From emotion resonance to empathic understanding: A social developmental neuroscience account

From emotion resonance to empathicunderstanding: A social developmentalneuroscience account

JEAN DECETYaAND MEGHAN MEYERb

aUniversity of Chicago; and bStanford University School of Medicine

Abstract

The psychological construct of empathy refers to an intersubjective induction process by which positive and negativeemotions are shared, without losing sight of whose feelings belong to whom. Empathy can lead to personal distress or toempathic concern (sympathy). The goal of this paper is to address the underlying cognitive processes and their neuralunderpinnings that constitute empathy within a developmental neuroscience perspective. In addition, we focus onhow these processes go awry in developmental disorders marked by impairments in social cognition, such as autismspectrum disorder, and conduct disorder. We argue that empathy involves both bottom-up and top-down informationprocessing, underpinned by specific and interacting neural systems. We discuss data from developmental psychologyas well as cognitive neuroscience in support of such a model, and highlight the impact of neural dysfunctions on socialcognitive developmental behavior. Altogether, bridging developmental science and cognitive neuroscience helpsapproach a more complete understanding of social cognition. Synthesizing these two domains also contributes to a bettercharacterization of developmental psychopathologies that impacts the development of effective treatment strategies.

While enjoying a walk in the park with your son,you suddenly notice a young woman with a sadexpression on her face who is sitting on a benchreading a letter. A wave of melancholy consumesyou, and your son and you both express a wish toconsole thewoman. This natural tendency to shareand understand the emotions and feelings of oth-ers in relation to oneself, whether one actually wit-nesses another person’s expression, perceived itfrom a photograph, read about it in a fictive novel,or imagined it, refers to the phenomenological ex-perience of empathy.

Various domains of psychology suggest thatone function of empathy is to promote social in-

teraction. For example, social psychologists re-gard empathy as a proximate factor motivatingprosocial behavior (Batson, 1991; Davis, 1994).Similarly, a large tradition in developmental sci-ence has been to study the onset and developmentof empathy, as some theorists suggest that empa-thy plays a crucial role in moral development,motivating prosocial behavior and inhibiting ag-gression toward others (e.g., Hoffman, 2001;Miller & Eisenberg, 1988). Indeed, empathy de-velops from infancy, and by 2 years of age mostchildren manifest prosocial helping responses’ toothers’ distress (Zahn-Waxler & Radke-Yarrow,1990). In contrast, certain developmental disor-ders, such as autism spectrum disorder (ASD)and conduct disorder (CD) are marked by empa-thy deficits that likely influence their antisocial re-sponses to other’s distress, albeit with aloof apa-thy or active aggression, respectively.

The link between empathy and social inter-action likely derives from the relationship be-tween empathy and intersubjectivity. It has been

Address correspondence and reprint requests to: JeanDecety, Departments of Psychology and Psychiatry andCenter for Cognitive and Social Neuroscience, Universityof Chicago, 5848 South University Avenue, Chicago, IL60637; E-mail: [email protected].

The writing of this manuscript was supported by NSF GrantBCS 0718480 (to J.D.).

Development and Psychopathology 20 (2008), 1053–1080Copyright # 2008 Cambridge University PressPrinted in the United States of Americadoi:10.1017/S0954579408000503

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postulated that empathy is a primary source of in-tersubjectivity, as the sense of shared experienceis a prerequisite for understanding what drivesother people’s intentions, emotions, and motiva-tions (Gallagher, 2001; Meltzoff & Decety,2003; Trevarthen & Aitken, 2001). That is, inter-subjectivity, the ability to share the subjectivestates of others and resonate with their perspec-tive, strongly relies on the ability to read (in thesense of reacting and understanding) others’ emo-tions to determine their psychological state. In-deed, the absence of intersubjectivity deprivesindividuals of the opportunity to develop proso-cial behaviors, empathy, and moral judgmentsthat are important byproducts of developing so-cial cognition (Rochat & Striano, 1999).

In addition to intersubjectivity, empathy is alsophenomenologically tied to psychological con-structs that may be partly innate in humans, offer-ing further evidence of the evolutionary basis offorming social bonds, and the role of empathy inthis process. Indeed, some of the basic buildingblocks of empathy, such as emotion sharing andan ecological sense of self, seem to be presentin the first days of life, suggesting a neurobio-logically based predisposition for humans to beconnected to others (Rochat, 2002). These pro-cesses prepare the individual for later empathicconnections through affective interaction withothers. Humans are indeed social animals, and vir-tually all of their actions are directed toward or areproduced in response to others (Batson, 1990).Humans rely on others for survival and are en-dowed with a motivation to form and maintainstrong interpersonal relationships, what Baumeis-ter and Leary (1995) have termed “the need tobelong.”

Recent data from cognitive neuroscience alsooffer new insights regarding the neural mecha-nisms and brain areas that underpin empathy(Decety & Jackson, 2004, 2006; Decety &Lamm, 2006; Leiberg & Anders, 2006). Thegoal of this paper is to address the underlying cog-nitive–neural architecture that instantiates empa-thy and to highlight the dysfunction of these pro-cesses in developmental disorders marked bysocial–cognitive impairments. Based on empiri-cal findings from cognitive neuroscience and de-velopmental science, we argue that a number ofcomponents contribute to the experience ofempathy: (a) affective sharing, a bottom-up pro-

cess grounded in perception–action couplingand potentially underpinned by mirror neuron sys-tems; (b) the ability to differentiate oneself from aperceived target, which relies on a sense ofagency, self-, and other awareness, and likely in-volves frontoparietal and prefrontal circuits; and(c) executive functions instantiated in the prefron-tal cortex (PFC), which operate as a top-down me-diator, helping to regulate emotions and yieldmental flexibility (Figure 1). Taken together,drawing from these multiple sources of data helppaint a more complete picture of the phenomeno-logical experience of empathy, as well as the re-spective mechanisms driving the phenomenon.

A Clarification of Terms

Empathy is a loaded term, with various definitionsroaming the literature. Broadly construed, empa-thy has been defined as an affective responsestemming from the understanding of another’semotional state or condition similar to what theother person is feeling or would be expected tofeel in the given situation (Eisenberg, Shea, Carlo,& Knight, 1991). In line with this conception, em-pathy can concede an interaction between twoindividuals, with one experiencing and sharingthe feeling of the other (Feshbach, 1997). Othertheorists more narrowly define empathy as onespecific set of congruent emotions, those feelingsthat are more other focused than self-focused (Bat-son, Fultz, & Schoenrade, 1987). Similarly, ac-cording to Hoffman (2000), empathy refers tothe psychological processes that allow a personto experience feelings more congruent with an-other’s situation than with his own situation.

Many developmental theories highlight therole of empathy in moral development, suggest-ing that when humans experience others’ emo-tions of distress they are motivated to respondwith prosocial help (Eisenberg, Spinrad, &Sadovsky, 2006). However, whether experienc-ing others’ emotional states entails prosocial re-sponding is unclear. During perspective-takingtasks (using cognitive means to adopt anotherperson’s point of view), social psychological re-search demonstrates that when individuals imag-ine how the other person would feel in a givensituation versus how they would feel in thesame situation, different emotions arise: the indi-viduals are prone to feel sympathy for the other in

J. Decety and M. Meyer1054

the former, whereas the latter can lead to personaldistress, that is, a self-oriented aversive emotionalresponse such as anxiety or discomfort (Batson,Early, & Salvarani, 1997). Personal distressmay lead an observer to relieve her own stress,and not necessarily help the other. Thus, it seemsthat the cognitive means used to assess an auto-matic shared affective statewith another’s distressinfluences the likeliness to respond prosocially.In the following sections, we review the affectiveand cognitive components that give way to empa-thy, reviewing first the automatic proclivity toshare emotions with others, and the cognitiveprocess of perspective taking and executive con-trol, which allow individuals to be aware of theirintentions and feelings and keep separate self andother perspectives.

Here we will consider empathy as a kind of in-duction process by which emotions, both positiveand negative, are automatically shared. Empathycan be the source of an emotional response ema-nating from the self and directed to the other, aconceptualization congruent with many scholars(see Table 1). It is important that such a definitionstresses the distinction between empathic concernand personal distress, both of which spring fromempathy but have different goals and conse-quences. Furthermore, we will consider the con-struct of empathy within an overarching concep-tual framework. This framework suggests thatempathy involves parallel and distributed pro-cessing in a number of dissociable neurocompu-tational mechanisms (Figure 1). Shared neuralcircuits, self-awareness, mental flexibility, and

Figure 1. Schematic representation of bottom-up (i.e., direct matching between perception and action) andtop-down (i.e., regulation and control) information processes involved in empathy. These two levels of pro-cessing are interrelated. The low level, which is automatically activated (unless inhibited) by perceptual in-put, accounts for emotion sharing. Executive functions, implemented in the prefrontal cortex, serve to reg-ulate both cognition and emotion, notably through selective attention and self-regulation. This metalevel iscontinuously updated by bottom-up information, and in return controls the lower level by providing top-down input. Thus, the top-down regulation, through executive functions modulates low levels and adds flex-ibility, making the individual less dependent on external cues. The metacognitive feedback plays a crucialrole in taking into account one’s own mental competence in order to react (or not) to the affective states ofothers.

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emotion regulation constitute the basic macro-components of empathy, which are mediated byspecific and interacting neural circuits, includingaspects of the PFC, insula, limbic system, andfrontoparietal networks. Consequently, thismodel assumes and predicts that dysfunction ineach of these macrocomponents may lead to analteration of the experience of empathy, andcorrespond with selective social cognitive disor-ders depending on which aspect is disrupted(Decety & Moriguchi, 2007).

In the following sections, we marshal sup-port for this model by discussing first the be-havioral evidence and then the putative neuralmechanisms that underpin them. We also sug-gest that inadequacies in these mechanismsmay help account for various social–cognitivedisorders. These sections are organized accord-ing to each major aspect that contributes toempathy: emotion sharing, self- or other aware-ness, and executive control and emotion regula-tion. We conclude by speculating on the conse-quences of the experience of empathy in moralreasoning. We believe that combining develop-mental science with cognitive neuroscience can

provide a more comprehensive understandingof empathy and related emotions, which alsohas the potential for generating new hypothesesregarding social–cognitive disorders and thuscontributes to better treatment and interventionin developmental psychopathology.

Emotion Sharing

The automaticity of emotion sharing

Bodily expressions help humans and other ani-mals communicate various types of informationto members of their species. Specifically, emo-tional expression and perception play pivotalroles in human social interaction (Schulkin,2005). Emotions are short-lived psychological–physiological phenomena that represent efficientmodes of adaptation to changing environmentaldemands. It has long been suggested that emo-tion expression is an evolutionary adaptationthat facilitates survival (Darwin, 1872). Such aclaim is supported by the observation that rulesgovern emotional expressions, which can beelicited by simple stimuli, as in the example ofdisgust in the presence of bitter taste, as well asthe speculation that detection of emotional ex-pression offers clear adaptive advantages, par-ticularly in the formation and maintenance of so-cial relationships.

Emotional expression not only informs an in-dividual of another’s subjective (and physiologi-cal) experience but also serves as a sort of socialglue maintaining emotional reciprocity amongdyads and groups. Emotional contagion, definedas the tendency to automatically mimic andsynchronize facial expressions, vocalizations,postures, and movements with those of anotherperson and, consequently, converge emotionallywith the other (Hatfield, Cacioppo, & Rapson,1994) is a social phenomenon of shared emotionalexpression that given its automaticity occurs at abasic level outside of conscious awareness.

From infancy, complex facial motor patternspermit infants to match facial emotion expres-sions with others (e.g., Field, Woodson, Green-berg, & Cohen, 1982; Haviland & Lelwica,1987). Very young infants are able to send emo-tional signals and to receive and detect the emo-tional signals sent by others. Shortly after birth,healthy infants convey facial expressions of

Table 1. Definitions of empathy

† The ability to put oneself into the mental shoes ofanother person to understand her emotions andfeelings (a form of simulation or inner imitation;Goldman, 1993)

† A complex form of psychological inference inwhich observation, memory, knowledge, andreasoning are combined to yield insights into thethoughts and feelings of others (Ickes, 1997)

† An affective response more appropriate tosomeone else’s situation than to one’s own(Hoffman, 1975)

† An other-oriented emotional response congruentwith the other’s perceived welfare (Batson, Sager,et al., 1997)

† An affective response that stems from theapprehension or comprehension of another’semotional state or condition and that is similar towhat the other person is feeling or would beexpected to feel in the given situation (Eisenberg,2000)

Note: These definitions point to an emotional experiencethat is more congruent with another’s situation than withone’s own. Another important aspect of the construct of em-pathy is that it must involve some sort of self–other differ-entiation, which makes it distinct from related reactionssuch as emotional contagion.


interest, sadness, and disgust (Field, 1989). Like-wise, discrete facial expressions of emotion havebeen identified in newborns, including joy, inter-est, disgust, and distress (Izard, 1982). These find-ings suggest that subcomponents of full emo-tional expressions are present at birth (Table 2),supporting the possibility that these processesare hard wired in the brain. It has been suggestedthat infant arousal in response to feelings, affects,and emotions signaled by others serves as aninstrument for social learning, reinforcing thesignificance of the social exchange, which thenbecome associated with the infant’s own emo-tional experience (Nielsen, 2002). Consequently,infants would come to experience emotions asshared states and learn to differentiate their ownstates, in part, by witnessing the resonant re-sponses they elicit in others. This automatic emo-tional resonance between other and self providesthe basic mechanism on which social cognition ingeneral and empathy in particular later develops.

Infant affective resonance manifests in infantcry reactions to peer crying. One-day-old infantsselectively cry in response to the vocal character-istics of another infant’s cry, a finding that led tothe speculation that from birth infants are en-dowed with an innate precursor of empathic dis-tress (Hoffman, 1975). Moreover, infants ex-posed to newborn cries cry significantly moreoften than those exposed to silence and those ex-posed to a synthetic newborn cry of the same in-tensity (Sagi & Hoffman, 1976). The findingdemonstrates that infants’ auditory perception ofanother’s aversive affective state elicits the samedistressful emotional state in the self. Importantly,this reaction exists before infants develop a senseof others as physical entities distinct from the self(Hastings, Zahn-Waxler, & McShane, 2006).This convergence between the self and other’saversive affective experience reflects the instan-tiation of the initial building block that precedesthe experience of empathy: a behavior matchingresponse to other’s emotional states.

Infants experience emotion contagion throughinteraction with their caretakers. Such a behaviorscaffolds what Bowlby (1958) termed attach-ment, that is, the inclination to seek proximity toanother person and feel secure in the presenceof that person. Attachment theory fits neatlywith evolutionary theory, which contends thatkin-related altruism and reciprocal altruism (a po-

tential result of empathy) may reflect activation ofbrain processes that mediate social attachments(Panksepp, 1986). By the first months of infant-hood, infants recognize and mimic the distinctemotions of their mothers, a behavior that ulti-mately facilitates attachment (Haviland & Leli-vica, 1987). This resonance or echoing of affect,feelings, and emotions that takes place in the re-ciprocal interaction between infants and theircaretakers is a necessary element for the develop-ment of empathy and advanced social cognition(Rochat & Striano, 1999).

The primary source of intersubjectivity im-pacts the quality of the infant’s affective state.For example, 3-month-old infants of depressedmothers are less inclined to match emotional stateswith their mother than 3-month-old infants ofnondepressed mothers. For instance, depressedmothers and their infants synchronize negative ex-pression states more frequently than nondepressedmothers and their infants (Field, Healy, Goldstein,& Guthertz, 1990). This seems to indicate that un-der normal conditions, mothers stimulate andarouse their infant while modulating their infant’sbehavior. Through this process, mother and in-fant’s emotional expression synchronize. Emo-tional unavailability and affective unresponsive-ness may lead to the lack of such emotional

Table 2. Classification of three basiccategories of subjective experiences

† Feelings correspond to the perception of privateexperiences such as pain, hunger, or frustration.This category of subjective experiences in generalterminates following particular actions such asfeeding for hunger, comfort for pain, or fulfilling agoal for frustration.

† Affects qualify the perception of a general moodor perceived private tone that exists as abackground to both feelings and emotions.Affects are diffused and protracted in comparisonto feelings. They fluctuate along a continuumfrom low to high tone.

† Emotions are the actual observable expressions offeelings and affections by invariant movementdynamics, postures, and facial display as in theexpressions of pain, joy, disgust, sadness,surprise, and anger.

Note: Rochat and Striano (1999) introduced a useful classi-fication of three basic categories of subjective experienceswhich are often confused in the literature, and which in-clude feelings, affects and emotions.


modulation among the depressed mother–infantdyad. The greater matching of negative emotionamong depressed mother–infant dyad likely re-flects experienced emotion contagion of negativeaffect. This interpretation is in line with findingsrelated to atypical autonomic arousal in anxiouslyattached children, a likely aftermath attachmentstyle of infants raised by depressed mothers. Au-tonomic arousal is associated with degree of facialmimicry, with anxiously depressed childrenshowing increased arousal in response to negativefacial expressions (Rogeness, Cepeda, Macedo,Fischer, & Harris, 1990).

Infants of healthy, nondepressed mothersshow similar behaviors to the infants of depressedmothers in experiments using perturbation tests inwhich researchers disrupted the flow of contin-gent expression modulation between healthymothers and infants. In the still or blank facetest (Tronick & Weinberg, 1997) a mother whopreviously established a protoconversationalflow with her infant arrests her expression, andlooks to the infant without a response to the in-fant’s behavior. Infants show several petitionsfor communication via smiling, vocalizing, andgesturing. When the mother continues to adopta “still face,” the infants show eye contact avoid-ance and distress, much like the infant’s reactionsto depressed mother’s despondent affective state.

Results from the still face perturbation testhave been replicated, however, using a double-video DTV link so that infants who are a fewweeks old and mothers could communicate live(Weinberg & Tronick, 1996). After rhythmiccommunication stabilized, a 1-min recording ofthe mother’s behavior was rewound and re-played. In this case, the mother’s behavior wasno longer contingent with the infant’s move-ments. The infants intermittently tried to interactwith the taped behavior, and showed confusionwhen the mother failed to respond with similartiming or appropriate expression, and eventuallyshowed prolonged distress and avoidance. It is ofinterest that replay of the infant’s behavior to themother caused the mother to feel uncomfortable,and verbal reports demonstrate that she worriedthat the infant was unable “to connect.” It shouldbe noted that many scholars remain skeptical ofsuch findings related to early infant intersubjec-tivity as measured by video dialogue between in-fant and mother. Attempt to replicate these results

show mixed success, and furthermore, research-ers of the reproduced studies interpret the infants’interactive behaviors as nothing more than socialcontingency outside of intersubjectivity (for a re-view, see Rochat, 1999).

In sum, the developmental data suggest thatthe mechanism subserving emotion (as theobservable expressions of feelings and affects)sharing between infant and caretaker is immedi-ately present from birth. Newborns are innatelyand highly attuned to other people and motivatedto socially interact with others. From the earliestmonths of their lives, infants engage with otherpeople and with the actions and feelings ex-pressed through other people’s bodies (Hobson,2002; Rochat & Striano, 2002). Such a mecha-nism is grounded in the automatic perception–ac-tion coupling of sensorimotor information, whichseems present at birth in some form. This mimicrybetween self and other is critical for many facetsof social functioning. For instance, it facilitates at-tachment and provides information about the oth-er’s emotional state. Mimicry also constitutes aprimary source of interpersonal engagementwith others, what has been termed primary inter-subjectivity (Gallagher & Meltzoff, 1996; Galla-gher, 2004). This mechanism provides the foun-dation for understanding that others are “likeme,” and underlie the development of theory ofmind and empathy for others (Meltzoff & Decety,2003). In the following section, we discuss in de-tail the mechanism that drives emotional sharingand mimicry, the direct link between perceptionand action.

Perception–action coupling mechanismand the mirror neuron system

The automatic mapping between self and other issupported by considerable empirical literature inthe domain of perception and action, which hasbeen marshaled under the prominent common-coding theory. This theory claims that somewherein the chain of operation that leads from percep-tion to action, the system generates certain deriva-tives of stimulation and certain antecedents ofaction that are commensurate in the sense thatthey share the same system of representational di-mensions (Prinz, 1997). The core assumption ofthe common coding theory is that actions arecoded in terms of the perceivable effects (i.e.,


the distal perceptual events) they should generate.Performing a movement leaves behind a bidi-rectional association between the motor patternit was generated by and the sensory effects thatit produces. Such an association can then beused backward to retrieve a movement by antici-pating its effects (Hommel, Musseler, Aschersle-ben, & Prinz, 2001). These perception–actioncodes are also accessible during action observa-tion, and perception activates action representa-tions to the degree that the perceived and the rep-resented actions are similar. Such a mechanismhas also been proposed to account for emotionsharing and its contribution to the experience ofempathy (Decety, 2002; Decety & Jackson,2004; Preston & de Waal, 2002). In the contextof emotion processing, it is posited that percep-tion of emotion activates in the observer theneural mechanisms that are responsible for thegeneration of similar emotion. It should be notedthat a similar mechanism was previously pro-posed to account for emotion contagion. Indeed,Hatfield et al. (1994) argued that people catch theemotions of others as a result of afferent feedbackgenerated by elementary motor mimicry ofothers’ expressive behavior, which produces a si-multaneous matching emotional experience.

Neurophysiological evidence for this percep-tion–action coupling comes from electrophysio-logical recordings in monkeys in which a uniqueclass of visuomotor neurons have been found inthe ventral premotor and posterior parietal corti-ces. These neurons, called mirror neurons, areactive during a specific motor action and theperception of the same action made byanother in-dividual (Rizzolatti, Fogassi, & Gallese, 2001).Evidence for the existence of mirror neurons inhumans is more indirect, and principally relieson functional neuroimaging studies that indicatethat the neural circuits involved in action execu-tion overlap with those activated when actionsare observed (Blakemore & Decety, 2001; Dec-ety & Grezes, 2006), as well as transcranialmagnetic stimulation (TMS) and motor-evokedpotentials (MEP) studies that show changes inthe excitability of the observer’s brain regionsthat encode the execution of observed actions(Fadiga & Craighero, 2004). This shared neuralnetwork for action production and observationincludes the premotor cortex, the inferior frontalgyrus, the parietal lobule, the supplementary

motor area, and the cerebellum. Recent neuro-imaging experiments demonstrate that the mir-ror–neuron system is flexible, and that experi-ence and motivation modulate its functioning.For instance, regions that belong to the mirror–neuron system showed greater hemodynamic re-sponse when hungry participants were pre-sented with videos of people grasping food. Incontrast, decreased activity was detected in theseregions when participants were in a satiated state(Cheng, Meltzoff, & Decety, 2007). In addition,a number of neuroimaging studies have shownthat similar brain areas, pertaining to the samenetwork are reliably activated during imaginingone’s own action, imagining another’s action,and imitating actions performed by a model(Decety & Chaminade, 2003; Decety & Grezes,2006). For instance, a similar neural network isengaged when individuals observe or imitateemotional facial expressions (Carr, Iacoboni, Du-beau, Mazziotta, & Lenzi, 2003). Within this net-work, there is greater activity during imitation,compared with observation of emotions, in pre-motor areas including the inferior frontal cortex,as well as in the superior temporal cortex, insula,and amygdala. Such shared neural circuits reflectan automatic transformation of other people’s be-havior (actions or emotions) into the neural repre-sentation of one’s own behavior, and provides afunctional bridge between first and third personperspectives, culminating in empathic experi-ence (Decety & Sommerville, 2003; Sommer-ville & Decety, 2006).

The perception of other people in pain has re-vealed to be of particular importance for the in-vestigation of the neural mechanisms underlyingempathy. Pain is a window through which onecan obtain a detailed view of the cognitive andneurophysiological mechanism underlying theexperiences of empathy and sympathy. The per-ception of pain in others thus constitutes an eco-logically valid way to investigate the mecha-nisms underpinning the experience of empathyfor two main reasons: first, most humans under-stand what is “pain”; it is acommon and universalexperience; and understands what are its physicaland psychological manifestations; second, wehave good knowledge about the neurophysio-logical pathways that are involved in processingnociceptive information that include the somato-sensory cortex, the supplementary motor area


(SMA), the anterior midcingulate cortex (aMCC),the insula, the periaqueductal gray (PAG), andthalamus. Numerous functional magnetic reso-nance imaging (fMRI) studies have shown thatwhen we perceive other people in pain, theneural circuits underpinning the processing offirst-hand experience of pain are activated inthe observer (for a meta-analysis, see Jackson,Rainville, & Decety, 2006). In one recent study,typically developing middle school-aged chil-dren were scanned while observing dynamic vi-sual stimuli depicting other people in pain (Dec-ety, Michalska, & Akitsuki, 2008). Resultsshow that neural circuits subserving the process-ing of nociceptive information are recruited bythe sight of other people in pain (Figure 2).Such a pattern of activation in children shouldnot be surprising given the behavioral and phys-iological data that document that affective shar-ing and vicarious emotional arousal, especiallyin response to others distress, is hard wiredand functional very early in life (e.g., Eisenberg& Eggum, 2008; Hoffman, 2000). This rudi-mentary capacity for resonating with the painof others may trigger empathic distress in the ob-server, and provides the affective and motiva-tional base for moral development (Hoffman,1982).

It can be speculated that the perception–action coupling physiological mechanism is al-ready present at birth and develops graduallythrough experience and exposure to actions per-formed by self and others (Lepage & Theoret,2007). This will account for neonate imitationas demonstrated by the work of Meltzoff andMoore (1997). Recent empirical findings offerevidence for a mirror neuron system encodingperceived and executed human action in thechild’s developing brain. For instance, onestudy recorded electroencephalographic signalsvia intracranial electrodes from a 36-month-oldchild with epilepsy while the infant observed anexperimenter either drew with his right hand orkept his right hand still (Fecteau et al., 2004).Cortical areas responding to the observationof biological movements partially overlappedwith those that were active during the executionof the same movements. An electrophysiologi-cal study demonstrated that the neural responseto the processing of biological motion was inplace by 8 months (Hirai & Hiraki, 2005).

Mirror neuron dysfunction in ASD

Burgeoning research efforts suggest that anaberrant mirror neuron system may contribute tomotor and social problems experienced in ASD.Research with humans using TMS demonstratesselective changes in the amplitude of the MEPs(M1) during action observation (e.g., Fadiga, Fo-gassi, Pavesi, & Rizzolati, 1995). To build on thisfinding, TMS was applied over the motor cortexof adults with ASD and matched healthy controls.Compared to the controls, individuals with ASDshowed significantly less M1 amplitude changeduring the observation of transitive, meaninglessfinger movements (Theoret et al., 2005). In con-trast, observation of the finger movements in con-trol subjects selectively modulated the excitabilityof the motor cortex in areas delivering signals tothe muscles concerned with the observed action.The weaker M1 modulation in individuals withASD suggests that the less mirror neuron activa-tion in the motor cortex may be partly responsi-ble for a cascade of deficits in social cognition.

The fMRI experiments are in line with theseTMS findings, and indicate abnormal activationof mirror neuron systems during imitation inadults with Asperger syndrome (Nishitani, Avi-kainen, & Hari, 2003) and reduced functionalconnectivity in mirror neuron system areas (Vil-lalobos, Mizuno, Dahl, Kemmostsu, & Muller,2004). In attempt to examine a potential link be-tween mirror neuron dysfunction and develop-mental delay of social cognitive skills, onefMRI study found a lack of activation in theinferior frontal gyrus (a key mirror neuron area)in children with ASD compared to controls dur-ing the observation and imitation of basic facialemotion expression (Dapretto et al., 2006). How-ever, this finding was recently challenged byBastiaanen, Thioux, and Keysers (2008, April),who scanned a group of 17 adults with ASD dur-ing the observation of dynamic facial expres-sions, including disgust. The authors found thatASD participants activate their mirror systemnot less, but more strongly than controls whenobserving dynamic facial expressions.

Structural neuroanatomical evidence also im-plicates aberrations in mirror neuron systems inASD. One morphometric study reported locallydiminished gray matter in adults with high-func-tioning ASD in areas incorporated in the mirror


neuron system compared to controls matched forgender, age, intelligence quotient, and handed-ness (Hadjikhani, Joseph, Snyder, & Gager-Flushber, 2005). Cortical thinning of the mirrorsystem was correlated with the severity of ASDsymptoms (as measured scores on the Autism Di-agnostic Interview—Revised), and cortical thin-ning was also seen in areas engaged in emotionrecognition and social cognition. Thus, irregularthinning of cortical areas that implement mirrorneurons and the broader network of cortical areassubserving social cognition may contribute to theemotional deficits characteristic of autism, such as

problems engaging in intersubjective transactionsand displays of empathic responding. It should benoted, however, that in the tables included in thepaper, not only mirror neuron cortical areas, butall areas of the brain, show a significant reductionof gray matter. Thus, one needs to be cautiouswith these new findings, as cortical thinningmay not be specific to areas where mirror neuronsare located. In fact, an earlier study using magne-toecephalography failed to find any difference inmotor cortex activation between individuals withASD and healthy controls while observing action(Avikainen, Kulomaki, & Hari, 1999), a result

Figure 2. In this fMRI study, 17 typically developing children (9 + 1 years) were scanned while presentedwith short dynamic (2.2-s duration) visual stimuli depicting painful and nonpainful situations (Decety et al.,2008). These situations involved either (a) a person whose pain was caused by accident or (c) a person whosepain was intentionally inflicted by another individual, as well as situations without any pain with one or twoagents for baseline. Consistent with previous fMRI studies of pain empathy with adults, the perception ofother people in pain in children was associated with increased neurohemodynamic activity in the neural cir-cuits involved in the processing of first-hand experience of pain, including the insula, somatosensory cortex(not shown), the aMCC, PAG, and SMA. (b) It was important that when children observed an individualharming another, regions of the prefrontal cortex that are consistently involved in representing social inter-action and moral behavior such as the temporoparietal junction (not shown), (d) the paracingulate cortex(PCC), and orbitofrontal cortex (OFC) were also recruited. Of interest, children indicated in the postscandebriefing that they thought that the situations in which pain was caused by another person were unfair,and they asked about the reason that could explain this behavior.


that is in contradiction with the study by Theoretand colleagues (2005).

Perhaps more convincing evidence of anom-alies in the mirror neuron system in ASD derivesfrom EEG studies that examine mu rhythm in sen-sorimotor areas. Robust evidence suggests that themagnitude of mu rhythm in sensorimotor areas isstrongly suppressed during the execution and ob-servation of an action in adults (e.g., Muthuku-maraswamy, Johnson, & McNair, 2003) and typi-cally developing children (Lepage & Theoret,2006). In children and adults with high-function-ing ASD, however, mu rhythm suppression oc-curs when individuals observe their own action,however it fails to suppress during the observationof other persons’ action (Oberman et al., 2005),suggesting dysfunction in mirror neuron systems.Moreover, this result did not significantly corre-late with age, implicating that this deficit mani-fests early and shows little improvement withage. Bernier, Dawson, Webb, and Murias (2007)extended these results to show that in individualswith high-functioning ASD, the degree of muwave suppression during action observation is as-sociated with behavioral assessments of imitationability. That is, less mu suppression correlateswith poorer imitation abilities, and is most robustfor facial imitation skills.

Together, these recent findings, which needto be replicated, seem to suggest that dysfunc-tions of the mirror neuron system may hamperthe normal development of self–other connect-edness, creating a cascade of deficient processesthat lead to social deficits, including empathy.However, it is worth noting that this account isstill debated, and that the results from a recentfMRI study do not support a global failure ofthe mirror neuron system in children with autism(Hamilton, Brindley, & Frith, 2007). In the fol-lowing section we consider the implications ofperception–action coupling deficits in a behav-ior that is considered a manifestation of emotioncontagion, which is facial mimicry.

Facial mimicry of emotions in childrenwith ASD and developmental coordinationdisorder (DCD)

An effective means to measure the role of percep-tion–action coupling in emotion sharing is viaelectromyography (EMG) recording of the activa-

tion of specific facial muscles in response to view-ing other people’s facial expressions. Facial mimi-cry has been defined narrowly as the congruentfacial reactions to the emotional facial displaysof others, and is thus an expressive component(Hess & Blairy, 2001). More broadly construed,emotion contagion is an affective state thatmatches the other’s emotional display. Thus, fa-cial mimicrycan beconceived of as a physical man-ifestation of emotion contagion, and it occurs at anautomatic level in response to viewing others’ emo-tions (Bush, Barr, McHugo, & Lanzetta, 1989).

Individuals with ASD are often reported tolack automatic and spontaneous mimicry of facialexpressions. A recent study measured adolescentsand adults with ASD and controls’ automatic andvoluntary mimicry of emotional facial expres-sions via EMG recordings of the cheek andbrow muscle regions while participants viewedstill photographs of happy, angry, and neutral fa-cial expressions (McIntosh, Reichmann-Decker,Winkelman, & Wilbarger, 2006). The cheek andbrow muscles of individuals with ASD failed toactivate in response to the videos, indicating thatthey did not automatically mimic the facial ex-pressions, whereas the muscles of the normallydeveloping controls showed activation. It isimportant that both groups showed evidence ofsuccessful voluntary mimicry. Difficulties in mi-micking other people’s emotional expressionmay thus prevent individuals with ASD from theafferent feedback that informs them of what othersare feeling (Rogers, 1999). Indeed, in real-life sit-uations, individuals with ASD are likely drawingon distinct cognitive processing when gaugingothers’ emotional states (Baron-Cohen, 2002).

Other developmental disorders known fortheir motor deficits are less obviously tied toproblems with emotion sharing and empathy.For example, DCD is characterized by delayedmotor development and weak motor skills, aswell as poor social skills, including deficientempathy (Gillberg, 1992). It is plausible thatpoor motor skills are the primary problem, be-cause a child with motor deficits may beshunned from social inclusion. Alternatively,the child may purposefully engage him/herselfin activities beyond the realm of physical activ-ity, for example, indulge in mathematics. Thus,weak social skills may develop by default asmuch of social interaction relies on motor


skills, especially in childhood. However, chil-dren with DCD show information processingdeficits, specifically in visual–spatial process-ing (Wilson & McKenzi, 1998). Such a weak-ness would influence perception–action cou-pling of emotional expression. Therefore, themechanism underlying their difficulty in coor-dinating movements may also contribute totheir inability empathize.

One study tried to tease out the nature of therelationship between motor skills and socialskills in children with DCD (Cummins, Piek, &Dyck, 2005). In a sample of 39 children withDCD and 39 normally developing children, chil-dren with motor problems performed worse onscales that measured the capacity to recognizestatic and dynamic facial expressions of emotion.What is more, when visuospatial processing wascontrolled, this difference remained; thus, thechild’s motor ability was a significant predictorof social behavior. Children with DCD’s motorimpairments may negatively influence their abil-ity to calibrate sensorimotor information abouttheir own body, and thus hinder activation ofshared motor responses between self and otherduring interactions of emotion expression.

The shared neural representations accountsuggests that problems with one’s own motoror body schematic system may undermine capac-ities for understanding others. Consequently, it ispossible that developmental problems involvingsensory–motor processes may have an effect onthe capabilities that make up “primary intersub-jectivity,” or the ability to react contingently toothers’ emotional expressions (Trevarthen &Aitken, 2001), and therefore the child’s abilityto resonate emotionally with others. It thus seemsplausible that the defects in social and sensory–motor problems in ASD and DCD may, in part,reflect a disturbed motor representation matchingsystem at the neuronal level. This speculation notonly helps explain problems in primary inter-subjectivity, but also the other sensory–motorsymptoms of autism: oversensitivity to stimuli,repetitious and odd movements, and possibly,echolalia (Gallagher, 2004).

Self- and Other Awareness

Although emotion contagion provides the obser-ver with direct information of the other’s emo-

tional state, this process only accounts for whathas been termed “motor empathy,” or “empathicmimicry.” However, that the observation of anemotion elicits the activation of analogous motorrepresentation in healthy observers, begs thequestion why there is not complete overlap be-tween internally generated and externally engen-dered motor representations.

In a complete empathic experience, observersmust be able to separate themselves from othersand have some minimal mentalizing ability.This aspect is a landmark of mature empathic ex-perience (Eisenberg et al., 2006; Zahn-Waxler &Radke-Yarrow, 1990). Affective sharing must bemodulated and monitored by the sense of whosefeelings belong to whom (Decety & Jackson,2004). Thus, self-awareness generally and agencyin particular are crucial aspects in promoting aprosocial regard for the other rather than a desireto escape aversive arousal. Phenomenologicallyspeaking, self-awareness pertains to the embod-ied, and contextually embedded first-person pointof view in subjective experience. In a similar vein,research in the neurosciences and developmentalscience use the term agency to describe the abilityto recognize oneself as the agent of an action,thought, or desire, which is crucial for attributinga behavior to its proper agent.

Developmental work demonstrates that infantscome into the world with an ecological sense ofself, that is, the self as perceived in relation tothe physical environment (Neisser, 1991). Theecologic sense of self is analogous to what phe-nomenologists term, prereflective self-awareness,or the subjective, qualitative “feel” of entertainingexperiences (Gallagher, 2000). An implicit, eco-logic sense of self develops from birth, prior toan explicit (conceptual) manifestation of self-knowledge by the second year, and this sense ofself is discriminated from the sense of others (Ro-chat & Striano, 2000). By 2 months, infants be-come incrementally systematic and deliberate inthe exploration of their own body and the percep-tual consequences of self-produced action. Forex-ample, infants delineate between perceptualevents that are self-generated or not self-gener-ated. In one study, Rochat and Hespos (1997a)tested whether newborn infants within 24 hr ofbirth discriminate between double touchstimulation specifying themselves and external(one way) tactile stimulation indicating nonself


objects via the robust rooting response manifestby healthy infants from birth. Recording thefrequency of the rooting in response to externalor self tactile stimulation indicated that newbornsare inclined to manifest rooting responses almostthree times more often in response to externalcompared to self-stimulation. The finding sug-gests that from birth, infants discriminate be-tween intermodal invariants that specify self-compared to external stimulation. Thus, infantsdevelop an understanding of their own body asa differentiated entity, situate, and agent in theenvironment.

The study by Martin and Clark (1982) is alsoof special interest; they tested 1-day-old babiesreactions to audiotapes of neonatal crying, thecrying of an 11-month-old, and the newborn’sown crying. They not only replicated Simmer’sresults that infants cry in response to other in-fant cries but also showed the more interestingtrait that newborns did not respond to the soundof their own cries. Another investigation, con-ducted by Dondi, Simion, and Caltran (1999),also demonstrated that newborns are able todiscriminate their own and other infants’ cries.These results suggest that there is some self-other distinction already functioning from birth.

By 3 months of age infants become aware oftheir own body as a dynamic and organized entitywith specific featural characteristics. In anotherseries of studies, infants faced two on-line videoimages presented on a split screen. Infants vieweda split videotape screen showing contingentmovements of the body from the waist down(Morgan & Rochat, 1997). One view showed in-fant’s theirown legs as they would be specified viadirect visual proprioceptive feedback, whereas theother showed experimentally modified on-lineview of their own legs. From 3 months of age, in-fants look significantly longer at the unfamiliarview of the legs that violates visual proprioceptivefeedback. Thus, by this age infants experience anintermodal calibration of the body, developing anintermodal body schema that serves as a percep-tual based “protorepresentation” of the body.

Although the above data highlights that infantrepresentations of self and other actions are dis-tinct, research also suggests that infants formshared representations of their own and others’ ac-tions. Neonates imitate the actions of others in aflexible and goal-directed way, suggesting that in-

fants represent the other as “like me” (e.g., similarto the self in some respect; Meltzoff & Brooks,2001). Further evidence suggests that infantsmay productively use information from theirown action capacities to understand the actionsof others (Woodward, Sommerville, & Guajardo,2001). Affective sharing among infants (reviewedabove) also highlights the automatic overlap be-tween other and self in infancy, which providesthe basis for the development of intersubjectivityand social cognition.

A sense of agency can also be traced to in-fancy. From birth, infants learn to be effectivein relation to objects and events. Within hoursfollowing birth, neonates can learn to suck in cer-tain ways and apply specific pressures on adummy pacifier to hear their mother’s voice orsee their mother’s face (Decasper & Fifer,1980; Walton, Bower, & Bower, 1992). The find-ing suggests that infants manifest a sense ofthemselves as agentive in the environment. Fur-thermore, by 2 months of age, infants alsoshow positive affect, such as smiling and plea-sure expression, when they accomplish causingan auditory and visual event (by activating a mu-sic box by pulling a cord attached to a limb).When the cord is then furtively disconnectedfrom the box, hindering infants’ effectiveness,they switch expressions from pleasure to anger(Rochat & Striano, 2000).

In sum, the studies reviewed indicate that inaddition to the early roots of perception–actioncoupling leading to emotional expression, asense of self, agency, and other distinctionemerge early in infancy. An ecologic sense ofself develops immediately via proprioceptivecalibration of sensory–motor experiences. Boththis resonance mechanism and an ecologicalsense of self situate the individual in the socialenvironment and account for the duality of hu-man beings who are strongly motivated to beconnected to others as well as to retain indepen-dence and autonomy. In the following section,we will highlight that primacy of the self-experi-ence permeates throughout development, andcan be seen in findings from cognitive neu-roscience studies showing immediate activationof self-produced actions prior to other-producedactions. In addition, we provide neurophysiolog-ical evidence for a cerebral mechanism specifi-cally devoted to self–other distinction.


Cognitive neuroscience of self–otherawareness and agency

One role that cognitive neuroscience can contrib-ute to the study of the self and other is to ground inphysiological mechanisms the distinct dimen-sions, aspects, and characteristics of the self andother to help address the potential separability orrelatedness of each component part of self-pro-cessing. It has been proposed that nonoverlappingparts of the neural circuit mediating shared repre-sentations (i.e., the areas that are activated for self-processing and not for other processing) generatesa specific signal for each form of representation(Jeannerod, 1999). This set of signals involvedin the comparison between self-generated actionsand actions observed from others ultimately allowthe attribution of agency (comparison between ef-ferent motor signals and afferent sensory signals).It has also been suggested that the dynamics ofneural activation with the shared cortical networkis an important aspect to distinguish one’s own ac-tions from the actions of others, and that the la-tency difference between the changes in activityelicited by the perception of self versus others’ ac-tions reflects the calibration process of sharedrepresentations (Decety & Jackson, 2004; Jackson& Decety, 2004). Furthermore, the fact that theonset of the hemodynamic signal is earlier forthe self than for the others (Jackson, Brunet,Meltzoff, & Decety, 2006; Grezes, Frith, & Pas-singham, 2004) may be considered as a neural sig-nature of the privileged and readilyaccessible self-perspective.

Accumulating evidence from neuroimagingstudies in both healthy people and psychiatricpopulations, as well as lesion studies in neurolog-ical patients, indicates that the right inferior parie-tal cortex, at the temporoparietal junction (TPJ)with the posterior temporal cortex, plays a criticalrole in the distinction between self-produced ac-tions and actions generated by others (Blakemore& Frith, 2003; Jackson & Decety, 2004). In addi-tion, some recent data suggest that this region isspecifically involved in theory of mind (Apperly,Samson, Chiavarino, & Humphreys, 2004; Saxe& Wexler, 2005). The TPJ is a heteromodal asso-ciation cortex, which integrates input from the lat-eral and posterior thalamus, as well as visual,auditory, somesthetic, and limbic areas. It has re-ciprocal connections to the PFC and to the tem-

poral lobes. Because of these anatomical charac-teristics, this region is a key neural locus for self-processing that is involved in multisensory body-related information processing, as well as in theprocessing of phenomenological and cognitiveaspects of the self (Blanke & Arzy, 2005). Its le-sion can produce a variety of disorders associatedwith body knowledge and self-awareness such asanosognosia, asomatognosia, or somatoparaphre-nia (Berluchi & Aglioti, 1997). For instance,Blanke, Ortigue, Landis, and Seeck (2002) dem-onstrated that out-of-body experiences (i.e., theexperience of dissociation of self from body)can be induced by electrical stimulation of theright TPJ. Of interest, one study found aberrantwhite matter adjacent to the TPJ, as well as inthe ventromedial prefrontal cortices and anteriorcingulate gyri (Barnea-Goraly et al., 2003) inchildren with ASD. Thus, deficits in self-otherprocessing in individuals with HFA may be dueto, in part, structural differences in pertinent brainareas or in abnormal connectivity between theseareas.

In addition, a number of functional imagingstudies point out the involvement of the rightTPJ in the process of agency (i.e., the awarenessof oneself as an agent who is the initiator of ac-tions, desires, thoughts, and feelings). In onefMRI study, participants were instructed to openand close their hand slowly and continuously(0.5 Hz), whereas this movement was filmedand projected to them online onto a screen (Leubeet al., 2003). The authors reported a positive cor-relation between the extent of temporal delay be-tween hand movement and its visual feedbackand the hemodynamic increase in the right TPJ.In another fMRI study, Farrer and Frith (2002) in-structed participants to use a joystick to drive a cir-cle along a T-shaped path. They were told that thecircle would be driven either by themselves or bythe experimenter. In the former case, subjectswere requested to drive the circle, to be awarethat they drove the circle, and thus to mentallyattribute the action seen on the screen to them-selves. In the latter case, they were also requestedto perform the task, but they were aware that theexperimenter drove action seen on the screen.The results showed that being aware of causingan action was associated with activation in the an-terior insula, whereas being aware of not causingthe action and attributing it to another person was


associated with activation in the right TPJ. It is in-teresting that individuals experiencing incorrectagency judgments, as it can be the case in schizo-phrenia, feel that some outside force is creatingtheir own actions. One neuroimaging study foundhyperactivity in the right TPJ when patients withschizophrenia experienced alien control during amovement selection task compared with healthycontrols (Spence et al., 1997). Such delusions ofcontrol may arise due to a disconnection betweenfrontal brain regions, where actions are initiated,and parietal regions where the current and pre-dicted states of limbs are represented.

Another study used a device that allowed mod-ifying the participant’s degree of control of themovements of avirtual hand presented on a screen(Farrer, Franck, Georgieff, Frith, Decety, & Jean-nerod, 2003). Experimental conditions varied tothe degree of distortion of the visual feedback pro-vided to the participants about their own move-ments. Results demonstrated a graded hemody-namic activity of the right TPJ that parallels thedegree of mismatch between the executed move-ments and the visual reafference. Strikingly, sucha pattern of neural response was not detected inschizophrenic patients who were scanned underthe same procedure (Farrer et al., 2004). Instead,an aberrant relationship between the subject’s de-gree of control of the movements and the hemo-dymamic activity was found in the right TPJand no modulation in the insular cortex. Addi-tional evidence for the contribution of the rightTPJ in self-awareness and the sense of agency de-rives from studies on imitation that document theselective involvement of this region during recip-rocal imitation, in which it may be difficult tokeep track of agency, that is, who is imitatingwhom (Chaminade & Decety, 2002; Decety,Chaminade, Grezes, & Meltzoff, 2002). Resultsfrom these studies provide strong support for theimplication of the right TPJ in the process ofself-agency by demonstrating a clear dissociationbetween the left and the right TPJ. When partici-pants imitated the other, the left TPJ was stronglyengaged, whereas greater activation was detectedin the right TPJ when they were being imitated.Only this later condition involved discrepanciesbetween predicted outcomes of the action per-formed by the participants and those perceived.

The right TPJ is also selectivelyactivated whenparticipants are asked to mentally simulate actions

from someone else’s perspective but not fromtheir own (Ruby & Decety, 2001). Similarly,this region was specifically involved when partic-ipants imagined how another person would feel ineveryday life situations that elicit social emotions(Ruby & Decety, 2004) or painful experiences(Jackson et al., 2006; Lamm, Batson, & Decety,2007) but not when they imagined these situationsfor themselves. Such findings point to the similar-ity of the neural mechanisms that account for thecorrect attribution of actions, emotions, pain,and thoughts to their respective agents when onementally simulates actions for oneself or for an-other individual. Further, they support a crucialrole for the right TPJ, not only in mental state pro-cessing, but also in lower level processing, includ-ing reorienting attention to salient stimuli (Decety& Lamm, 2007).

Other areas implicated in self-processing, suchas the medial PFC, posterior cingulate cortex, andprecuneus, have been shown to be active whenindividuals are at rest and deactivate during cogni-tively demanding tasks (Raichle et al., 2001). Ithas been hypothesized that this “resting state” net-work contribtes to self-reflective thought, socialperceptions, and theory of mind (Gusnard, Akbu-dak, Shulman, & Raichle, 2001). It is of interestthat in line with the social deficits observed inASD, individuals with ASD demonstrate atypicalresting state activation in these networks (Ken-nedy, Redcay, & Courchesne, 2006). However,further research is needed to understand the natureof the relationship between self-experience, theresting state networks, and social behavior in typi-cally developing children, and those with ASD.

Self, other, agency, and intersubjectiveexchange in ASD

A mature sense of self-, agency, and otherawareness are crucial for full-blown empathy,as they allow the observer to move beyondshared representations and accurately gaugethe other’s emotional state in relation to oneself,in other words engage in intersubjective ex-changes. According to clinical descriptions, au-tistic children show problems in thinking, relat-ing, and communicating to the world as well asmoving through alternative perspectives thatothers entertain (Hobson & Meyer, 2006), allof which we suggest draw from more than basic


level motor resonance, as they include an agen-tive stance over one’s actions and an ability tointerpret others as agentive actors as well.

Empirical evidence supports the suggestionthat children with ASD fail to effectively discrim-inate the actions of the self and other. A recentstudy examined self–other orientation (identifica-tion) among 16 olderchildren with autism, and 16comparison, developmentally delayed childrenmatched for age and IQ (Meyer & Hobson,2004). Participants performed four object-ori-ented tasks such as rolling a wheel and stackingobjects. Lines on the floor segregated the child’sand experimenter’s “personal space,” and taskswere either directed toward the child’s “personalspace” or toward the adult’s “personal space.”After the model, children were encouraged to imi-tate actions with a toy. In comparison to controlparticipants, children with autism performed sig-nificantly fewer responses that modeled the self–other orientation to the object. Instead, a signifi-cant portion of the children with ASD showed“geometric repetition.” That is, they accuratelyimitated the experimenter’s actions (i.e., rollingthe wheel); however, they did so without eithera “self”-orientation or an “other” norientation.For example, children with ASD would roll awheel horizontally in the center of the testingspace, disregarding the experimenters’ wheelrolling either toward themselves or the child.These findings suggest that it is not motor mim-icry that is problematic in autism per se, but in-stead, specific impairments in intersubjective imi-tation. Children in the control group did not showthis pattern of responding, which was interesting.Instead, they fell into one of two categories of re-sponding: either consistently adopting appropri-ate self- or other orientation, or showing a mix astrategies, including not imitating at all. The au-thors speculated that the findings reflect the fail-ure of identification in autism, highlighting corre-spondence between performance on this task andthe capacity to comprehend others’ perspectivesand to mentally shift from one perspective to an-other. The finding is in line with other data sug-gesting an autism-specific difficulty in accuratelyimitating the orientation of an action in relation tothe model’s body (e.g., Ohta, 1987; Smith & Bry-son, 1998). However, future research shouldreplicate these findings with an additional con-trol group of typically developing children, as

it is unclear whether observed differences reflectunique responding in children with ASD orunique responding in children with develop-mental, cognitive delay.

Further evidence of weak self–other differen-tiation among children with ASD derives from astudy utilizing a visual perspective taking task(Lee, Hobson, & Chiat, 1994). During such atask autistic children were significantly less proneto use the pronoun “me” to answer whether theywere the subject in a photograph. Moreover, autis-tic subjects were less likely than controls to em-ploy the pronoun “you” to refer to the experi-menter. The experimenters suggest that theseresults do not reflect vocabulary or semantic prob-lems, as the children with ASD showed high ver-bal ability, which was measured by the BritishPicture Vocabulary Scale. Instead, it was sug-gested that failures to use pronouns reflect deficitsin perspective taking. Person pronoun use isamong the few trademarks signifying self-con-sciousness, others including self-recognition inmirrors and demonstration of self-conscious emo-tions such as shame (Zelazo, 2004). By age 2,executive function allows individuals to controlaspects of conscious awareness, including con-scious control of emotion, thought, and action.Thus, executive functions may allow individualsto regulate their egocentric bias, and engage in ac-curate perspective taking. In the case of ASD,problems seem to reflect not a bias in one’s ownperspective per se, but a weakness in adopting aconscious perspective albeit personal or otheroriented. Thus, it is likely that empathy deficitsin autism reflect problems at each or several ofthe components integral to empathy. In the fol-lowing section, we discuss the crucial role of ex-ecutive function in mature empathy.

Mental Flexibility and Self-Regulation

Given the sharedness of the representations ofone’s own emotional states and others, as wellas similarities in brain circuits involved duringfirst- and third-person perspective taking, itwould seem difficult not to experience emotionaldistress while viewing another’s distressed stateand personal distress does not contribute to theempathic concern and prosocial behavior (Bat-son et al., 2003; Decety & Lamm, 2008). Indeed,distress in the self can hinder one’s inclination to


soothe the other’s distress. However, it would notbe adaptive if this automatic sharing mechanismbetween self and other was not modulated bycognitive control and metacognition. It is neces-sary that executive functions work in a top-downfashion to regulate our proclivity to be biased inour self-perspective while gauging another per-sons’ emotional state, and promoting a sympa-thetic regard for the other rather than a desire toescape aversive arousal (Decety, 2005). Ventraland dorsal regions of the PFC have been associ-ated with response inhibition and self-control,which are key components of emotion regulation(i.e., adjustments in type, magnitude, and dura-tion of emotional responses that are made tomeet personal, situational and interpersonal de-mands; Ochsner & Gross, 2005). Support forthis hypothesis in the domain of pain empathycomes from a recent fMRI study in which physi-cians who practice acupuncture were comparedto naıve participants while observing animatedvisual stimuli depicting needles being insertedinto different body parts including the mouth re-gion, hands, and feet. Results indicate that the an-terior insula, periaqueducal gray, and anteriorcingulate cortex (ACC; i.e., neural regions thatbelong to the pain matrix) were significantly ac-tivated in the control group, but not in the physi-cian group, who instead showed activation of thedorsal and ventral medial regions of the PFC, aswell as the right TPJ, involved in emotion regu-lation and metacognition (Cheng et al., 2007).

It is of interest that the development of selfand other mental state understanding is func-tionally linked to that of executive functions,that is, the processes that serve to monitor andcontrol thought and actions, including self-regulation, planning, cognitive flexibility, re-sponse inhibition, and resistance to interference(Russell, 1996). There is increasingly clear evi-dence of a specific developmental link betweenthe development of mentalizing (i.e., the pro-cess of making sense of mental states in oneselfand other persons) and improved self-control ataround the age of four (e.g., Carlson & Moses,2001). Improvement in inhibitory control corre-sponds with increasing metacognitive abilities(Zelazo, Craik, & Booth, 2004), as well aswith maturation of brain regions that underlieworking memory and inhibitory control(Tamm, Menon, & Reiss, 2002). A series of

studies by Posner and Rothbart (2000) stronglysuggest that executive regulation undergoesdramatic change during the third year of life.

The PFC develops slowly compared to otherregions during ontogeny, and reaches its matura-tion only late in adolescence (Bunge, Dudukovic,Thomason, Validya, & Gabrieli, 2002). Evidencefor this delayed maturation is provided by mea-sures of myelination, gray matter reduction, syn-aptogenesis, and resting metabolism (Huttenlo-cher & Dabholkar, 1997). Imaging studiesindicate that prefrontal areas do not attain full ma-turations prior to adolescence (Paus et al., 1999;Sowell, Thompson, Holmes, Jernigan, & Toga,1999). Childhood cognitive development relatesto maturation of the middorsolateral frontal cortexas well as the ACC, which are critical for the de-velopment of executive functions, especially thedramatic increase in children’ ability to suppressexternal influences (Paus et al., 1999). Specifi-cally, changes in cerebral blood flow, which re-flects synaptic activity, in the PFC, almost doublesfrom age 0 to 2 years (Chiron et al., 1992). Further,the frontal association cortex is the last area to in-crease blood flow from infancy to childhood, andreaches adult values only by adolescence (Taka-hashi, Shirane, Sato, & Yoshimoto, 1999). Directsupport for age-related changes in brain activityassociated with metacognition is provided by aneuroimaging investigation of theory of mind inparticipants whose age ranged between 9 and 16years (Moriguchi, Ohnishi, Mori, Matsuda, &Komaki, 2007). Both children and adolescentsdemonstrated significant activation in the neuralcircuits associated with mentalizing tasks,including the TPJ, the temporal poles, and themedial PFC. Furthermore, the authors found apositive correlation between age and the degreeof activation in the dorsal part of the medialPFC. Impairment of the medial/cingulate PFC iscommonly associated with deficits in social inter-action and self-conscious emotions (Sturm, Ro-sen, Allison, Miller, & Levenson, 2006). Such pa-tients may become apathetic, disinterested in theenvironment, and unable to concentrate their at-tention on behavioral and cognitive tasks. It hasalso been suggested that frontal damage hindersperspective taking ability (Price, Daffner, Stowe,& Mesulam, 1990). The current understandingof the role of the PFC in executive functioningfits well with developmental research, which


indicates that empathic concern is strongly relatedto effortful control and self-regulation, with chil-dren high in effortful control expressing greatersympathy and less personal distress (Rothbart,Ahadi, & Hershey, 1994). Effortful control maysupport empathy and prosocial behavior by allow-ing the child to attend to the thoughts and feelingsof another without becoming overwhelmed bytheir own distress (Posner & Rothbart, 2000).

Adopting another’s perspective is integral tohuman empathy and is linked to the developmentof moral reasoning (Kohlberg, 1976), altruism(Batson, 1991) and a decreased likelihood of in-terpersonal aggression (Eisenberg et al., 2006).Of special interest are findings from social psy-chology that document the distinction betweenimagine the other and imagine oneself (Batson,Sager, et al., 1997). These studies show that theformer may evoke empathic concern (definedas an other-oriented response congruent withthe perceived distress of the person in need),whereas the latter induces both empathic concernand personal distress. This observation may helpexplain why empathy, or sharing someone else’semotion, need not yield prosocial behavior. Ifperceiving another person in an emotionally orphysically painful circumstance elicits personaldistress, then the observer may tend not to fullyattend to the other’s experience and as a resultlack sympathetic behaviors.

The effect of perspective taking to generateempathic concern was documented in a study con-ducted by Stotland (1969). In his experiment, par-ticipants viewed an individual whose hand wasstrapped in a machine that participants were toldgenerated painful heat. One group of subjectswere instructed to watch the target person care-fully, another group of participants were instructedto imagine the way the target felt, and the thirdgroup was instructed to image themselves in thetarget’s situation. Physiological (palm sweatingand vasoconstriction) and verbal assessments ofempathy demonstrated that the deliberate acts ofimagination yielded a greater response than pas-sive viewing. Empathy specifically seems to besensitive to perspective taking, as demonstratedbya series of studies demonstrate the effectivenessof perspective-taking instructions in inducing em-pathy (Batson, Sager, et al., 1997) and that empa-thy-inducing conditions do not compromise thedistinction between the self and other (Batson,

Sager, et al., 1997, but see Cialdini, Brown,Lewis, Luce, & Neuberg, 1997, for a differentaccount of empathy and self-other merging).

A recent study by Lamm et al. (2007) investi-gated the distinction between empathic concernand personal distress combining a number ofbehavioral measures and event-related fMRI.Participants were asked to watch a series of video-clips featuring patients (their face only) undergo-ing painful medical treatment either with the in-struction to put themselves explicitly in theshoes of the patient (“imagine self”), or, inanother condition, to focus their attention on thefeelings and reactions of the patient (“imagineother”). Behavioral measures confirmed previoussocial psychology findings that projecting oneselfinto an aversive situation leads to higher personaldistress and lower empathic concern while focus-ing on the emotional and behavioral reactions ofanother’s plight is accompanied by higher em-pathic concern and lower personal distress (e.g.,Batson et al., 2003). Neuroimaging data were con-sistent with such findings. Both the self and other’perspectives were associated with hemodynamicsignal increase in the neural regions that belongto the pain matrix including the insula and ACC.However, the self-perspective evoked strongerhemodynamic responses in brain regions in-volved in coding the motivational– affective di-mensions of pain, including bilateral insularcortices and aMCC. In addition, the self-per-spective led to stronger activation in the amyg-dala, a limbic structure that plays a critical rolein fear-related behaviors, such as the evaluationof actual or potential threats. It is of interest thatthe amygdala receives nociceptive informationfrom the spinoparabrachial pain system andthe insula, and its activity appears closely tiedto the context and level of aversiveness of theperceived stimuli (Zald, 2003). Imagining one-self to be in a painful and potentially dangeroussituation thus triggers a stronger fearful and/or aversive response than imagining someoneelse to be in the same situation. Alternativelyand less specifically, the stronger involvementof the amygdala might also reflect a general in-crease of arousal evoked by imagining oneselfto be in a painful situation. Regarding the insularactivation, it is worth noting that it was locatedin the middorsal section of this area. This partof the insula plays a role in coding the


sensory–motor aspects of painful stimulation,and it has strong connections with the basalganglia, in which activity was also higherwhen adopting the self-perspective. Taken to-gether, activity in this aspect of the insula possi-bly reflects the simulation of the sensory aspectsof the painful experience. Such a simulationmight both lead to the mobilization of motorareas (including the SMA) to prepare defensiveor withdrawal behaviors, and to interoceptivemonitoring associated with autonomic changesevoked by this simulation process.

Various domains of research suggest thatmental flexibility to adopt another person’spoint of view is an effortful and controlledprocess. Moreover, the capacity to take the con-ceptual perspective of the other is thought to bea necessary component in the fully developed,mature theory of mind. Developmental researchindicates that perspective taking develops pro-gressively. In the affective domain, childrendemonstrate emerging awareness of the subjec-tivity of other people’s emotions around18 months. By this age, infants understandthat they should provide an experimenter witha piece of food that the experimenter reacts towith apparent happiness (e.g., broccoli) ratherthan one that the experimenter previously re-acted to with disgust (fish crackers), even if theinfant prefers the latter food (Repacholi & Gop-nik, 1997). In contrast, 14-month-olds fail todemonstrate this understanding. This is the firstempirical evidence that infants of this age haveat least a limited ability to reason nonegocentri-cally about people’s desires (Flavell, 1999).

Executive functions not only facilitate per-spective taking, but also control attention andmetacognitive capacities, both of which facili-tate prosocial responding in reaction to another’sdistress. Attention to others and the environmentoccurs when individuals are able to attend to ex-ternal stimuli and disregard to some extent theirself-experience. Metacognitive capacities allowfor recursive thinking about the self’s actions,and are thus linked to emotions such as shameor guilt which emerge as a result of causing an-other’s distress. Children first demonstrate re-sponses to the distress of others with other-focused behaviors like concern, attention to thedistress of the other, cognitive exploration ofthe event, and prosocial interventions around

the second year of life. At this age children man-ifest a self-concept and self-conscious emotions,and children’s reparative behaviors after theycause distress in the other emerge (Zahn-Waxler& Radke-Yarrow, 1990). A longitudinal study ofyoung children’s development of concern forothers’ distress showed that prosocial behaviors,such as hugs and pats, emerge around the begin-ning of the second year of life, increasing in in-tensity throughout this year and sometimes pro-vide self-comfort. However, by the end of thesecond year, prosocial behaviors appear to bemore appropriate to the victims needs, are notnecessarily self-serving, and children’s emotionsappear to be better regulated (Radke-Yarrow &Zahn-Waxler, 1984).

The ability to regulate emotions may be sub-ject to individual differences, and may interactwith the degree to which individuals experienceemotions. Eisenberg and her colleagues (1994)proposed a model suggesting an interaction be-tween the intensity at which emotions are experi-enced and the extent to which individuals can reg-ulate their emotions. In line with her model,multimethod regression analysis of empathy-re-lated responses combining self-report measuresand facial muscle activity in response to empa-thy-inducing videos (of impoverished chil-dren), suggest that increased emotional in-tensity and decreased regulation on standardself-report measures predict personal distressin response to viewing the video vignettes.These interactions are first seen in infancy, asfindings from infant development demonstratethat 4-month-olds low in self-regulation areprone to personal distress at 12 months of age(Ungerer et al., 1990). In childhood, individualswith increased levels of emotional intensity(based on self-report, teacher–parent report,and autonomic measurements) and weak regu-lation are prone to personal distress in responseto another’s predicament, as they become over-whelmed due to their vicariously inducednegative emotions (Miller & Eisenberg, 1988).

Mental flexibility deficits in developmentaldisorders of empathy

Children with empathy deficits likewise show def-icits in executive function and children with ASDspecifically show deficits in mental flexibility


(Bennetto, Pennington, & Rogers, 1996; Min-shew, Meyer, & Goldstein, 2002; Ozonoff &McEvoy, 1994; Ozonoff, Pennington, & Rogers,1991). A series of studies found that when an ex-perimenter feigns distress in a room where chil-dren were playing, children with ASD looked tothe experimenter much less than healthy and men-tally retarded children (Corona, Dissanayake, Ar-belle, Wellington, & Sigman, 1998; Dissanayake& Sigma, & Kasari, 1996; Sigman, Kasari, Kwon,& Yirmiya, 1992). However, when Blair (1999)replicated such studies, but controlled forexecutivefunction demands of attention, children with ASDperformed similar to healthy children. That is,when experimenters’ feigned distress was unam-biguous and took place under conditions of lowdistractibility, children with ASD showed auto-nomic responses similar to controls. In studiesmeasuring facial mimicry, when given ampletime, individuals with ASD do show affectivecompensatory tactics to accomplish emotion read-ing; and in emotion recognition tasks, they showactivation in brain areas related to intentional atten-tional provision and categorization (Hall, Szecht-man, & Nahmias, 2003). These data indicate thatalongside bottom-up information processing defi-cits (e.g., affective mimicry), top-down executivecontrol is also impaired in individuals with ASD.

Empathy deficits in Asperger syndrome alsoseem to reflect poor executive function. A casestudy of two adolescents with Asperger syndromewith severe inabilities for emotional and cognitiveaspects of empathysuggests that theseweaknessesdo not reflect significantly worse emotion recog-nition or cognitive perspective taking per se, butinstead, reveal poor integration of the cognitiveand affective components of empathy (Shamay-Tsoory, Tomer, Yaniv, & Aharon-Peretz, 2002).

Indeed, these executive function deficits inASD have been documented by fMRI experi-ments using cognitive tasks. Aberrant activityin prefrontal, frontal, as well as atypical fronto-parietal interactions, have all been documentedin fMRI experiments probing executive func-tion in ASD (Kana, Keller, Minshew, & Just,2007; Silk et al., 2006). It is likely that deficitsin mental flexibility are grounded in atypicalstructure and function in prefrontal, frontal,and parietal lobes and contribute to perspec-tive-taking difficulties observed in individualswith ASD.

It is noteworthy that violent offenders, andchildren with aggressive behavior problems, ex-perience deficits in empathy and empathic con-cern, although the result of the lack of empathymanifests in behavior differently than that seenin ASD or DCD. The former responds aggres-sively to others’ distress (Arsenio & Lemerise,2001), whereas the later simply lack prosocial be-havior. The distinction can be understood as thedifference between apathy and hostility, both ofwhich are categorized as unempathetic in the tra-ditional sense, although one is “passive,” and theother is “active.” Individuals with ASD seem tolack either an interest or capacity to resonate emo-tionally with others, or engage in intersubjectivetransactions (Gallagher, 2001). In contrast, chil-dren with developmental aggression disordersreact aggressively to the observation of others’distress.

CD is a mental disorder of childhood and ado-lescence that is characterized by a longstandingpattern of violations of rules and laws. Symptomsof CD include aggression, frequent lying, runningaway from home overnight, and destruction ofproperty. CD is important partly because it is themajor childhood precursor to antisocial personal-ity disorder in adulthood (Lahey, Loeber, Burke,& Applegate, 2005). Children with aggressive be-havior problems show deficits in regulating emo-tions, which may result in harmful patterns of in-terpersonal behavior. Lewis, Granic, and Lamm(2006) reviewed several of their recent studies in-vestigating individual and developmental differ-ences in cortical mechanisms of emotion regula-tion, corresponding with different patterns ofinterpersonal behavior. Their methods includeevent-related potentials and cortical source mod-eling, using dense-array EEG, as well as video-taped observations of parent–child interactions,with both normal and aggressive children. By re-lating patterns of brain activation to observed be-havioral differences, the authors found (a) a steadydecrease in cortical activation subserving self-reg-ulation across childhood and adolescence, (b) dif-ferent cortical activation patterns as well as behav-ioral constellations distinguishing subtypes ofaggressive children, and (c) robust correlations be-tween the activation of cortical mediators of emo-tion regulation and flexibility in parent–childemotional communication in children referredfor aggressive behavior problems.


Emotion is normally regulated in the humanbrain by a complex circuit that includes several re-gions of the PFC (dorsal and ventral), the amyg-dala, hypothalamus, ACC, insula, and ventralstriatum. Descending pathways from orbitofron-tal and medial prefrontal cortices, which arealso linked with the amygdala, provide the meansfor speedy influence of the PFC on the autonomicsystem, in processes underlying appreciation andexpression of emotions (Barbas, Saha, Rempel-Clover, & Ghashghael, 2003). It is of interestthat key areas found to be functionally or struc-turally impaired in antisocial populations includedorsal and ventral regions of the PFC, amygdala,hippocampus, TPJ, and ACC (Raine & Yang,2006). Raine has hypothesized that the rule-breaking behavior common to antisocial, violent,and psychopathic individuals may in part be at-tributable to impairments in some of the struc-tures (dorsal and ventral PFC, amygdala, andTPJ) or dysfunction in amygdala–orbitofrontalcortex (OFC) structural connectivity, normallysubserving moral cognition and emotion.

In contrast, impulsive aggression may be theproduct of failed emotion regulation. Impulsiveaggression is associated with a low thresholdfor activating negative affect and with failure torespond appropriately to the anticipated negativeconsequences of behaving aggressively. David-son, Jackson, and Kalin (2000) have proposedthat the mechanism underlying suppression ofnegative emotion is via an inhibitory connectionfrom regions of the PFC to the amygdala.

In addition to functional brain abnormalitiescorresponding with emotion dysregulation andempathy deficits in CD, impulsive aggressionin CD is associated with decreased noradrener-gic (NA) function, which also correlates withpoor empathic ability in this population (Raine,1996). In fact, a low resting heart rate, a partlyheritable trait reflecting fearlessness andstimulation seeking, at 3 years of age predictedaggressive behavior at 11 years of age (Raine,Venables, Mednick, & Sarnoff, 1997). Childrenwith clinical levels of behavior problems, oftena precursor to the development of CD, show in-creased disregard for others, for example, anger,avoidance, and/or amusement by another’s dis-tress, a negatively toned response pattern thatdiffers significantly from normal children’s re-sponses. It is likely that decreased NA function,

which is associated with aggressive behavior,contributes to these antisocial reactions.

One way to determine whether CD is associ-ated with low arousal or poor regulation is toinvestigate patterns and changes in autonomicnervous system. Sympathetic activation or para-sympathetic inhibition leads to changes in cardiacfunctioning, which can be interpreted as bodilycues of discomfort or distress and a need for ac-tion. Porges (1996) has found that parasympa-thetic nervous system functioning, as reflected inheart rate variability (heart rate [HR] variabilitymeasures the variability in HR associated withbreathing and indexes an individual’s competencyto physiologicallyand behaviorally reacts to exter-nal stimuli) influenced by the vagal system, is re-lated to the control of attention, emotion and be-havior. Porges suggests that the tonus of thevagus nerve provides a theoretical basis for thechild’s ability to focus attentional processes, in-hibit irrelevant activity, regulate emotion, and ap-propriately engage with the environment (Porges,1995).

In the domain of empathy, the work of Eisen-berg and Fabes (1994) suggests that decelerationof HR may be associated with attention to othersthat characterizes empathic concern, and HR de-celeration is also associated with an increase in de-sire to help and comforting. A number of studiesindicate that antisocial behavior, and CD are asso-ciated with, and predictable from, low resting HRin children, adolescents, and adults (e.g., Lahey,Hart, Pliszka, Applegate, & McBurrett, 1993;Raine, Venables, & Sarnoff, 1997). Becauselow resting HR is associated with greater aggres-sion, and aggression and concern for others are in-versely related, it has been predicted that high HRshould predict greater concern for others. Onestudy found that HR was positively correlatedwith concerned responses toward adults whowere simulating injuries (Zahn-Waxler, Cole,Welsh, & Fox, 1995). However, Calkins and Ded-mond (2000) reported that aggressive childrendisplayed no physiological indicators of under-arousal, as indexed by resting HR. The authorsdid find, however, that these children displayedpoor behavioral and physiological regulation, asindexed by a lack of HRV during challenging sit-uations. This latter finding supports the idea of afailure of self-regulation in relation to empathyand aggression. Cardiac vagal regulation was


found to differentiate among children at risk forbehavior problems (Calkins, Graziano & Keane,2007). In that study (a sample of 335 children),there was a trend for the children at risk for exter-nalizing problemsto display less vagal withdrawalthan the control group. Future research should ul-timately clarify the relationship between struc-tural/functional differences in patterns of brain ac-tivation with NA function in individuals with CD.

The maturation of executive functions, includ-ing emotion regulation (subserved by the dorsaland ventral PFC and their connections with theamygdala) by 2 years of age contributes to the de-velopment of prosocial behaviors. Conversely, ifexecutive functioning is not intact, self and otherperspectives may not be regulated and individualsmay over- or underidentify with an observed tar-get. In the case of childhood aggression and CD,it is likely that poorexecutive control and dysfunc-tion of emotion regulation contributes to empathydeficits, although other factors (NA function) alsocontribute to reactionary behaviors.

Conclusions

We have argued that empathy depends upon bothbottom-up processes, which are driven by emo-tion expressions, and top-down processes, includ-ing self-regulation and executive control. Thesedifferent aspects are underpinned by distinctneural systems that develop at different stages.Notably, emotion sharing relies on the percep-tion–action coupling mechanism, which seemsfunctional very early in development, and allowsthe newborn to implicitly share subjective bodilyexperiences with others. Controlled processes,subserved by the PFC, develop later and play amajor role in metacognition, including takinginto account a cognitive representation of one’sown mind and other’s mind, aspects that arenecessary for social emotions which requireself-monitoring (see Figure 1). We have alsoshown that developmental disorders related toempathy reflect dysfunction of these different as-pects. It is noteworthy that the current knowl-edge in social cognitive neuroscience is at a pre-liminary stage, and many findings need to bereproduced. In relation to the goal of this paper,ties drawn between developmental and neuro-scientific evidence in emotion sharing and em-pathy can only be loosely strung together, as

many neuroscience findings pertain to adult par-ticipants, not children. Future studies should aimto incorporate children in the investigation of theneural basis of empathy, especially because con-tradictions surround the few neuroscience stud-ies that examine emotion sharing in children.

Finally, the model reviewed here offers inter-esting insights for debates surrounding the natur-alization of normative ethics. Empathy has beenassociated with the propensity to respond to an-other’s predicament in a prosocial, or “moral”way. Yet, an understanding of what motivatesus to feel empathy in the sense of caring for theother (Batson et al., 2003) and then help themis unclear. In fact, humans fail to consistently re-spond to others’ negative situations prosociallyacross contexts. Further research in child develop-ment and cognitive neuroscience may help eluci-date these interrelationships and hopefully offer abetter understanding of emotional resonance, em-pathy, and their relationship with prosocial, moralreasoning (and the lack thereof). The results of arecent fMRI study on empathy and theory ofmind with children seem to indicate that there islittle overlap in the brain circuits associated withempathy for pain and moral reasoning, althoughthis does not mean that these circuits do not com-municate (Decety et al., 2008). In this study, chil-dren watched situations involving either a personwhose pain was caused accidentally or a personwhose pain was intentionally inflicted by anotherindividual, as well as situations without any painwith one or two agents. It is important that whenchildren observed an individual intentionallyharming another, regions of the PFC that are con-sistently involved in representing social interac-tion and moral behavior such as the temporopa-rietal junction, the paracingulate cortex (PCC),and OFC were recruited (see Figure 2). It is of in-terest that children indicated in the postscan de-briefing that they thought that the situations inwhich pain was caused by another person wereunfair, and were asking about the reason thatcould explain this behavior. Evidence from moralneuroscience suggests a critical role of a cortico-limbic network subserving moral judgment. Thisnetwork includes the medial OFC, the TPJ, theamygdala, and anterior PCC (Moll, de Oliveria-Souze, & Eslinger, 2003). Furthermore, the mon-itoring of outcomes that relate to punishments andrewards is linked to activity in the OFC


(Kringelbach & Rolls, 2004). It is worth empha-sizing that the regions selectively associated withthe perception of an agent harming the other be-long to the neural systems underlying moralthinking.

We have argued that genuine empathy goesbeyond emotion sharing and a simple resonanceof affect between the self and other. It dependscrucially on self–other awareness and on the abil-ity to regulate one’s own emotional state, allow-ing proper identification of the other’s conditionand freeing up resources for coping with an-other’s distress in prosocial ways. Successfulemotion regulation in infancy is essential for thedevelopment of the ability to control one’s ownarousal and, with the sense of agency, be ableto tag the aroused state as indicative of the stateof the other. Children as well as adults who be-come overaroused by another’s distress, due tolack of emotion regulation and/or self–other dis-tinction, may use up too many cognitive re-sources dealing with their own emotion and failto act in a prosocial fashion (Nielsen, 2002).

Limitations of the scope

It is important to note several limitations of ourreview. The first limitation pertains to the extentto which conclusions can be drawn from the re-lationship between the development of empathyin healthy children and the manifestation of em-pathy deficits that occur in developmental disor-ders. We covered findings from infant develop-ment to address the innateness of the interactingcomponents of empathy; however, most of thefindings reviewed from developmental disorderspertain to observations from early childhood.This limitation in part reflects the difficulty to ob-tain infant data across developmental disorders asthey are often not diagnosed until childhood.Some analysis of infant behavior of children di-agnosed with developmental disorders comesfrom home video analysis (see Baranek, 1999),although such studies are sparse, and findingsare ambiguous due to weak scientific control.

Second, the relationship between neural evi-dence and behavioral data is indirect, and thusspeculations may be far reaching. Neuroimagingdata help to answer fundamental questions aboutthe mechanisms subserving imitation. However,their interpretation in relating structure to function

should be done with caution. It is difficult to derivethe computational function of an area without tak-ing into account its extrinsic and intrinsic connec-tivity, the distribution of receptor types, and the in-formation processing of the intrinsic neurons. Suchinformation is generally lacking. In addition, a setof cortical areas may be active in a wide range offunctions from action perception to empathy andtheory of mind, but across those functions the net-works in which they participate may be quite dif-ferent (see Cacioppo et al., 2003). More empiricaldata from both developmental science and cog-nitive neuroscience in the future will contributeto a fuller understanding of the mechanisms in-volved in empathy and their developmental timecourse. Furthermore, brain imaging investigationsof emotional processes often draw from limitedmethodologies that may overlook flaws in the op-erational definitions of the emotional phenomenastudied. For example, many fMRI experiments re-quire participants to identify the emotion in staticfaces or short animations, implicitly consideringthat emotion recognition can be equated with emo-tional experience. Clinical investigations with neu-rological patients, however, indicate that these pro-cesses (emotion recognition and experience)involve quite different neural substrates (Leven-son, 2007). Future neuroimaging studies of emo-tion in general, and empathy in particular, shouldbase stimuli on the discrete emotional experienceexamined. Meeting this goal would be facilitatedby the furthercollaboration betweencognitiveneu-roscientists and developmental psychologists.

Third, and finally, empathy is a complex con-struct and the above model does not account forall that empathy entails. The phenomenologicalexperience of empathy and its role in initiatingprosocial, empathic reactions likely draws onseveral interacting factors (and complicateddistributed brain networks) not mentioned inour review. For example, motivation likely in-fluences empathic accuracy: people who aremotivated to produce empathically accurate re-sponses to another’s predicament are less sus-ceptible to social inference biases such as thefundamental attribution error (Fletcher, Reeder, &Bull, 1990; Tetlock, 1985). In addition, the typeof rapport between observer and target influencesthe intensity of emotion contagion between mem-bers of a dyad, with patients and therapists, mothersand infants, and spouses, and even individuals who


perceive others as similar to themselves rankinghigh in autonomic synchrony (Levenson & Ruef,1997).

Another important area of interest regarding thecontribution of empathy to the development of in-tersubjectivity is its relation to the so-called attach-ment system described by Bowlby (1958), that is,an innate psychobiological system that motivatesinfants to seekproximity topeoplewhowill protectthem. One can argue that the mechanisms that un-derpin the development of empathy, especiallythrough interaction with caregivers who are re-sponsive, partly overlaps, and are functionallylinked with promoting optimal functioning of theattachment system. The consequences of this linkbetween empathy and attachment are paramount.Indeed, Mikulineer and Shaver (2005) have docu-mented the idea that people who have the benefitsof secure social attachments find it easier to per-ceive and respond to other people suffering, com-pared to those who have insecure attachments.

Personality traits, temperaments, and culturalnorms of emotional display also contribute to thedegree to which empathy may be experienced inthe observer (Eisenberg & Fabes, 1994; Posner& Rothbart, 2000). Likewise, children from cul-tures that promote reciprocal relations and coop-eration tend to be better at perspective-taking

tasks than children living in individualistic cul-tures (Eisenberg, Bridget, & Shepard, 1997).

Social psychologists emphasize the role ofsituational context as opposed to personality inthe experience of empathy (or the absence of it),although many recognize the combination of sit-uation and personality as the best predictor of so-cial behavior (Fiske, 2004). Although situationalcontext is important, creating ecologically validsituations in a laboratory setting or in an MRIscanner poses a challenge. Theoretically, assess-ing personality traits and correlating them withtask performance and biological markers shouldpose no great challenge. These constructs, how-ever, are rarely stable and they are dependent onmany variables. Thus, designing ecologicallyvalid experiments remains a challenging process,especially with children.

A current aim in cognitive neuroscience is tostudy the interaction between affect and cogni-tion. Empathy, a valuable social phenomenon,exemplifies this complex relationship becauseit draws on aspects such as emotion sharingand self-regulation. In addition, affective andsocial cognitive developmental neuroscience of-fers promising insights for both our understand-ing of typical and psychopathological socialbehavior.

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From emotion resonance to empathic understanding: A social developmental neuroscience account

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