of directing or regulatingrsquo

Attachment theory as rst propounded in Bowlbyrsquos (1969) denitionalvolume is fundamentally a regulatory theory Attachment can thus be con-ceptualized as the interactive regulation of synchrony between psychobiolog-ically attuned organisms This attachment dynamic which operates at levelsbeneath awareness underlies the dyadic regulation of emotion Emotions arethe highest order direct expression of bioregulation in complex organisms(Damasio 1998) Imprinting the learning process it accesses is described byPetrovich and Gewirtz (1985) as synchrony between sequential infant mater-nal stimuli and behavior (see Schore 1994 and Nelson amp Panksepp 1998 formodels of the neurochemistry of attachment)

According to Feldman et al (1999) lsquoface-to-face synchrony affords infantstheir rst opportunity to practice interpersonal coordination of biologicalrhythmsrsquo (p 223) and acts as an interpersonal context in which lsquointeractantsintegrate into the ow of behavior the ongoing responses of their partner andthe changing inputs of the environmentrsquo (p 224) The visual prosodic-auditory and gestural stimuli embedded in these emotional communicationsare rapidly transmitted back and forth between the infantrsquos and motherrsquos faceand in these transactions the caregiver acts as a regulator of the childrsquos arousallevels

Because arousal levels are known to be associated with changes in meta-bolic energy the caregiver is thus modulating changes in the childrsquos energeticstate (Schore 1994 1997b) These regulated increases in energy metabolismare available for biosynthetic processes in the babyrsquos brain which is in thebrain growth spurt (Dobbing amp Sands 1973) In this manner lsquothe intrinsicregulators of human brain growth in a child are specically adapted to becoupled by emotional communication to the regulators of adult brainsrsquo(Trevarthen 1990 p 357)

In addition the mother also regulates moments of asynchrony that isstressful negative affect Social stressors can be characterized as the occur-rence of an asynchrony in an interactional sequence (Chapple 1970) Stressdescribes both the subjective experience induced by a distressing potentiallythreatening or novel situation and the organismrsquos reactions to a homeosta-tic challenge It is now thought that social stressors are lsquofar more detrimen-talrsquo than non-social aversive stimuli (Sgoifo et al 1999)

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 134

Separation stress in essence is a loss of maternal regulators of the infantrsquosimmature behavioral and physiological systems that results in the attachmentpatterns of protest despair and detachment The principle that lsquoa period ofsynchrony following the period of stress provides a ldquorecoveryrdquo periodrsquo(Chapple 1970 p 631) underlies the mechanism of interactive repair(Tronick 1989 Schore 1994) The primary caregiverrsquos interactive regulationis therefore critical to the infantrsquos maintaining positively charged as well ascoping with stressful negatively charged affects These affect regulatingevents are particularly impacting the organization of the early developingright hemisphere

Bowlbyrsquos control system is located in the right hemisphere that is not onlydominant for lsquoinhibitory controlrsquo (Garavan et al 1999) but also for the pro-cessing of facial information in infants (Deruelle amp de Schonen 1998) andadults (Kim et al 1999) and for the regulation of arousal (Heilman amp VanDen Abell 1979) Because the major coping systems the hypothalamo-pituitary-adrenocortical axis and the sympathetic-adrenomedullary axis areboth under the main control of the right cerebral cortex this hemisphere con-tains lsquoa unique response system preparing the organism to deal efcientlywith external challengesrsquo and so its adaptive functions mediate the humanstress response (Wittling 1997 p 55) Basic research in stress physiologyshows that the behavioral and physiological response of an individual to aspecic stressor is consistent over time (Koolhaas et al 1999)

These attachment transactions are imprinted into implicit-proceduralmemory as enduring internal working models which encode coping strat-egies of affect regulation (Schore 1994) that maintain basic regulation andpositive affect even in the face of environmental challenge (Sroufe 1989)Attachment patterns are now conceptualized as lsquopatterns of mental process-ing of information based on cognition and affect to create models of realityrsquo(Crittenden 1995 p 401) The lsquoanterior limbic prefrontal networkrsquo whichinterconnects the orbital and medial prefrontal cortex with the temporal polecingulate and amygdala lsquois involved in affective responses to events and inthe mnemonic processing and storage of these responsesrsquo (Carmichael ampPrice 1995 p 639) and lsquoconstitutes a mental control system that is essentialfor adjusting thinking and behavior to ongoing realityrsquo (Schnider amp Ptak1999 p 680) An ultimate indicator of secure attachment is resilience in theface of stress (Greenspan 1981) which is expressed in the capacity to ex-ibly regulate emotional states via autoregulation and interactive regulationHowever early social environments that engender insecure attachmentsinhibit the growth of this control system (Schore 1997b) and therefore pre-clude its adaptive coping function in lsquooperations linked to behavioral exi-bilityrsquo (Nobre et al 1999 p 12)

In support of Bowlbyrsquos assertion that the childrsquos capacity to cope withstress is correlated with certain maternal behaviors current developmentalbiological studies are exploring lsquomaternal effectsrsquo the inuence of themotherrsquos experiences on her progenyrsquos development and ability to adapt to

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 35

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

cerebral cortex show anatomical maturation at 15 months (Rabinowicz1979) In a number of works I offer evidence to show that attachment experi-ences face-to-face transactions of affect synchrony between caregiver andinfant directly inuence the imprinting the circuit wiring of the orbitalprefrontal cortex a corticolimbic area that is known to begin a major matu-rational change at 10 to 12 months and to complete a critical period of growthfrom the middle to the end of the second year This time-frame is identical toBowlbyrsquos maturation of an attachment control system that is open to in u-ence from the developmental environment

The co-created environment of evolutionary adaptiveness is thus isomor-phic to a growth-facilitating environment for the experience-dependent mat-uration of a regulatory system in the orbitofrontal cortex Indeed thisprefrontal system appraises visual facial information (Scalaidhe Wilson ampGoldman-Rakic 1997) and processes responses to pleasant touch tastesmell (Francis D et al 1999) and music (Blood Zatorre Bermudez ampEvans 1999) as well as to unpleasant images of angry and sad faces (BlairMorris Frith Perrett amp Dolan 1999) But this system is also involved in theregulation of the body state and reects changes taking place in that state(Luria 1980)

This frontolimbic system provides a high-level coding that exibly co-ordinates exteroceptive and interoceptive domains and functions to correctresponses as conditions change (Derryberry amp Tucker 1992) processes feed-back information (Elliott Frith amp Dolan 1997) and thereby monitorsadjusts and corrects emotional responses (Rolls 1986) and modulates themotivational control of goal-directed behavior (Tremblay amp Schultz 1999)So after a rapid evaluation of an environmental stimulus the orbitofrontalsystem monitors feedback about the current internal state in order to makeassessments of coping resources and it updates appropriate response outputsin order to make adaptive adjustments to particular environmental perturba-tions (Schore 1998a) In this manner lsquothe integrity of the orbitofrontal cortexis necessary for acquiring very specic forms of knowledge for regulatinginterpersonal behaviorrsquo (Dolan 1999 p 928)

These functions reect the unique anatomical properties of this area of thebrain Due to its location at the ventral and medial hemispheric surfaces itacts as a convergence zone where cortex and subcortex meet It is thus situ-ated at the apogee of the lsquorostral limbic systemrsquo a hierarchical sequence ofinterconnected limbic areas in orbitofrontal cortex insular cortex anteriorcingulate and amygdala (Schore 1997b in press a in preparation) Thelimbic system is now thought to be centrally involved in the implicit pro-cessing of facial expressions without conscious awareness (Critchley et al2000) and in the capacity lsquoto adapt to a rapidly changing environmentrsquo and inlsquothe organization of new learningrsquo (Mesulam 1998 p 1028) Emotionallyfocused limbic learning underlies the unique and fast-acting processes ofimprinting the learning mechanism associated with attachment as thisdynamic evolves over the rst and second years Hinde (1990 p 162) points

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 130

out that lsquothe development of social behavior can be understood only in termsof a continuing dialectic between an active and changing organism and anactive and changing environmentrsquo

But the orbitofrontal system is also deeply connected into the autonomicnervous system and the arousal-generating reticular formation and due tothe fact that it is the only cortical structure with such direct connections itcan regulate autonomic responses to social stimuli (Zald amp Kim 1996) andmodulate lsquoinstinctual behaviorrsquo (Starkstein amp Robinson 1997) The activityof this frontolimbic system is therefore critical to the modulation of socialand emotional behaviors and the homeostatic regulation of body and moti-vational states affect-regulating functions that are centrally involved inattachment processes The essential aspect of this function is highlighted byWestin (1997 p 542) who asserts that lsquoThe attempt to regulate affect ndash to min-imize unpleasant feelings and to maximize pleasant ones ndash is the driving forcein human motivationrsquo

The orbital prefrontal region is especially expanded in the right hemispherewhich is specialized for lsquoinhibitory controlrsquo (Garavan Ross amp Stein 1999)and it comes to act as an executive control function for the entire right brainThis hemisphere which is dominant for unconscious processes computes ona moment-to-moment basis the affective salience of external stimuli Keepingin mind Bowlbyrsquos earlier descriptions this lateralized system performs alsquovalence taggingrsquo function (Schore 1998a 1999) in which perceptions receivea positive or negative affective charge in accord with a calibration of degreesof pleasurendashunpleasure It also contains a lsquononverbal affect lexiconrsquo a vocabu-lary for nonverbal affective signals such as facial expressions gestures andvocal tone or prosody (Bowers Bauer amp Heilman 1993) The right hemi-sphere is thus faster than the left in performing valence-dependent automaticpre-attentive appraisal of emotional facial expressions (Pizzagalli Regard ampLehmann 1999)

Because the right cortical hemisphere more so than the left contains exten-sive reciprocal connections with limbic and subcortical regions (Tucker 1992Joseph 1996) it is dominant for the processing and expression of lsquoself-relatedmaterialrsquo (Keenan et al 1999) and emotional information and for regulatingpsychobiological states (Schore 1994 1998a 1999 Spence Shapiro amp Zaidel1996) Thus the right hemisphere is centrally involved in what Bowlbydescribed as the social and biological functions of the attachment system(Henry 1993 Schore 1994 Shapiro Jamner amp Spence 1997 Wang 1997Siegel 1999)

Conrming this model Ryan Kuhl and Deci (1997 p 719) using EEGand neuroimaging data conclude that lsquoThe positive emotional exchangeresulting from autonomy-supportive parenting involves participation ofright hemispheric cortical and subcortical systems that participate in globaltonic emotional modulationrsquo And in line with Bowlbyrsquos assertion thatattachment behavior is vital to the survival of the species it is now held thatthe right hemisphere is central to the control of vital functions supporting

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 31

survival and enabling the organism to cope with stresses and challenges(Wittling amp Schweiger 1993)

There is a growing body of studies which shows that the infantrsquos earlymaturing (Geschwind amp Galaburda 1987) right hemisphere is specicallyimpacted by early social experiences (Schore 1994 1998b) This develop-mental principle is now supported in a recent single photon emissioncomputed tomographic (SPECT) study by Chiron et al (1997) whichdemonstrates that the right brain hemisphere is dominant in preverbal humaninfants and indeed for the rst 3 years of life I suggest that the ontogeneticshift of dominance from the right to left hemisphere after this time may expli-cate Bowlbyrsquos description of a diminution of the attachment system at theend of the third year that is due to an lsquoabruptrsquo passage of a lsquomaturationalthresholdrsquo

Current neuropsychological studies indicate that lsquothe emotional experi-ence(s) of the infant are disproportionately stored or processed in theright hemisphere during the formative stages of brain ontogenyrsquo (Semrud-Clikeman amp Hynd 1990 p 198) that lsquothe infant relies primarily on its pro-cedural memory systemsrsquo during lsquothe rst 2ndash3 years of lifersquo (Kandel 1999 p 513) and that the right brain contains the lsquocerebral representation of onersquosown pastrsquo and the substrate of affectively laden autobiographical memory(Fink et al 1996 p 4275) These ndings suggest that early-forming inter-nal working models of the attachment relationship are processed and storedin implicit-procedural memory systems in the right cortex the hemispheredominant for implicit learning (Hugdahl 1995)

In the securely attached individual these models encode an expectationthat lsquohomeostatic disruptions will be set rightrsquo (Pipp amp Harmon 1987 p 650) In discussing these internal models Rutter (1987) notes that lsquochildrenderive a set of expectations about their own relationship capacities and aboutother peoplersquos resources to their social overtures and interactions theseexpectations being created on the basis of their early parentndashchild attach-mentsrsquo (p 449) Such representations are processed by the orbitofrontalsystem which is known to be activated during lsquobreaches of expectationrsquo(Nobre Coull Frith amp Mesulam 1999) and to generate affect-regulatingstrategies for coping with expected negative and positive emotional states thatare inherent in intimate social contexts

The efcient operations of this regulatory system allow for corticallyprocessed information concerning the external environment (such as visualand auditory stimuli emanating from the emotional face of the attachmentobject) to be integrated with subcortically processed information regardingthe internal visceral environment (such as concurrent changes in the childrsquosemotional or bodily self-state) The relaying of sensory information into thelimbic system allows incoming information about the social environment totrigger adjustments in emotional and motivational states and in this mannerthe orbitofrontal system integrates what Bowlby termed environmental andorganismic models Recent ndings that the orbitofrontal cortex generates

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 132

nonconscious biases that guide behavior before conscious knowledge does(Bechara Damasio Tranel amp Damasio 1997) and codes the likely signicanceof future behavioral options (Dolan 1999) and represents an important siteof contact between emotional information and mechanisms of action selec-tion (Rolls 1996) are consonant with Bowlbyrsquos (1981) assertion that internalworking models are used as guides for future action

These mental representations according to Main Kaplan and Cassidy(1985) contain cognitive as well as affective components and act to guideappraisals of experience The orbitofrontal cortex is known to function as anappraisal mechanism (Pribram 1987 Schore 1998a) and to be centrallyinvolved in the generation of lsquocognitive-emotional interactionsrsquo (Barbas1995) It acts to lsquointegrate and assign emotional-motivational signicance tocognitive impressions the association of emotion with ideas and thoughtsrsquo(Joseph 1996 p 427) and in lsquothe processing of affect-related meaningsrsquo (Teas-dale et al 1999)

Orbitofrontal activity is associated with a lower threshold for awarenessof sensations of both external and internal origin (Goldenberg et al 1989)thereby enabling it to act as an lsquointernal re ecting and organizing agencyrsquo(Kaplan-Solms amp Solms 1996) This orbitofrontal role in lsquoself-re ectiveawarenessrsquo (Stuss Gow amp Hetherington 1992) allows an individual to reecton his or her own internal emotional states as well as those of others(Povinelli amp Preuss 1995) According to Fonagy and Target (1997) the reec-tive function is a mental operation that enables the perception of anotherrsquosstate The right hemisphere mediates empathic cognition and the perceptionof the emotional states of other human beings (Voeller 1986) andorbitofrontal function is essential to the capacity of inferring the states ofothers (Baron-Cohen 1995) This adaptive capacity may thus be the outcomeof a secure attachment to a psychobiologically attuned affect-regulating care-giver A recent neuropsychological study indicates that the orbitofrontalcortex is lsquoparticularly involved in theory of mind tasks with an affective com-ponentrsquo (Stone Baron-Cohen amp Knight 1998 p 651)

Furthermore the functioning of the orbitofrontal control system in theregulation of emotion (Baker Frith amp Dolan 1997) and in lsquoacquiring veryspecic forms of knowledge for regulating interpersonal and social behaviorrsquo(Dolan 1999 p 928) is central to self-regulation the ability to exibly regu-late emotional states through interactions with other humans ndash that is inter-active regulation in interconnected contexts ndash and without other humans ndashthat is autoregulation in autonomous contexts The adaptive capacity to shiftbetween these dual regulatory modes depending upon the social contextemerges out of a history of secure attachment interactions of a maturing bio-logical organism and an early attuned social environment

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 33

ATTACH MENT THEORY IS FUNDAMENTALLYA REGULATORY THEORY

Attachment behavior is currently thought to be the output of lsquoa neuro-biologically based biobehavioral system that regulates biological syn-chronicity between organismsrsquo (Wang 1997 p 168) I suggest that thecharacterization of the orbitofrontal system as a frontolimbic structure thatdetermines the regulatory signi cance of stimuli that reach the organism andregulates body state (Luria 1980) bears a striking resemblance to the behav-ioral control system characterized by Bowlby over 30 years ago The OxfordDictionary denes control as lsquothe act or power of directing or regulatingrsquo

Attachment theory as rst propounded in Bowlbyrsquos (1969) denitionalvolume is fundamentally a regulatory theory Attachment can thus be con-ceptualized as the interactive regulation of synchrony between psychobiolog-ically attuned organisms This attachment dynamic which operates at levelsbeneath awareness underlies the dyadic regulation of emotion Emotions arethe highest order direct expression of bioregulation in complex organisms(Damasio 1998) Imprinting the learning process it accesses is described byPetrovich and Gewirtz (1985) as synchrony between sequential infant mater-nal stimuli and behavior (see Schore 1994 and Nelson amp Panksepp 1998 formodels of the neurochemistry of attachment)

According to Feldman et al (1999) lsquoface-to-face synchrony affords infantstheir rst opportunity to practice interpersonal coordination of biologicalrhythmsrsquo (p 223) and acts as an interpersonal context in which lsquointeractantsintegrate into the ow of behavior the ongoing responses of their partner andthe changing inputs of the environmentrsquo (p 224) The visual prosodic-auditory and gestural stimuli embedded in these emotional communicationsare rapidly transmitted back and forth between the infantrsquos and motherrsquos faceand in these transactions the caregiver acts as a regulator of the childrsquos arousallevels

Because arousal levels are known to be associated with changes in meta-bolic energy the caregiver is thus modulating changes in the childrsquos energeticstate (Schore 1994 1997b) These regulated increases in energy metabolismare available for biosynthetic processes in the babyrsquos brain which is in thebrain growth spurt (Dobbing amp Sands 1973) In this manner lsquothe intrinsicregulators of human brain growth in a child are specically adapted to becoupled by emotional communication to the regulators of adult brainsrsquo(Trevarthen 1990 p 357)

In addition the mother also regulates moments of asynchrony that isstressful negative affect Social stressors can be characterized as the occur-rence of an asynchrony in an interactional sequence (Chapple 1970) Stressdescribes both the subjective experience induced by a distressing potentiallythreatening or novel situation and the organismrsquos reactions to a homeosta-tic challenge It is now thought that social stressors are lsquofar more detrimen-talrsquo than non-social aversive stimuli (Sgoifo et al 1999)

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 134

Separation stress in essence is a loss of maternal regulators of the infantrsquosimmature behavioral and physiological systems that results in the attachmentpatterns of protest despair and detachment The principle that lsquoa period ofsynchrony following the period of stress provides a ldquorecoveryrdquo periodrsquo(Chapple 1970 p 631) underlies the mechanism of interactive repair(Tronick 1989 Schore 1994) The primary caregiverrsquos interactive regulationis therefore critical to the infantrsquos maintaining positively charged as well ascoping with stressful negatively charged affects These affect regulatingevents are particularly impacting the organization of the early developingright hemisphere

Bowlbyrsquos control system is located in the right hemisphere that is not onlydominant for lsquoinhibitory controlrsquo (Garavan et al 1999) but also for the pro-cessing of facial information in infants (Deruelle amp de Schonen 1998) andadults (Kim et al 1999) and for the regulation of arousal (Heilman amp VanDen Abell 1979) Because the major coping systems the hypothalamo-pituitary-adrenocortical axis and the sympathetic-adrenomedullary axis areboth under the main control of the right cerebral cortex this hemisphere con-tains lsquoa unique response system preparing the organism to deal efcientlywith external challengesrsquo and so its adaptive functions mediate the humanstress response (Wittling 1997 p 55) Basic research in stress physiologyshows that the behavioral and physiological response of an individual to aspecic stressor is consistent over time (Koolhaas et al 1999)

These attachment transactions are imprinted into implicit-proceduralmemory as enduring internal working models which encode coping strat-egies of affect regulation (Schore 1994) that maintain basic regulation andpositive affect even in the face of environmental challenge (Sroufe 1989)Attachment patterns are now conceptualized as lsquopatterns of mental process-ing of information based on cognition and affect to create models of realityrsquo(Crittenden 1995 p 401) The lsquoanterior limbic prefrontal networkrsquo whichinterconnects the orbital and medial prefrontal cortex with the temporal polecingulate and amygdala lsquois involved in affective responses to events and inthe mnemonic processing and storage of these responsesrsquo (Carmichael ampPrice 1995 p 639) and lsquoconstitutes a mental control system that is essentialfor adjusting thinking and behavior to ongoing realityrsquo (Schnider amp Ptak1999 p 680) An ultimate indicator of secure attachment is resilience in theface of stress (Greenspan 1981) which is expressed in the capacity to ex-ibly regulate emotional states via autoregulation and interactive regulationHowever early social environments that engender insecure attachmentsinhibit the growth of this control system (Schore 1997b) and therefore pre-clude its adaptive coping function in lsquooperations linked to behavioral exi-bilityrsquo (Nobre et al 1999 p 12)

In support of Bowlbyrsquos assertion that the childrsquos capacity to cope withstress is correlated with certain maternal behaviors current developmentalbiological studies are exploring lsquomaternal effectsrsquo the inuence of themotherrsquos experiences on her progenyrsquos development and ability to adapt to

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 35

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

out that lsquothe development of social behavior can be understood only in termsof a continuing dialectic between an active and changing organism and anactive and changing environmentrsquo

But the orbitofrontal system is also deeply connected into the autonomicnervous system and the arousal-generating reticular formation and due tothe fact that it is the only cortical structure with such direct connections itcan regulate autonomic responses to social stimuli (Zald amp Kim 1996) andmodulate lsquoinstinctual behaviorrsquo (Starkstein amp Robinson 1997) The activityof this frontolimbic system is therefore critical to the modulation of socialand emotional behaviors and the homeostatic regulation of body and moti-vational states affect-regulating functions that are centrally involved inattachment processes The essential aspect of this function is highlighted byWestin (1997 p 542) who asserts that lsquoThe attempt to regulate affect ndash to min-imize unpleasant feelings and to maximize pleasant ones ndash is the driving forcein human motivationrsquo

The orbital prefrontal region is especially expanded in the right hemispherewhich is specialized for lsquoinhibitory controlrsquo (Garavan Ross amp Stein 1999)and it comes to act as an executive control function for the entire right brainThis hemisphere which is dominant for unconscious processes computes ona moment-to-moment basis the affective salience of external stimuli Keepingin mind Bowlbyrsquos earlier descriptions this lateralized system performs alsquovalence taggingrsquo function (Schore 1998a 1999) in which perceptions receivea positive or negative affective charge in accord with a calibration of degreesof pleasurendashunpleasure It also contains a lsquononverbal affect lexiconrsquo a vocabu-lary for nonverbal affective signals such as facial expressions gestures andvocal tone or prosody (Bowers Bauer amp Heilman 1993) The right hemi-sphere is thus faster than the left in performing valence-dependent automaticpre-attentive appraisal of emotional facial expressions (Pizzagalli Regard ampLehmann 1999)

Because the right cortical hemisphere more so than the left contains exten-sive reciprocal connections with limbic and subcortical regions (Tucker 1992Joseph 1996) it is dominant for the processing and expression of lsquoself-relatedmaterialrsquo (Keenan et al 1999) and emotional information and for regulatingpsychobiological states (Schore 1994 1998a 1999 Spence Shapiro amp Zaidel1996) Thus the right hemisphere is centrally involved in what Bowlbydescribed as the social and biological functions of the attachment system(Henry 1993 Schore 1994 Shapiro Jamner amp Spence 1997 Wang 1997Siegel 1999)

Conrming this model Ryan Kuhl and Deci (1997 p 719) using EEGand neuroimaging data conclude that lsquoThe positive emotional exchangeresulting from autonomy-supportive parenting involves participation ofright hemispheric cortical and subcortical systems that participate in globaltonic emotional modulationrsquo And in line with Bowlbyrsquos assertion thatattachment behavior is vital to the survival of the species it is now held thatthe right hemisphere is central to the control of vital functions supporting

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 31

survival and enabling the organism to cope with stresses and challenges(Wittling amp Schweiger 1993)

There is a growing body of studies which shows that the infantrsquos earlymaturing (Geschwind amp Galaburda 1987) right hemisphere is specicallyimpacted by early social experiences (Schore 1994 1998b) This develop-mental principle is now supported in a recent single photon emissioncomputed tomographic (SPECT) study by Chiron et al (1997) whichdemonstrates that the right brain hemisphere is dominant in preverbal humaninfants and indeed for the rst 3 years of life I suggest that the ontogeneticshift of dominance from the right to left hemisphere after this time may expli-cate Bowlbyrsquos description of a diminution of the attachment system at theend of the third year that is due to an lsquoabruptrsquo passage of a lsquomaturationalthresholdrsquo

Current neuropsychological studies indicate that lsquothe emotional experi-ence(s) of the infant are disproportionately stored or processed in theright hemisphere during the formative stages of brain ontogenyrsquo (Semrud-Clikeman amp Hynd 1990 p 198) that lsquothe infant relies primarily on its pro-cedural memory systemsrsquo during lsquothe rst 2ndash3 years of lifersquo (Kandel 1999 p 513) and that the right brain contains the lsquocerebral representation of onersquosown pastrsquo and the substrate of affectively laden autobiographical memory(Fink et al 1996 p 4275) These ndings suggest that early-forming inter-nal working models of the attachment relationship are processed and storedin implicit-procedural memory systems in the right cortex the hemispheredominant for implicit learning (Hugdahl 1995)

In the securely attached individual these models encode an expectationthat lsquohomeostatic disruptions will be set rightrsquo (Pipp amp Harmon 1987 p 650) In discussing these internal models Rutter (1987) notes that lsquochildrenderive a set of expectations about their own relationship capacities and aboutother peoplersquos resources to their social overtures and interactions theseexpectations being created on the basis of their early parentndashchild attach-mentsrsquo (p 449) Such representations are processed by the orbitofrontalsystem which is known to be activated during lsquobreaches of expectationrsquo(Nobre Coull Frith amp Mesulam 1999) and to generate affect-regulatingstrategies for coping with expected negative and positive emotional states thatare inherent in intimate social contexts

The efcient operations of this regulatory system allow for corticallyprocessed information concerning the external environment (such as visualand auditory stimuli emanating from the emotional face of the attachmentobject) to be integrated with subcortically processed information regardingthe internal visceral environment (such as concurrent changes in the childrsquosemotional or bodily self-state) The relaying of sensory information into thelimbic system allows incoming information about the social environment totrigger adjustments in emotional and motivational states and in this mannerthe orbitofrontal system integrates what Bowlby termed environmental andorganismic models Recent ndings that the orbitofrontal cortex generates

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 132

nonconscious biases that guide behavior before conscious knowledge does(Bechara Damasio Tranel amp Damasio 1997) and codes the likely signicanceof future behavioral options (Dolan 1999) and represents an important siteof contact between emotional information and mechanisms of action selec-tion (Rolls 1996) are consonant with Bowlbyrsquos (1981) assertion that internalworking models are used as guides for future action

These mental representations according to Main Kaplan and Cassidy(1985) contain cognitive as well as affective components and act to guideappraisals of experience The orbitofrontal cortex is known to function as anappraisal mechanism (Pribram 1987 Schore 1998a) and to be centrallyinvolved in the generation of lsquocognitive-emotional interactionsrsquo (Barbas1995) It acts to lsquointegrate and assign emotional-motivational signicance tocognitive impressions the association of emotion with ideas and thoughtsrsquo(Joseph 1996 p 427) and in lsquothe processing of affect-related meaningsrsquo (Teas-dale et al 1999)

Orbitofrontal activity is associated with a lower threshold for awarenessof sensations of both external and internal origin (Goldenberg et al 1989)thereby enabling it to act as an lsquointernal re ecting and organizing agencyrsquo(Kaplan-Solms amp Solms 1996) This orbitofrontal role in lsquoself-re ectiveawarenessrsquo (Stuss Gow amp Hetherington 1992) allows an individual to reecton his or her own internal emotional states as well as those of others(Povinelli amp Preuss 1995) According to Fonagy and Target (1997) the reec-tive function is a mental operation that enables the perception of anotherrsquosstate The right hemisphere mediates empathic cognition and the perceptionof the emotional states of other human beings (Voeller 1986) andorbitofrontal function is essential to the capacity of inferring the states ofothers (Baron-Cohen 1995) This adaptive capacity may thus be the outcomeof a secure attachment to a psychobiologically attuned affect-regulating care-giver A recent neuropsychological study indicates that the orbitofrontalcortex is lsquoparticularly involved in theory of mind tasks with an affective com-ponentrsquo (Stone Baron-Cohen amp Knight 1998 p 651)

Furthermore the functioning of the orbitofrontal control system in theregulation of emotion (Baker Frith amp Dolan 1997) and in lsquoacquiring veryspecic forms of knowledge for regulating interpersonal and social behaviorrsquo(Dolan 1999 p 928) is central to self-regulation the ability to exibly regu-late emotional states through interactions with other humans ndash that is inter-active regulation in interconnected contexts ndash and without other humans ndashthat is autoregulation in autonomous contexts The adaptive capacity to shiftbetween these dual regulatory modes depending upon the social contextemerges out of a history of secure attachment interactions of a maturing bio-logical organism and an early attuned social environment

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 33

ATTACH MENT THEORY IS FUNDAMENTALLYA REGULATORY THEORY

Attachment behavior is currently thought to be the output of lsquoa neuro-biologically based biobehavioral system that regulates biological syn-chronicity between organismsrsquo (Wang 1997 p 168) I suggest that thecharacterization of the orbitofrontal system as a frontolimbic structure thatdetermines the regulatory signi cance of stimuli that reach the organism andregulates body state (Luria 1980) bears a striking resemblance to the behav-ioral control system characterized by Bowlby over 30 years ago The OxfordDictionary denes control as lsquothe act or power of directing or regulatingrsquo

Attachment theory as rst propounded in Bowlbyrsquos (1969) denitionalvolume is fundamentally a regulatory theory Attachment can thus be con-ceptualized as the interactive regulation of synchrony between psychobiolog-ically attuned organisms This attachment dynamic which operates at levelsbeneath awareness underlies the dyadic regulation of emotion Emotions arethe highest order direct expression of bioregulation in complex organisms(Damasio 1998) Imprinting the learning process it accesses is described byPetrovich and Gewirtz (1985) as synchrony between sequential infant mater-nal stimuli and behavior (see Schore 1994 and Nelson amp Panksepp 1998 formodels of the neurochemistry of attachment)

According to Feldman et al (1999) lsquoface-to-face synchrony affords infantstheir rst opportunity to practice interpersonal coordination of biologicalrhythmsrsquo (p 223) and acts as an interpersonal context in which lsquointeractantsintegrate into the ow of behavior the ongoing responses of their partner andthe changing inputs of the environmentrsquo (p 224) The visual prosodic-auditory and gestural stimuli embedded in these emotional communicationsare rapidly transmitted back and forth between the infantrsquos and motherrsquos faceand in these transactions the caregiver acts as a regulator of the childrsquos arousallevels

Because arousal levels are known to be associated with changes in meta-bolic energy the caregiver is thus modulating changes in the childrsquos energeticstate (Schore 1994 1997b) These regulated increases in energy metabolismare available for biosynthetic processes in the babyrsquos brain which is in thebrain growth spurt (Dobbing amp Sands 1973) In this manner lsquothe intrinsicregulators of human brain growth in a child are specically adapted to becoupled by emotional communication to the regulators of adult brainsrsquo(Trevarthen 1990 p 357)

In addition the mother also regulates moments of asynchrony that isstressful negative affect Social stressors can be characterized as the occur-rence of an asynchrony in an interactional sequence (Chapple 1970) Stressdescribes both the subjective experience induced by a distressing potentiallythreatening or novel situation and the organismrsquos reactions to a homeosta-tic challenge It is now thought that social stressors are lsquofar more detrimen-talrsquo than non-social aversive stimuli (Sgoifo et al 1999)

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 134

Separation stress in essence is a loss of maternal regulators of the infantrsquosimmature behavioral and physiological systems that results in the attachmentpatterns of protest despair and detachment The principle that lsquoa period ofsynchrony following the period of stress provides a ldquorecoveryrdquo periodrsquo(Chapple 1970 p 631) underlies the mechanism of interactive repair(Tronick 1989 Schore 1994) The primary caregiverrsquos interactive regulationis therefore critical to the infantrsquos maintaining positively charged as well ascoping with stressful negatively charged affects These affect regulatingevents are particularly impacting the organization of the early developingright hemisphere

Bowlbyrsquos control system is located in the right hemisphere that is not onlydominant for lsquoinhibitory controlrsquo (Garavan et al 1999) but also for the pro-cessing of facial information in infants (Deruelle amp de Schonen 1998) andadults (Kim et al 1999) and for the regulation of arousal (Heilman amp VanDen Abell 1979) Because the major coping systems the hypothalamo-pituitary-adrenocortical axis and the sympathetic-adrenomedullary axis areboth under the main control of the right cerebral cortex this hemisphere con-tains lsquoa unique response system preparing the organism to deal efcientlywith external challengesrsquo and so its adaptive functions mediate the humanstress response (Wittling 1997 p 55) Basic research in stress physiologyshows that the behavioral and physiological response of an individual to aspecic stressor is consistent over time (Koolhaas et al 1999)

These attachment transactions are imprinted into implicit-proceduralmemory as enduring internal working models which encode coping strat-egies of affect regulation (Schore 1994) that maintain basic regulation andpositive affect even in the face of environmental challenge (Sroufe 1989)Attachment patterns are now conceptualized as lsquopatterns of mental process-ing of information based on cognition and affect to create models of realityrsquo(Crittenden 1995 p 401) The lsquoanterior limbic prefrontal networkrsquo whichinterconnects the orbital and medial prefrontal cortex with the temporal polecingulate and amygdala lsquois involved in affective responses to events and inthe mnemonic processing and storage of these responsesrsquo (Carmichael ampPrice 1995 p 639) and lsquoconstitutes a mental control system that is essentialfor adjusting thinking and behavior to ongoing realityrsquo (Schnider amp Ptak1999 p 680) An ultimate indicator of secure attachment is resilience in theface of stress (Greenspan 1981) which is expressed in the capacity to ex-ibly regulate emotional states via autoregulation and interactive regulationHowever early social environments that engender insecure attachmentsinhibit the growth of this control system (Schore 1997b) and therefore pre-clude its adaptive coping function in lsquooperations linked to behavioral exi-bilityrsquo (Nobre et al 1999 p 12)

In support of Bowlbyrsquos assertion that the childrsquos capacity to cope withstress is correlated with certain maternal behaviors current developmentalbiological studies are exploring lsquomaternal effectsrsquo the inuence of themotherrsquos experiences on her progenyrsquos development and ability to adapt to

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 35

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

survival and enabling the organism to cope with stresses and challenges(Wittling amp Schweiger 1993)

There is a growing body of studies which shows that the infantrsquos earlymaturing (Geschwind amp Galaburda 1987) right hemisphere is specicallyimpacted by early social experiences (Schore 1994 1998b) This develop-mental principle is now supported in a recent single photon emissioncomputed tomographic (SPECT) study by Chiron et al (1997) whichdemonstrates that the right brain hemisphere is dominant in preverbal humaninfants and indeed for the rst 3 years of life I suggest that the ontogeneticshift of dominance from the right to left hemisphere after this time may expli-cate Bowlbyrsquos description of a diminution of the attachment system at theend of the third year that is due to an lsquoabruptrsquo passage of a lsquomaturationalthresholdrsquo

Current neuropsychological studies indicate that lsquothe emotional experi-ence(s) of the infant are disproportionately stored or processed in theright hemisphere during the formative stages of brain ontogenyrsquo (Semrud-Clikeman amp Hynd 1990 p 198) that lsquothe infant relies primarily on its pro-cedural memory systemsrsquo during lsquothe rst 2ndash3 years of lifersquo (Kandel 1999 p 513) and that the right brain contains the lsquocerebral representation of onersquosown pastrsquo and the substrate of affectively laden autobiographical memory(Fink et al 1996 p 4275) These ndings suggest that early-forming inter-nal working models of the attachment relationship are processed and storedin implicit-procedural memory systems in the right cortex the hemispheredominant for implicit learning (Hugdahl 1995)

In the securely attached individual these models encode an expectationthat lsquohomeostatic disruptions will be set rightrsquo (Pipp amp Harmon 1987 p 650) In discussing these internal models Rutter (1987) notes that lsquochildrenderive a set of expectations about their own relationship capacities and aboutother peoplersquos resources to their social overtures and interactions theseexpectations being created on the basis of their early parentndashchild attach-mentsrsquo (p 449) Such representations are processed by the orbitofrontalsystem which is known to be activated during lsquobreaches of expectationrsquo(Nobre Coull Frith amp Mesulam 1999) and to generate affect-regulatingstrategies for coping with expected negative and positive emotional states thatare inherent in intimate social contexts

The efcient operations of this regulatory system allow for corticallyprocessed information concerning the external environment (such as visualand auditory stimuli emanating from the emotional face of the attachmentobject) to be integrated with subcortically processed information regardingthe internal visceral environment (such as concurrent changes in the childrsquosemotional or bodily self-state) The relaying of sensory information into thelimbic system allows incoming information about the social environment totrigger adjustments in emotional and motivational states and in this mannerthe orbitofrontal system integrates what Bowlby termed environmental andorganismic models Recent ndings that the orbitofrontal cortex generates

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 132

nonconscious biases that guide behavior before conscious knowledge does(Bechara Damasio Tranel amp Damasio 1997) and codes the likely signicanceof future behavioral options (Dolan 1999) and represents an important siteof contact between emotional information and mechanisms of action selec-tion (Rolls 1996) are consonant with Bowlbyrsquos (1981) assertion that internalworking models are used as guides for future action

These mental representations according to Main Kaplan and Cassidy(1985) contain cognitive as well as affective components and act to guideappraisals of experience The orbitofrontal cortex is known to function as anappraisal mechanism (Pribram 1987 Schore 1998a) and to be centrallyinvolved in the generation of lsquocognitive-emotional interactionsrsquo (Barbas1995) It acts to lsquointegrate and assign emotional-motivational signicance tocognitive impressions the association of emotion with ideas and thoughtsrsquo(Joseph 1996 p 427) and in lsquothe processing of affect-related meaningsrsquo (Teas-dale et al 1999)

Orbitofrontal activity is associated with a lower threshold for awarenessof sensations of both external and internal origin (Goldenberg et al 1989)thereby enabling it to act as an lsquointernal re ecting and organizing agencyrsquo(Kaplan-Solms amp Solms 1996) This orbitofrontal role in lsquoself-re ectiveawarenessrsquo (Stuss Gow amp Hetherington 1992) allows an individual to reecton his or her own internal emotional states as well as those of others(Povinelli amp Preuss 1995) According to Fonagy and Target (1997) the reec-tive function is a mental operation that enables the perception of anotherrsquosstate The right hemisphere mediates empathic cognition and the perceptionof the emotional states of other human beings (Voeller 1986) andorbitofrontal function is essential to the capacity of inferring the states ofothers (Baron-Cohen 1995) This adaptive capacity may thus be the outcomeof a secure attachment to a psychobiologically attuned affect-regulating care-giver A recent neuropsychological study indicates that the orbitofrontalcortex is lsquoparticularly involved in theory of mind tasks with an affective com-ponentrsquo (Stone Baron-Cohen amp Knight 1998 p 651)

Furthermore the functioning of the orbitofrontal control system in theregulation of emotion (Baker Frith amp Dolan 1997) and in lsquoacquiring veryspecic forms of knowledge for regulating interpersonal and social behaviorrsquo(Dolan 1999 p 928) is central to self-regulation the ability to exibly regu-late emotional states through interactions with other humans ndash that is inter-active regulation in interconnected contexts ndash and without other humans ndashthat is autoregulation in autonomous contexts The adaptive capacity to shiftbetween these dual regulatory modes depending upon the social contextemerges out of a history of secure attachment interactions of a maturing bio-logical organism and an early attuned social environment

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 33

ATTACH MENT THEORY IS FUNDAMENTALLYA REGULATORY THEORY

Attachment behavior is currently thought to be the output of lsquoa neuro-biologically based biobehavioral system that regulates biological syn-chronicity between organismsrsquo (Wang 1997 p 168) I suggest that thecharacterization of the orbitofrontal system as a frontolimbic structure thatdetermines the regulatory signi cance of stimuli that reach the organism andregulates body state (Luria 1980) bears a striking resemblance to the behav-ioral control system characterized by Bowlby over 30 years ago The OxfordDictionary denes control as lsquothe act or power of directing or regulatingrsquo

Attachment theory as rst propounded in Bowlbyrsquos (1969) denitionalvolume is fundamentally a regulatory theory Attachment can thus be con-ceptualized as the interactive regulation of synchrony between psychobiolog-ically attuned organisms This attachment dynamic which operates at levelsbeneath awareness underlies the dyadic regulation of emotion Emotions arethe highest order direct expression of bioregulation in complex organisms(Damasio 1998) Imprinting the learning process it accesses is described byPetrovich and Gewirtz (1985) as synchrony between sequential infant mater-nal stimuli and behavior (see Schore 1994 and Nelson amp Panksepp 1998 formodels of the neurochemistry of attachment)

According to Feldman et al (1999) lsquoface-to-face synchrony affords infantstheir rst opportunity to practice interpersonal coordination of biologicalrhythmsrsquo (p 223) and acts as an interpersonal context in which lsquointeractantsintegrate into the ow of behavior the ongoing responses of their partner andthe changing inputs of the environmentrsquo (p 224) The visual prosodic-auditory and gestural stimuli embedded in these emotional communicationsare rapidly transmitted back and forth between the infantrsquos and motherrsquos faceand in these transactions the caregiver acts as a regulator of the childrsquos arousallevels

Because arousal levels are known to be associated with changes in meta-bolic energy the caregiver is thus modulating changes in the childrsquos energeticstate (Schore 1994 1997b) These regulated increases in energy metabolismare available for biosynthetic processes in the babyrsquos brain which is in thebrain growth spurt (Dobbing amp Sands 1973) In this manner lsquothe intrinsicregulators of human brain growth in a child are specically adapted to becoupled by emotional communication to the regulators of adult brainsrsquo(Trevarthen 1990 p 357)

In addition the mother also regulates moments of asynchrony that isstressful negative affect Social stressors can be characterized as the occur-rence of an asynchrony in an interactional sequence (Chapple 1970) Stressdescribes both the subjective experience induced by a distressing potentiallythreatening or novel situation and the organismrsquos reactions to a homeosta-tic challenge It is now thought that social stressors are lsquofar more detrimen-talrsquo than non-social aversive stimuli (Sgoifo et al 1999)

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 134

Separation stress in essence is a loss of maternal regulators of the infantrsquosimmature behavioral and physiological systems that results in the attachmentpatterns of protest despair and detachment The principle that lsquoa period ofsynchrony following the period of stress provides a ldquorecoveryrdquo periodrsquo(Chapple 1970 p 631) underlies the mechanism of interactive repair(Tronick 1989 Schore 1994) The primary caregiverrsquos interactive regulationis therefore critical to the infantrsquos maintaining positively charged as well ascoping with stressful negatively charged affects These affect regulatingevents are particularly impacting the organization of the early developingright hemisphere

Bowlbyrsquos control system is located in the right hemisphere that is not onlydominant for lsquoinhibitory controlrsquo (Garavan et al 1999) but also for the pro-cessing of facial information in infants (Deruelle amp de Schonen 1998) andadults (Kim et al 1999) and for the regulation of arousal (Heilman amp VanDen Abell 1979) Because the major coping systems the hypothalamo-pituitary-adrenocortical axis and the sympathetic-adrenomedullary axis areboth under the main control of the right cerebral cortex this hemisphere con-tains lsquoa unique response system preparing the organism to deal efcientlywith external challengesrsquo and so its adaptive functions mediate the humanstress response (Wittling 1997 p 55) Basic research in stress physiologyshows that the behavioral and physiological response of an individual to aspecic stressor is consistent over time (Koolhaas et al 1999)

These attachment transactions are imprinted into implicit-proceduralmemory as enduring internal working models which encode coping strat-egies of affect regulation (Schore 1994) that maintain basic regulation andpositive affect even in the face of environmental challenge (Sroufe 1989)Attachment patterns are now conceptualized as lsquopatterns of mental process-ing of information based on cognition and affect to create models of realityrsquo(Crittenden 1995 p 401) The lsquoanterior limbic prefrontal networkrsquo whichinterconnects the orbital and medial prefrontal cortex with the temporal polecingulate and amygdala lsquois involved in affective responses to events and inthe mnemonic processing and storage of these responsesrsquo (Carmichael ampPrice 1995 p 639) and lsquoconstitutes a mental control system that is essentialfor adjusting thinking and behavior to ongoing realityrsquo (Schnider amp Ptak1999 p 680) An ultimate indicator of secure attachment is resilience in theface of stress (Greenspan 1981) which is expressed in the capacity to ex-ibly regulate emotional states via autoregulation and interactive regulationHowever early social environments that engender insecure attachmentsinhibit the growth of this control system (Schore 1997b) and therefore pre-clude its adaptive coping function in lsquooperations linked to behavioral exi-bilityrsquo (Nobre et al 1999 p 12)

In support of Bowlbyrsquos assertion that the childrsquos capacity to cope withstress is correlated with certain maternal behaviors current developmentalbiological studies are exploring lsquomaternal effectsrsquo the inuence of themotherrsquos experiences on her progenyrsquos development and ability to adapt to

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 35

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

nonconscious biases that guide behavior before conscious knowledge does(Bechara Damasio Tranel amp Damasio 1997) and codes the likely signicanceof future behavioral options (Dolan 1999) and represents an important siteof contact between emotional information and mechanisms of action selec-tion (Rolls 1996) are consonant with Bowlbyrsquos (1981) assertion that internalworking models are used as guides for future action

These mental representations according to Main Kaplan and Cassidy(1985) contain cognitive as well as affective components and act to guideappraisals of experience The orbitofrontal cortex is known to function as anappraisal mechanism (Pribram 1987 Schore 1998a) and to be centrallyinvolved in the generation of lsquocognitive-emotional interactionsrsquo (Barbas1995) It acts to lsquointegrate and assign emotional-motivational signicance tocognitive impressions the association of emotion with ideas and thoughtsrsquo(Joseph 1996 p 427) and in lsquothe processing of affect-related meaningsrsquo (Teas-dale et al 1999)

Orbitofrontal activity is associated with a lower threshold for awarenessof sensations of both external and internal origin (Goldenberg et al 1989)thereby enabling it to act as an lsquointernal re ecting and organizing agencyrsquo(Kaplan-Solms amp Solms 1996) This orbitofrontal role in lsquoself-re ectiveawarenessrsquo (Stuss Gow amp Hetherington 1992) allows an individual to reecton his or her own internal emotional states as well as those of others(Povinelli amp Preuss 1995) According to Fonagy and Target (1997) the reec-tive function is a mental operation that enables the perception of anotherrsquosstate The right hemisphere mediates empathic cognition and the perceptionof the emotional states of other human beings (Voeller 1986) andorbitofrontal function is essential to the capacity of inferring the states ofothers (Baron-Cohen 1995) This adaptive capacity may thus be the outcomeof a secure attachment to a psychobiologically attuned affect-regulating care-giver A recent neuropsychological study indicates that the orbitofrontalcortex is lsquoparticularly involved in theory of mind tasks with an affective com-ponentrsquo (Stone Baron-Cohen amp Knight 1998 p 651)

Furthermore the functioning of the orbitofrontal control system in theregulation of emotion (Baker Frith amp Dolan 1997) and in lsquoacquiring veryspecic forms of knowledge for regulating interpersonal and social behaviorrsquo(Dolan 1999 p 928) is central to self-regulation the ability to exibly regu-late emotional states through interactions with other humans ndash that is inter-active regulation in interconnected contexts ndash and without other humans ndashthat is autoregulation in autonomous contexts The adaptive capacity to shiftbetween these dual regulatory modes depending upon the social contextemerges out of a history of secure attachment interactions of a maturing bio-logical organism and an early attuned social environment

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 33

ATTACH MENT THEORY IS FUNDAMENTALLYA REGULATORY THEORY

Attachment behavior is currently thought to be the output of lsquoa neuro-biologically based biobehavioral system that regulates biological syn-chronicity between organismsrsquo (Wang 1997 p 168) I suggest that thecharacterization of the orbitofrontal system as a frontolimbic structure thatdetermines the regulatory signi cance of stimuli that reach the organism andregulates body state (Luria 1980) bears a striking resemblance to the behav-ioral control system characterized by Bowlby over 30 years ago The OxfordDictionary denes control as lsquothe act or power of directing or regulatingrsquo

Attachment theory as rst propounded in Bowlbyrsquos (1969) denitionalvolume is fundamentally a regulatory theory Attachment can thus be con-ceptualized as the interactive regulation of synchrony between psychobiolog-ically attuned organisms This attachment dynamic which operates at levelsbeneath awareness underlies the dyadic regulation of emotion Emotions arethe highest order direct expression of bioregulation in complex organisms(Damasio 1998) Imprinting the learning process it accesses is described byPetrovich and Gewirtz (1985) as synchrony between sequential infant mater-nal stimuli and behavior (see Schore 1994 and Nelson amp Panksepp 1998 formodels of the neurochemistry of attachment)

According to Feldman et al (1999) lsquoface-to-face synchrony affords infantstheir rst opportunity to practice interpersonal coordination of biologicalrhythmsrsquo (p 223) and acts as an interpersonal context in which lsquointeractantsintegrate into the ow of behavior the ongoing responses of their partner andthe changing inputs of the environmentrsquo (p 224) The visual prosodic-auditory and gestural stimuli embedded in these emotional communicationsare rapidly transmitted back and forth between the infantrsquos and motherrsquos faceand in these transactions the caregiver acts as a regulator of the childrsquos arousallevels

Because arousal levels are known to be associated with changes in meta-bolic energy the caregiver is thus modulating changes in the childrsquos energeticstate (Schore 1994 1997b) These regulated increases in energy metabolismare available for biosynthetic processes in the babyrsquos brain which is in thebrain growth spurt (Dobbing amp Sands 1973) In this manner lsquothe intrinsicregulators of human brain growth in a child are specically adapted to becoupled by emotional communication to the regulators of adult brainsrsquo(Trevarthen 1990 p 357)

In addition the mother also regulates moments of asynchrony that isstressful negative affect Social stressors can be characterized as the occur-rence of an asynchrony in an interactional sequence (Chapple 1970) Stressdescribes both the subjective experience induced by a distressing potentiallythreatening or novel situation and the organismrsquos reactions to a homeosta-tic challenge It is now thought that social stressors are lsquofar more detrimen-talrsquo than non-social aversive stimuli (Sgoifo et al 1999)

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 134

Separation stress in essence is a loss of maternal regulators of the infantrsquosimmature behavioral and physiological systems that results in the attachmentpatterns of protest despair and detachment The principle that lsquoa period ofsynchrony following the period of stress provides a ldquorecoveryrdquo periodrsquo(Chapple 1970 p 631) underlies the mechanism of interactive repair(Tronick 1989 Schore 1994) The primary caregiverrsquos interactive regulationis therefore critical to the infantrsquos maintaining positively charged as well ascoping with stressful negatively charged affects These affect regulatingevents are particularly impacting the organization of the early developingright hemisphere

Bowlbyrsquos control system is located in the right hemisphere that is not onlydominant for lsquoinhibitory controlrsquo (Garavan et al 1999) but also for the pro-cessing of facial information in infants (Deruelle amp de Schonen 1998) andadults (Kim et al 1999) and for the regulation of arousal (Heilman amp VanDen Abell 1979) Because the major coping systems the hypothalamo-pituitary-adrenocortical axis and the sympathetic-adrenomedullary axis areboth under the main control of the right cerebral cortex this hemisphere con-tains lsquoa unique response system preparing the organism to deal efcientlywith external challengesrsquo and so its adaptive functions mediate the humanstress response (Wittling 1997 p 55) Basic research in stress physiologyshows that the behavioral and physiological response of an individual to aspecic stressor is consistent over time (Koolhaas et al 1999)

These attachment transactions are imprinted into implicit-proceduralmemory as enduring internal working models which encode coping strat-egies of affect regulation (Schore 1994) that maintain basic regulation andpositive affect even in the face of environmental challenge (Sroufe 1989)Attachment patterns are now conceptualized as lsquopatterns of mental process-ing of information based on cognition and affect to create models of realityrsquo(Crittenden 1995 p 401) The lsquoanterior limbic prefrontal networkrsquo whichinterconnects the orbital and medial prefrontal cortex with the temporal polecingulate and amygdala lsquois involved in affective responses to events and inthe mnemonic processing and storage of these responsesrsquo (Carmichael ampPrice 1995 p 639) and lsquoconstitutes a mental control system that is essentialfor adjusting thinking and behavior to ongoing realityrsquo (Schnider amp Ptak1999 p 680) An ultimate indicator of secure attachment is resilience in theface of stress (Greenspan 1981) which is expressed in the capacity to ex-ibly regulate emotional states via autoregulation and interactive regulationHowever early social environments that engender insecure attachmentsinhibit the growth of this control system (Schore 1997b) and therefore pre-clude its adaptive coping function in lsquooperations linked to behavioral exi-bilityrsquo (Nobre et al 1999 p 12)

In support of Bowlbyrsquos assertion that the childrsquos capacity to cope withstress is correlated with certain maternal behaviors current developmentalbiological studies are exploring lsquomaternal effectsrsquo the inuence of themotherrsquos experiences on her progenyrsquos development and ability to adapt to

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 35

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

ATTACH MENT THEORY IS FUNDAMENTALLYA REGULATORY THEORY

Attachment behavior is currently thought to be the output of lsquoa neuro-biologically based biobehavioral system that regulates biological syn-chronicity between organismsrsquo (Wang 1997 p 168) I suggest that thecharacterization of the orbitofrontal system as a frontolimbic structure thatdetermines the regulatory signi cance of stimuli that reach the organism andregulates body state (Luria 1980) bears a striking resemblance to the behav-ioral control system characterized by Bowlby over 30 years ago The OxfordDictionary denes control as lsquothe act or power of directing or regulatingrsquo

Attachment theory as rst propounded in Bowlbyrsquos (1969) denitionalvolume is fundamentally a regulatory theory Attachment can thus be con-ceptualized as the interactive regulation of synchrony between psychobiolog-ically attuned organisms This attachment dynamic which operates at levelsbeneath awareness underlies the dyadic regulation of emotion Emotions arethe highest order direct expression of bioregulation in complex organisms(Damasio 1998) Imprinting the learning process it accesses is described byPetrovich and Gewirtz (1985) as synchrony between sequential infant mater-nal stimuli and behavior (see Schore 1994 and Nelson amp Panksepp 1998 formodels of the neurochemistry of attachment)

According to Feldman et al (1999) lsquoface-to-face synchrony affords infantstheir rst opportunity to practice interpersonal coordination of biologicalrhythmsrsquo (p 223) and acts as an interpersonal context in which lsquointeractantsintegrate into the ow of behavior the ongoing responses of their partner andthe changing inputs of the environmentrsquo (p 224) The visual prosodic-auditory and gestural stimuli embedded in these emotional communicationsare rapidly transmitted back and forth between the infantrsquos and motherrsquos faceand in these transactions the caregiver acts as a regulator of the childrsquos arousallevels

Because arousal levels are known to be associated with changes in meta-bolic energy the caregiver is thus modulating changes in the childrsquos energeticstate (Schore 1994 1997b) These regulated increases in energy metabolismare available for biosynthetic processes in the babyrsquos brain which is in thebrain growth spurt (Dobbing amp Sands 1973) In this manner lsquothe intrinsicregulators of human brain growth in a child are specically adapted to becoupled by emotional communication to the regulators of adult brainsrsquo(Trevarthen 1990 p 357)

In addition the mother also regulates moments of asynchrony that isstressful negative affect Social stressors can be characterized as the occur-rence of an asynchrony in an interactional sequence (Chapple 1970) Stressdescribes both the subjective experience induced by a distressing potentiallythreatening or novel situation and the organismrsquos reactions to a homeosta-tic challenge It is now thought that social stressors are lsquofar more detrimen-talrsquo than non-social aversive stimuli (Sgoifo et al 1999)

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 134

Separation stress in essence is a loss of maternal regulators of the infantrsquosimmature behavioral and physiological systems that results in the attachmentpatterns of protest despair and detachment The principle that lsquoa period ofsynchrony following the period of stress provides a ldquorecoveryrdquo periodrsquo(Chapple 1970 p 631) underlies the mechanism of interactive repair(Tronick 1989 Schore 1994) The primary caregiverrsquos interactive regulationis therefore critical to the infantrsquos maintaining positively charged as well ascoping with stressful negatively charged affects These affect regulatingevents are particularly impacting the organization of the early developingright hemisphere

Bowlbyrsquos control system is located in the right hemisphere that is not onlydominant for lsquoinhibitory controlrsquo (Garavan et al 1999) but also for the pro-cessing of facial information in infants (Deruelle amp de Schonen 1998) andadults (Kim et al 1999) and for the regulation of arousal (Heilman amp VanDen Abell 1979) Because the major coping systems the hypothalamo-pituitary-adrenocortical axis and the sympathetic-adrenomedullary axis areboth under the main control of the right cerebral cortex this hemisphere con-tains lsquoa unique response system preparing the organism to deal efcientlywith external challengesrsquo and so its adaptive functions mediate the humanstress response (Wittling 1997 p 55) Basic research in stress physiologyshows that the behavioral and physiological response of an individual to aspecic stressor is consistent over time (Koolhaas et al 1999)

These attachment transactions are imprinted into implicit-proceduralmemory as enduring internal working models which encode coping strat-egies of affect regulation (Schore 1994) that maintain basic regulation andpositive affect even in the face of environmental challenge (Sroufe 1989)Attachment patterns are now conceptualized as lsquopatterns of mental process-ing of information based on cognition and affect to create models of realityrsquo(Crittenden 1995 p 401) The lsquoanterior limbic prefrontal networkrsquo whichinterconnects the orbital and medial prefrontal cortex with the temporal polecingulate and amygdala lsquois involved in affective responses to events and inthe mnemonic processing and storage of these responsesrsquo (Carmichael ampPrice 1995 p 639) and lsquoconstitutes a mental control system that is essentialfor adjusting thinking and behavior to ongoing realityrsquo (Schnider amp Ptak1999 p 680) An ultimate indicator of secure attachment is resilience in theface of stress (Greenspan 1981) which is expressed in the capacity to ex-ibly regulate emotional states via autoregulation and interactive regulationHowever early social environments that engender insecure attachmentsinhibit the growth of this control system (Schore 1997b) and therefore pre-clude its adaptive coping function in lsquooperations linked to behavioral exi-bilityrsquo (Nobre et al 1999 p 12)

In support of Bowlbyrsquos assertion that the childrsquos capacity to cope withstress is correlated with certain maternal behaviors current developmentalbiological studies are exploring lsquomaternal effectsrsquo the inuence of themotherrsquos experiences on her progenyrsquos development and ability to adapt to

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 35

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

Separation stress in essence is a loss of maternal regulators of the infantrsquosimmature behavioral and physiological systems that results in the attachmentpatterns of protest despair and detachment The principle that lsquoa period ofsynchrony following the period of stress provides a ldquorecoveryrdquo periodrsquo(Chapple 1970 p 631) underlies the mechanism of interactive repair(Tronick 1989 Schore 1994) The primary caregiverrsquos interactive regulationis therefore critical to the infantrsquos maintaining positively charged as well ascoping with stressful negatively charged affects These affect regulatingevents are particularly impacting the organization of the early developingright hemisphere

Bowlbyrsquos control system is located in the right hemisphere that is not onlydominant for lsquoinhibitory controlrsquo (Garavan et al 1999) but also for the pro-cessing of facial information in infants (Deruelle amp de Schonen 1998) andadults (Kim et al 1999) and for the regulation of arousal (Heilman amp VanDen Abell 1979) Because the major coping systems the hypothalamo-pituitary-adrenocortical axis and the sympathetic-adrenomedullary axis areboth under the main control of the right cerebral cortex this hemisphere con-tains lsquoa unique response system preparing the organism to deal efcientlywith external challengesrsquo and so its adaptive functions mediate the humanstress response (Wittling 1997 p 55) Basic research in stress physiologyshows that the behavioral and physiological response of an individual to aspecic stressor is consistent over time (Koolhaas et al 1999)

These attachment transactions are imprinted into implicit-proceduralmemory as enduring internal working models which encode coping strat-egies of affect regulation (Schore 1994) that maintain basic regulation andpositive affect even in the face of environmental challenge (Sroufe 1989)Attachment patterns are now conceptualized as lsquopatterns of mental process-ing of information based on cognition and affect to create models of realityrsquo(Crittenden 1995 p 401) The lsquoanterior limbic prefrontal networkrsquo whichinterconnects the orbital and medial prefrontal cortex with the temporal polecingulate and amygdala lsquois involved in affective responses to events and inthe mnemonic processing and storage of these responsesrsquo (Carmichael ampPrice 1995 p 639) and lsquoconstitutes a mental control system that is essentialfor adjusting thinking and behavior to ongoing realityrsquo (Schnider amp Ptak1999 p 680) An ultimate indicator of secure attachment is resilience in theface of stress (Greenspan 1981) which is expressed in the capacity to ex-ibly regulate emotional states via autoregulation and interactive regulationHowever early social environments that engender insecure attachmentsinhibit the growth of this control system (Schore 1997b) and therefore pre-clude its adaptive coping function in lsquooperations linked to behavioral exi-bilityrsquo (Nobre et al 1999 p 12)

In support of Bowlbyrsquos assertion that the childrsquos capacity to cope withstress is correlated with certain maternal behaviors current developmentalbiological studies are exploring lsquomaternal effectsrsquo the inuence of themotherrsquos experiences on her progenyrsquos development and ability to adapt to

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 35

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

its environment (Bernardo 1996) This body of research indicates that lsquovari-ations in maternal care can serve as the basis for a nongenomic behavioraltransmission of individual differences in stress reactivity across generationsrsquo(Francis Diorio Liu amp Meaney 1999 p 1155) and that lsquomaternal care duringinfancy serves to ldquoprogramrdquo behavioral responses to stress in the offspringrsquo(Caldji et al 1998 p 5335)

Recent developmental neurobiological ndings support the idea thatlsquoinfantsrsquo early experiences with their mothers (or absence of these experi-ences) may come to in uence how they respond to their own infants whenthey grow uprsquo (Fleming OrsquoDay amp Kraemer 1999 p 673) I suggest that theintergenerational transmission of stress-coping decits occurs within thecontext of relational environments that are growth-inhibiting to the develop-ment of regulatory corticolimbic circuits sculpted by early experiences (seeSchore in press e for a detailed discussion of the effects of early traumaticabuse andor neglect on right brain development) These attachment-relatedpsychopathologies are thus expressed in dysregulation of social behavioraland biological functions that are associated with an immature frontolimbiccontrol system and an inefcient right hemisphere (Schore 1994 19961997b in press e) This conceptualization directly bears upon Bowlbyrsquos(1978) assertion that attachment theory can be used to frame the early eti-ologies of a diverse group of psychiatric disorders and the neurophysiologi-cal changes that accompany them

FUTURE DIRECTIONS OF RESEARCH INTOREGULATORY PROCESSES

Returning to Attachment Bowlby asserts that lsquoThe merits of a scientictheory are to be judged in terms of the range of phenomena it embraces theinternal consistency of its structure the precision of the predictions it canmake and the practibility of testing themrsquo (1969 p 173) The republicationof this classic volume is occurring at a point in time coincident with thebeginning of the new millennium when we are now able to explore the neu-ropsychobiological substrata on which attachment theory is based In earlierwritings I have suggested that lsquothe primordial environment of the infant ormore properly of the commutual psychobiological environment shared bythe infant and mother represents a primal terra incognita of sciencersquo (Schore1994 p 64) The next generation of studies of Bowlbyrsquos theoretical landscapewill chart in detail how different early social environments and attachmentexperiences inuence the unique microtopography of a developing brain

Such studies will be projecting an experimental searchlight upon eventsoccurring at the common dynamic interface of brain systems that representthe psychological and biological realms The right-brain-to-right-brain psy-chobiological transactions that underlie attachment processes are bodilybased and critical to the adaptive capacities and growth of the infant This

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 136

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

calls for studies that concurrently measure brain behavioral and bodilychanges in both members of the dyad Autonomic measures of synchronouschanges to the infantrsquos and the motherrsquos bodily states need to be included instudies of attachment functions and the development of co-ordinated inter-actions between the maturing central and autonomic nervous systems shouldbe investigated in research on attachment structures

It is now accepted that internal working models that encode strategies ofaffect regulation act at levels beneath conscious awareness In a recent issueof the American Psychologist Bargh and Chartrand (1999 p 426) assert thatlsquomost of moment-to-moment psychological life must occur through non-conscious means if it is to occur at all various nonconscious mentalsystems perform the lionrsquos share of the self-regulatory burden benecientlykeeping the individual grounded in his or her lsquocurrent environmentrsquo Thischaracterization describes unconscious internal working models and sincetheir affective-cognitive components regulate and are regulated by the invol-untary autonomic nervous system these functions may very well be inacces-sible to self-report measures that mainly tap into conscious thoughts andimages

The psychobiological mechanisms that trigger organismic responses arefast-acting and dynamic Studying very rapid affective phenomena in realtime involves attention to a different time dimension from usual a focus oninterpersonal attachment and separations on a microtemporal scale Theemphasis is less on enduring traits and more on transient dynamic states andresearch methodologies will have to be created that can visualize the dyadicregulatory events occurring at the brainndashmindndashbody interface of two subjec-tivities that are engaged in attachment transactions

Since the human face is a central focus of these transactions studies of rightbrain appraisals of visual and prosodic facial stimuli even presented at tachis-toscopic levels may more accurately tap into the fundamental mechanismsthat are involved in the processing of social-emotional information And inlight of the principle that dyadic regulatory affective communications maxi-mize positive as well as minimize negative affect both procedures thatmeasure coping with negative affect ndash the Strange Situation ndash and those thatmeasure coping with positive affect ndash play situations ndash need to be used toevaluate attachment capacities

It is now established that face-to-face contexts of affect synchrony not onlygenerate positive arousal but also expose infants to high levels of social andcognitive information (Feldman et al 1999) In such interpersonal contextsincluding attachment-related lsquojoint attentionrsquo transactions (Schore 1994) thedeveloping child is exercising early attentional capacities There is now evi-dence to show that lsquointrinsic alertnessrsquo the most basic intensity aspect ofattention is mediated by a network in the right hemisphere (Sturm et al1999) In light of the known impaired functioning of right frontal circuits inattention-de cithyperactivity disorders (Casey et al 1997) developmentalattachment studies may elucidate the early etiology of these disorders as well

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 37

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

as of right hemisphere learning disabilities (Semrud-Klikeman amp Hynd 1990Gross-Tsur Shalev Manor amp Amir 1995)

Furthermore although most attachment studies refer to lsquoinfantsrsquo and lsquotod-dlersrsquo it is well known that the brain maturation rates of baby girls are sig-nicantly more advanced than boys Gender differences in infant emotionalregulation (Weinberg Tronick Cohn amp Olson 1999) and in the orbitofrontalsystem that mediates this function (Overman Bachevalier Schuhmann ampRyan 1996) have been demonstrated Studies of how different social experi-ences interact with different femalendashmale regional brain growth rates couldelucidate the origins of gender differences within the limbic system that arelater expressed in variations of social-emotional information processingbetween the sexes This research should include measures of lsquopsychologicalgenderrsquo (see Schore 1994) And in addition to maternal effects on early brainmaturation the effects of fathers especially in the second and third years onthe female and male toddlerrsquos psychoneurobiological development can tell usmore about paternal contributions to the childrsquos expanding stress copingcapacities

We must also more fully understand the very early pre- and postnatallymaturing limbic circuits that organize what Bowlby calls the lsquobuildingblocksrsquo of attachment experiences (Schore in press a d) Bowlby (1969) refersto a succession of increasingly sophisticated systems of limbic structures thatare involved in attachment (see Schore in press a d for an ontogenetic pro-gression of amygdala anterior cingulate insula and orbitofrontal cortex)Since attachment is the outcome of the childrsquos genetically encoded biological(temperamental) predisposition and the particular caregiver environment weneed to know more about the mechanisms of gene-environment interactionsThis work could elucidate the nature of the expression of particular genes inspecic brain regions that regulate stress reactivity as well as a deeper know-ledge of the dynamic components of lsquonon-sharedrsquo environmental factors(Plomin Rende amp Rutter 1991) It should be remembered that DNA levelsin the cortex signicantly increase over the rst year the period of attach-ment (Winick Rosso amp Waterlow 1970)

A very recent report of an association between perinatal complications(deviations of normal pregnancy labor-delivery and early neonatal develop-ment) and later signs of specically orbitofrontal dysfunction (Kinney et al2000) may elucidate the mechanism by which an interaction of a vulnerablegenetically-encoded psychobiological predisposition interacts with a misat-tuned relational environment to produce a high risk scenario for future dis-orders Orbitofrontal dysfunction in infancy has also been implicated in alater appearing impairment of not only social but moral behavior (Andersonet al 1999)

Furthermore developmental neuroscientic studies of the effects ofattuned and misattuned parental environments will reveal the subtle butimportant differences in brain organization among securely and insecurelyattached individuals as well as the psychobiological mechanisms that mediate

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 138

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

resilience to or risk for later-forming psychopathologies Neurobiologicalstudies now indicate that although the right prefrontal system is necessary tomount a normal stress response extreme alterations of such activity is mal-adaptive (Sullivan amp Gratton 1999) In line with the association of attach-ment experiences and the development of brain systems for coping withrelational stress future studies need to explore the relationship betweendifferent adaptive and maladaptive coping styles of various attachment cat-egories and correlated decits in brain systems involved in stress regulationSubjects classied on the Adult Attachment Inventory could be exposed toa real-life personally meaningful stressor and brain imaging and autonomicmeasures could then evaluate the individualrsquos adaptive or maladaptive regu-latory mechanisms Such studies can also elucidate the mechanisms of theintergenerational transmission of the regulatory decits of different classesof psychiatric disorders (see Schore 1994 1996 1997b)

In light of the fact that the right hemisphere subsequently re-enters intogrowth spurts (Thatcher 1994) and ultimately forms an interactive systemwith the later maturing left (Schore 1994 in press b Siegel 1999) neurobi-ological reorganizations of the attachment system and their functional cor-relates in ensuing stages of childhood and adulthood need to be exploredPsychoneurobiological research of the continuing experience-dependentmaturation of the right hemisphere could elucidate the underlying mechan-isms by which certain attachment patterns can change from lsquoinsecurityrsquo tolsquoearned securityrsquo (Phelps Belsky amp Crnic 1998)

The documented ndings that the orbitofrontal system is involved inlsquoemotion-related learningrsquo (Rolls Hornak Wade amp McGrath 1994) and thatit retains plasticity throughout later periods of life (Barbas 1995) may alsohelp us understand how developmentally-based affectively-focused psycho-therapy can alter early attachment patterns A recently published functionalmagnetic resonance imaging study (Hariri Bookheimer amp Mazziotta 2000)provides evidence that higher regions of specically the right prefrontalcortex attenuate emotional responses at the most basic levels in the brain thatsuch modulating processes are lsquofundamental to most modern psychothera-peutic methodsrsquo (p 43) that this lateralized neocortical network is active inlsquomodulating emotional experience through interpreting and labelingemotional expressionsrsquo (p 47) and that lsquothis form of modulation may beimpaired in various emotional disorders and may provide the basis for ther-apies of these same disordersrsquo (p 48) This process is a central component oftherapeutic narrative organization of turning lsquoraw feelings into symbolsrsquo(Holmes 1993 p 150) This lsquoneocortical networkrsquo which lsquomodulates thelimbic systemrsquo is identical to the right-lateralized orbitofrontal system thatregulates attachment dynamics Attachment models of motherndashinfant psy-chobiological attunement may thus be used to explore the origins of empathicprocesses in both development and psychotherapy and reveal the deepermechanisms of the growth-facilitating factors operating within the thera-peutic alliance (see Schore 1994 1997c in press b in preparation)

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 39

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

In a sense these deeper explorations into the early roots of the humanexperience have been waiting for not just theoretical advances in develop-mental neurobiology and technical improvements in methodologies that cannoninvasively image developing brain-mind-body processes in real time butalso for a perspective of brain-mind-body development that can bridge psy-chology and biology Such interdisciplinary models can shift back and forthbetween different levels of organization in order to accomodate heuristicconceptions of how the primordial experiences with the external social worldalters the ontogeny of internal structural systems Ultimately these psy-choneurobiological attachment models can be used as a scientic basis forcreating even more effective early prevention programs

In her concluding comments of a recent overview of the eld Mary Maina central gure in the continuing development of attachment theory writeslsquowe are currently at one of the most exciting junctures in the history of oureld We are now or will soon be in a position to begin mapping the rela-tions between individual differences in early attachment experiences andchanges in neurochemistry and brain organization In addition investigationof physiological ldquoregulatorsrdquo associated with infant-caregiver interactionscould have far-reaching implications for both clinical assessment and inter-ventionrsquo (1999 pp 881ndash882)

But I leave the nal word to Bowlby himself who in the last paragraph ofthis book sums up the meaning of his work

The truth is that the least-studied phase of human development remainsthe phase during which a child is acquiring all that makes him most dis-tinctively human Here is still a continent to conquer

REFERENCES

Ainsworth M D S (1967) Infancy in Uganda Infant care and the growth of loveBaltimore MD Johns Hopkins University Press

Ainsworth M D S (1969) Object relations dependency and attachment A theor-etical review of the infantndashmother relationship Child Development 40969ndash1025

Anders T F amp Zeanah C H (1984) Early infant development from a biologicalpoint of view In J D Call E Galenson amp R L Tyson (Eds) Frontiers of infantpsychiatry Vol 2 (pp 55ndash69) New York Basic Books

Anderson S W Bechara A Damasio H Tranel D amp Damasio A R (1999)Impairment of social and moral behavior related to early damage in humanprefrontal cortex Nature Neuroscience 2 1032ndash1037

Baker C C Frith C D amp Dolan R J (1997) The interaction between mood andcognitive function studied with PET Psychological Medicine 27 565ndash578

Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primateprefrontal cortex Neuroscience and Biobehavioral Reviews 19 499ndash510

Bargh J A amp Chartrand T L (1999) The unbearable automaticity of beingAmerican Psychologist 54 462ndash479

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 140

Baron-Cohen S (1995) Mindblindness An essay on autism and theory of mindCambridge MA MIT Press

Bechara A Damasio A R Damasio H amp Anderson S W (1994) Insensitivity tofuture consequences following damage to human prefrontal cortex Cognition50 7ndash15

Bernardo J (1996) Maternal effects in animal ecology American Zoologist 36 83ndash105Blair R J R Morris J S Frith C D Perrett D I amp Dolan R J (1999) Dis-

sociable neural responses to facial expressions of sadness and anger Brain 122883ndash893

Blood A J Zatorre R J Bermudez P amp Evans A C (1999) Emotional responsesto pleasant and unpleasant music correlate with activity in paralimbic brainregions Nature Neuroscience 2 382ndash387

Bowers D Bauer R M amp Heilman K M (1993) The nonverbal affect lexiconTheoretical perspectives from neuropsychological studies of affect perceptionNeuropsychology 7 433ndash444

Bowlby J (1940) The in uence of early environment in the development of neurosisand neurotic character International Journal of Psycho-Analysis 1 154ndash178

Bowlby J (1969) Attachment and loss Vol 1 Attachment New York BasicBooks

Bowlby J (1973) Attachment and loss Vol 2 Separation New York Basic BooksBowlby J (1978) Attachment theory and its therapeutic implications In S C

Feinstein amp P L Giovacchini (Eds) Adolescent psychiatry Developmental andclinical studies Chicago University of Chicago Press

Bowlby J (1981) Attachment and loss Vol 3 Loss sadness and depression NewYork Basic Books

Bretherton I amp Munholland K A (1999) Internal working models in attachmentrelationships A construct revisited In J Cassidy amp P R Shaver (Eds)Handbook of attachment Theory research and clinical applications (pp 89ndash111)New York Guilford Press

Carmichael S T amp Price J L (1995) Limbic connections of the orbital and medialprefrontal cortex in macaque monkeys Journal of Comparative Neurology 363615ndash641

Caldji C Tannenbaum B Sharma S Francis D Plotsky P M amp Meaney M J(1998) Maternal care during infancy regulates the development of neural systemsmediating the expression of fearfulness in the rat Proceedings of the NationalAcademy of Sciences of the United States of America 95 5335ndash5340

Casey B J Castellanos F X Giedd J N Marsh W L Hamburger S D SchubertA B Vauss Y C Vaituzis A C Dickstein D P Sarfatti S E amp RapoportJ L (1997) Implication of right frontostriatal circuitry in response inhibitionand attention-decithyperactivity disorders Journal of the American Academyof Child and Adolescent Psychiatry 36 374ndash383

Cassidy J amp Shaver P R (1999) Handbook of attachment Theory research andclinical applications New York Guilford Press

Chapple E D (1970) Experimental production of transients in human interactionNature 228 630ndash633

Chiron Jambaque I Nabbout R Lounes R Syrota A amp Dulac O (1997) Theright brain hemisphere is dominant in human infants Brain 120 1057ndash1065

Critchley H Daly E Philips M Brammer M Bullmore E Williams S VanAmelsvoort T Robertson D David A amp Murphy D (2000) Explicit and

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 41

implicit neural mechanisms for processing of social information from facialexpressions A functional magnetic resonance imaging study Human BrainMapping 9 93ndash105

Crittenden P M (1995) Attachment and psychopathology In S Goldberg R Muiramp J Kerr (Eds) Attachment theory Social developmental and clinical perspec-tives (pp 367ndash406) Mahweh NJ Analytic Press

Darwin C (1872) The expression of emotion in man and animals Reprint ChicagoUniversity of Chicago Press 1965

Derryberry D amp Tucker D M (1992) Neural mechanisms of emotion Journal ofClinical and Consulting Psychology 60 329ndash338

Deruelle C amp de Schonen S (1998) Do the right and left hemispheres attend to thesame visuospatial information within a face in infancy DevelopmentalNeuropsychology 14 535ndash554

Dobbing J amp Sands J (1973) Quantitative growth and development of humanbrain Archives of Diseases of Childhood 48 757ndash767

Dolan R J (1999) On the neurology of morals Nature Neuroscience 2 927ndash929Elliott R Frith C D amp Dolan R J (1997) Differential neural response to positive

and negative feedback in planning and guessing tasks Neuropsychologia 351395ndash1404

Feldman R Greenbaum C W amp Yirmiya N (1999) Motherndashinfant affectsynchrony as an antecedent of the emergence of self-control DevelopmentalPsychology 35 223ndash231

Field T (1985) Attachment as psychobiological attunement Being on the same wave-length In M Reite amp T Field (Eds) The psychobiology of attachment and separ-ation (pp 415ndash454) Orlando FL Academic Press

Fink G R Markowitsch H J Reinkemeier M Bruckbauer T Kessler J amp HeissW-D (1996) Cerebral representation of onersquos own past Neural networksinvolved in autobiographical memory Journal of Neuroscience 16 4275ndash4282

Fleming A S OrsquoDay D H amp Kraemer G W (1999) Neurobiology ofmotherndashinfant interactions experience and central nervous system plasticityacross development and generations Neuroscience and Biobehavioral Reviews23 673ndash685

Fonagy P amp Target M (1997) lsquoAttachment and reective function Their role inself-organizationrsquo Development and Psychopathology 9 679ndash700

Francis D Diorio J Liu D amp Meaney M J (1999) Nongenomic transmissionacross generations of maternal behavior and stress responses in the rat Science286 1155ndash1158

Francis S Rolls E T Bowtell R McGlone F OrsquoDoherty J Browning A ClareS amp Smith E (1999) The representation of pleasant touch in the brain and itsrelationship with taste and olfactory areas Cognitive Neuroscience 10 453ndash459

Freud S (1895) Project for a scientic psychology The Standard Edition ofthe Psychological Works of Sigmund Freud (J Strachey Ed) (Vol 1) LondonHogarth Press

Freud S (1925) An autobiographical study The Standard Edition of the PsychologicalWorks of Sigmund Freud (J Strachey Ed) (Vol 20) London Hogarth Press

Garavan H Ross T J amp Stein E A (1999) Right hemisphere dominance ofinhibitory control An event-related functional MRI study Proceedings of theNational Academy of Sciences of the United States of America 96 8301ndash8306

Geschwind N amp Galaburda A M (1987) Cerebral lateralization Biologicalmechanisms associations and pathology Boston MA MIT Press

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 142

Goldberg S Muir R amp Kerr J (1995) Attachment theory Social developmentaland clinical perspectives Mahweh NJ Analytic Press

Goldenberg G Podreka I Uhl F Steiner M Willmes K amp Deecke L (1989)Cerebral correlates of imagining colours faces and a map ndash I SPECT of regionalcerebral blood ow Neuropsychologia 27 1315ndash1328

Greenspan S (1981) Psychopathology and adaptation in infancy and early childhoodNew York International Universities Press

Gross-Tsur V Shalev R S Manor O amp Amir N (1995) Developmental right-hemisphere syndrome Clinical spectrum of the nonverbal learning disabilityJournal of Learning Disabilities 28 80ndash86

Hariri A R Bookheimer S Y amp Mazziotta J C (2000) Modulating emotionalresponses Effects of a neocortical network on the limbic system NeuroReport11 43ndash48

Heilman K M amp Van Den Abell T (1979) Right hemispheric dominance formediating cerebral activation Neuropsychologia 17 315ndash321

Henry J P (1993) Psychological and physiological responses to stress The righthemisphere and the hypothalamo-pituitary-adrenal axis an inquiry into prob-lems of human bonding Integrative Physiological and Behavioral Science 28369ndash387

Hinde R (1990) Causes of social development from the perspective of an integrateddevelopmental science In G Butterworth amp P Bryant (Eds) Causes of develop-ment (pp 161ndash185) Mahweh NJ Erlbaum

Holmes J (1993) John Bowlby and attachment theory London RoutledgeHugdahl K (1995) Classical conditioning and implicit learning the right hemisphere

hypothesis In R J Davidson amp K Hugdahl (Eds) Brain asymmetry (pp235ndash267) Cambridge MA MIT Press

Joseph R (1996) Neuropsychiatry neuropsychology and clinical neuroscience (3rded) Baltimore MD Williams amp Wilkins

Kandel E R (1999) Biology and the future of psychoanalysis A new intellectualframework for psychiatry revisited American Journal of Psychiatry 156505ndash524

Kaplan-Solms K amp Solms M (1996) Psychoanalytic observations on a case offrontal-limbic disease Journal of Clinical Psychoanalysis 5 405ndash438

Keenan J P McCutcheon B Freund S Gallup G C Jr Sanders G amp Pascual-Leone A (1999) Left hand advantage in a self-face recognition task Neuropsy-chologia 37 1421ndash1425

Kim J J Andreasen N C OrsquoLeary D S Wiser A K Boles Ponto L L WatkinsG L amp Hichwa R D (1999) Direct comparison of the neural substrates ofrecognition memory for words and faces Brain 122 1069ndash1083

Kinney D K Steingard R J Renshaw P F amp Yurgelun-Todd D A (2000)Perinatal complications and abnormal proton metabolite concentrations infrontal cortex of adolescents seen on magnetic resonance spectroscopyNeuropsychiatry Neuropsychology and Behavioral Neurology 13 8ndash12

Kinney H C Brody B A Kloman A S amp Gilles F H (1988) Sequence of centralnervous system myelination in human infancy II Patterns of myelination inautopsied infants Journal of Neuropathology and Experimental Neurology 47217ndash234

Kobak R R amp Sceery A (1988) Attachment in late adolescence Working modelsaffect regulation and representations of self and others Child Development 59135ndash146

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 43

Koolhaas J M Korte S M De Boer S F Van derr Vegt B J Van Reenen C GHopster H De Jong I C Ruis M A W amp Blokhuis H J (1999) Copingstyles in animals Current status in behavior and stress-physiology Neuroscienceand Biobehavioral Reviews 23 73ndash102

Lewis M D (1995) Cognition-emotion feedback and the self-organization ofdevelopmental paths Human Development 38 71ndash102

Lewis M D (1999) A new dynamic systems method for the analysis of early socio-emotional development Developmental Science 2 457ndash475

Lewis M D (in press) The promise of dynamic systems approaches for an integratedaccount of humna devleopment Child Development

Luria A R (1980) Higher cortical functions in man (2nd ed) New York BasicBooks

Main M (1999) Epilogue Attachment theory Eighteen points with suggestions forfuture studies In J Cassidy amp P R Shaver (Eds) Handbook of attachmentTheory research and clinical applications (pp 845ndash887) New York GuilfordPress

Main M Kaplan N amp Cassidy J (1985) Security in infancy childhood andadulthood A move to the level of representation Monographs of the Society forResearch in Child Development 50 66ndash104

Mesulam M-M (1998) From sensation to cognition Brain 121 1013ndash1052Nelson E E amp Panksepp J (1998) Brain substrates of infantndashmother attachment

contributions of opioids oxytocin and norepinephrine Neuroscience amp Bio-behavioral Reviews 22 437ndash452

Nobre A C Coull J T Frith C D amp Mesulam M-M (1999) Orbitofrontalcortex is activated during breaches of expectation in tasks of visual attentionNature Neuroscience 2 11ndash12

Overman W H Bachevalier J Schuhmann E amp Ryan P (1996) Cognitive genderdifferences in very young children parallel biologically based cognitive genderdifferences in monkeys Behavioral Neuroscience 110 673ndash684

Penman R Meares R amp Milgrom-Friedman J (1983) Synchrony in motherndashinfantinteraction A possible neurophysiological base British Journal of MedicalPsychology 56 1ndash7

Petrovich S B amp Gewirtz J L (1985) The attachment learning process and itsrelation to cultural and biological evolution Proximate and ultimate consider-ations In M Reite amp T Field (Eds) The psychobiology of attachment and separ-ation (pp 259ndash291) Orlando FL Academic Press

Phelps J L Belsky J amp Crnic K (1998) Earned security daily stress andparenting A comparison of ve alternative models Development and Psycho-pathology 10 21ndash38

Pizzagalli D Regard M amp Lehmann D (1999) Rapid emotional face processingin the human right and left brain hemispheres An ERP study NeuroReport 102691ndash2698

Pipp S amp Harmon R J (1987) Attachment as regulation A commentary ChildDevopment 58 648ndash652

Plomin R Rende R amp Rutter M (1991) Quantitative genetics and developmentalpsychopathology In D Cicchetti amp S L Toth (Eds) Internalizing andexternalizing expressions of dysfunction Rochester symposium on developmentalpsychopathology Vol 2 (pp 155ndash202) Mahweh NJ Erlbaum

Polan H J amp Hofer M A (1999) Psychobiological origins of infant attachment and

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 144

separation responses In J Cassidy amp P R Shaver (Eds) Handbook of attach-ment Theory research and clinical application (pp 162ndash180) New YorkGuilford Press

Povinelli D amp Preuss T M (1995) Theory of mind evolutionary history of acognitive specialization Trends in Neuroscience 18 418ndash424

Pribram K H (1987) The subdivisions of the frontal cortex revisited In E Perecman(Ed) The frontal lobes revisited (pp 11ndash39) Mahweh NJ Erlbaum

Price J L Carmichael S T amp Drevets W C (1996) Networks related to the orbitaland medial prefrontal cortex a substrate for emotional behavior Progress inBrain Research 107 523ndash536

Rabinowicz T (1979) The differentiate maturation of the human cerebral cortex InF Falkner amp J M Tanner (Eds) Human growth Vol 3 Neurobiology andnutrition (pp 97ndash123) New York Plenum Press

Reite M amp Capitanio J P (1985) On the nature of social separation and attach-ment In M Reite amp T Field (Eds) The psychobiology of attachment and separ-ation (pp 223ndash255) Orlando FL Academic Press

Rolls E T (1986) Neural systems involved in emotion in primates In R Plutchik ampH Kellerman (Eds) Emotion theory research and practice Vol 3 (pp125ndash143) Orlando FL Academic Press

Rolls E T (1996) The orbitofrontal cortex Philosophical Transactions of the RoyalSociety of London B 351 1433ndash1444

Rolls E T Hornak J Wade D amp McGrath J (1994) Emotion-related learning inpatients with social and emotional changes associated with frontal lobe damageJournal of Neurology Neurosurgery and Psychiatry 57 1518ndash1524

Romanski L M Tian B Fritz J Mishkin M Goldman-Rakic P S ampRauschecker J P (1999) Dual streams of auditory afferents target multipledomains in the primate prefrontal cortex Nature Neuroscience 2 1131ndash1136

Rutter M (1987) Temperament personality and personality disorder British Journalof Psychiatry 150 443ndash458

Ryan R M Kuhl J amp Deci E L (1997) Nature and autonomy An organizationalview of social and neurobiological aspects of self-regulation in behavior anddevelopment Development and Psychopathology 9 701ndash728

Scalaidhe S P Wilson F A W amp Goldman-Rakic P S (1997) Areal segregationof face-processing neurons in prefrontal cortex Science 278 1135ndash1138

Schnider A amp Ptak R (1999) Spontaneous confabulators fail to suppress currentlyirrelevant memory traces Nature Neuroscience 2 677ndash681

Schore A N (1994) Affect regulation and the origin of the self The neurobiology ofemotional development Mahweh NJ Erlbaum

Schore A N (1996) The experience-dependent maturation of a regulatory system inthe orbital prefrontal cortex and the origin of developmental psychopathologyDevelopment and Psychopathology 8 59ndash87

Schore A N (1997a) A century after Freudrsquos project Is a rapprochement betweenpsychoanalysis and neurobiology at hand Journal of the American Psycho-analytic Association 45 841ndash867

Schore A N (1997b) Early organization of the nonlinear right brain and develop-ment of a predisposition to psychiatric disorders Development and Psycho-pathology 9 595ndash631

Schore A N (1997c) Interdisciplinary developmental research as a source of clinicalmodels In M Moskowitz C Monk C Kaye amp S Ellman (Eds) The

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 45

neuro-biological and developmental basis for psychotherapeutic intervention (pp1ndash71) Northvale NJ Aronson

Schore A N (1998a) The experience-dependent maturation of an evaluative systemin the cortex In K Pribram (Ed) Brain and values Is a biological science ofvalues possible (pp 337ndash358) Mahweh NJ Erlbaum

Schore A N (1998b) Early shame experiences and infant brain development In PGilbert amp B Andrews Shame interpersonal behavior psychopathology andculture (pp 57ndash77) New York Oxford University Press

Schore A N (1999) Commentary on emotions Neuro-psychoanalytic viewsNeuro-Psychoanalysis 1 49ndash55

Schore A N (2000) Foreword to the reissue of Attachment and Loss Vol 1 Attach-ment by John Bowlby New York Basic Books

Schore A N (in press a) The self-organization of the right brain and the neuro-biology of emotional development In M D Lewis amp I Granic (Eds) Emotiondevelopment and self-organization New York Cambridge University Press

Schore A N (in press b) Clinical implications of a psychoneurobiological model ofprojective identication In S Alhanati (Ed) Primitive mental states Vol lllPre- and peri-natal inuences on personality development New York ESFPublishers

Schore A N (in press c) The right brain as the neurobiological substratum of Freudrsquosdynamic unconscious In D Scharff amp J Scharff (Eds) Freud at the millenniumThe evolution and application of psychoanalysis New York Other Press

Schore A N (in press d) The effects of a secure attachment relationship on rightbrain development affect regulation and infant mental health Infant MentalHealth Journal

Schore A N (in press e) The effects of relational trauma on right brain develop-ment affect regulation and infant mental health Infant Mental Health Journal

Schore A N (in preparation) Affect regulation and the repair of the self New YorkGuilford Press

Semrud-Clikeman M amp Hynd G W (1990) Right hemisphere dysfunction innonverbal learning disabilities Social academic and adaptive functioning inadults and children Psychological Bulletin 107 196ndash209

Sgoifo A Koolhaas J De Boer S Musso E Stilli D Buwalda B amp Meerlo P(1999) Social stress autonomic neural activation and cardiac activity in ratsNeuroscience and Biobehavioral Reviews 23 915ndash923

Shapiro D Jamner L D amp Spence S (1997) Cerebral laterality repressive copingautonomic arousal and human bonding Acta Physiologica Scandinavica Supple-ment 640 60ndash64

Siegel D J (1999) The developing mind Toward a neurobiology of interpersonalexperience New York Guilford Press

Spence S Shapiro D amp Zaidel E (1996) The role of the right hemisphere in thephysiological and cognitive components of emotional processing Psychophysi-ology 33 112ndash122

Sroufe L A (1989) Relationships self and individual adaptation In A J Sameroffamp R N Emde (Eds) Relationship disturbances in early childhood (pp 70ndash94)New York Basic Books

Sroufe L A (1996) Emotional development The organization of emotional life inthe early years New York Cambridge University Press

Starkstein S E amp Robinson R G (1997) Mechanism of disinhibition after brainlesions Journal of Nervous and Mental Disease 185 108ndash114

AT TA C H M E N T amp H U M A N D E V E L O P M E N T VOL 2 NO 146

Stone V E Baron-Cohen S amp Knight R T (1998) Frontal lobe contributions totheory of mind Journal of Cognitive Neuroscience 10 640ndash656

Sturm W de Simone A Krause B J Specht K Heselmann V Radermacher IHerzog H Tellann L Muller-Gartner H-W amp Willmes K (1999) Func-tional anatomy of intrinsic alertness evidence for a fronto-parietal-thalamic-brainstem network in the right hemisphere Neuropsychologia 37 797ndash805

Stuss D T Gow C A amp Hetherington C R (1992) lsquoNo longer Gagersquo Frontallobe dysfunction and emotional changes Journal of Consulting and ClinicalPsychology 60 349ndash359

Sullivan R M amp Gratton A (1999) Lateralized effects of medial prefrontal cortexlesions on neuroendocrine and autonomic stress responses in rats Journal ofNeuroscience 19 2834ndash2840

Teasdale J D Howard R J Cox S G Ha Y Brammer M J Williams S C Ramp Checkley S A (1999) Functional MRI study of the cognitive generation ofaffect American Journal of Psychiatry 156 209ndash215

Thatcher R W (1994) Cyclical cortical reorganization Origins of human cognitivedevelopment In G Dawson amp K W Fischer (Eds) Human behavior and thedeveloping brain (pp 232ndash266) New York Guilford Press

Tremblay L amp Schultz W (1999) Relative reward preference in primateorbitofrontal cortex Nature 398 704ndash708

Trevarthen C (1990) Growth and education of the hemispheres In C Trevarthen(Ed) Brain circuits and functions of the mind (pp 334ndash363) CambridgeCambridge University Press

Tucker D M (1992) Developing emotions and cortical networks In M R Gunnaramp C A Nelson (Eds) Minnesota symposium on child psychology Vol 24Developmental behavioral neuroscience (pp 75ndash128) Mahweh NJ Erlbaum

Voeller K K S (1986) Right-hemisphere decit syndrome in children AmericanJournal of Psychiatry 143 1004ndash1009

Wang S (1997) Traumatic stress and attachment Acta Physiologica ScandinavicaSupplement 640 164ndash169

Weinberg M K Tronick E Z Cohn J F amp Olson K L (1999) Gender differ-ences in emotional expressivity and self-regulation during infancy Develop-mental Psychology 35 175ndash188

Westin D (1997) Towards a clinically and empirically sound theory of motivationInternational Journal of Psychoanalysis 78 521ndash548

Winick M Rosso P amp Waterlow J (1970) Cellular growth of the cerebrum cere-bellum and brain stem in normal and marasmic children ExperimentalNeurology 26 393ndash400

Wittling W (1997) The right hemisphere and the human stress response Acta Phys-iologica Scandinavica Supplement 640 55ndash59

Wittling W amp Schweiger E (1993) Neuroendocrine brain asymmetry and physicalcomplaints Neuropsychologia 31 591ndash608

Zald D H amp Kim S W (1996) Anatomy and function of the orbital frontal cortexII Function and relevance to obsessive-compulsive disorder Journal ofNeuropsychiatry 8 249ndash261

S C H O R E AT TA C H M E N T A N D T H E R I G H T B R A I N 47