1967 - Scheibel - Anatomical Basis of Attention Mechanisms in Vertebrate Brains

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erienced consciously. And as William James emphasized,ven a consciously learned response can become soabituated that it submerges to the non-conscious levelnd thereafter is taken care of quite automatically by theervous system, more or less on the same plane as genet-

cally endowed behavior.Perception, memory, learning, and consciousness are

ll biological activities of the nervous system. As Herrick

emarked: "The problem with which science is properly

concerned is not a search for liaison between brain as aphysical instrument and some other entity which is mind. What we must do is to discover those characteristics of brain as living tissue which enable it to have as one of itsown intrinsic physicalistic properties the awareness that we call mind. . . . What we need here is more knowledgeof the actual structure and operation of the nervous mech-anisms that do the thinking."55

Anatomical Basis of Attention

Mechanisms in Vertebrate Brains

M. E. SCHEIBEL and A. B. SCH EIBEL

COMPLEX OF neurons and fibers that constitute the mostrimitive part of the brain wanders through the substancef the brain stem. This archaic system shows little evidencef rigid structure, and approaches, in some respects, theommunication engineer's ideal of the statistical net. Weannot call this reticular formation truly isotropic, but here

ne can find no hint of the columnar arrays of corticalyramids, the file-on-file of bidimensional Purkinje cellsf cerebellum, nor even the whorled clusters of sensory eld cells, such as characterize analogically mapping fieldsf sensory relays.But perhaps as a result of this muted statement of its

ructural theme, there resides within the brain-stemore a remarkable pluripotentium of functional roles thatave become increasingly obvious over the past quarterentury and that probably mark it as the most critical

tegrative center of the brain—determiner of operationalmodes, gating mechanism for all sensory influx, modulatornd monitor of cortical function, readout mechanism forhe cortical differentiative and comparative processes andain manipulator for motor output. A brief,hronologically oriented survey of the development of ourhoughts about this multi-faceted system may proveseful in gaining insight into its present stature.

E . S C H E I B E L A N D A . B . S C H E I B E L D e p a r t m e n t s o f natomy and Psychiatry and Brain Research Institute, UCLA,

edical Center, Los Angeles, California

Historical resume

"It is known from embryology that most of the leftovercells of the brain stem and spinal cord which are not con-cerned in the formation of motor root nuclei and purely sensory relay nuclei are utilized in the production of theformatio reticularis." In this curiously negative mannercommences a short and prescient article by W. F. Allen,'published in 1932, which sketched out an envelope of functional roles for the brain-stem reticular core that wasto be followed by investigators for the next three decades.But the tenor of the sentence also reflects almost a century of neurological prejudice, which conceived the reticularcore of the brain stem largely as filler—a kind of neuro-ectodermally derived excelsior, in which were cushionedthe more functionally attractive cranial nerve nuclei.

During the past quarter century, there has been a dra-matic change in value judgments. Compared to the spec-trum of presently recognized reticular functions, ranging from homeostat operations practiced on the internal mi-lieu to modulation and control of highest psychic func-tions, the workings of cranial nerve nuclei seem almosthumdrum. If our appreciation of the astonishing range of physiological possibilities inherent in the core seems astrictly contemporary phenomenon, it was not necessary that it be so, for the anatomical and physiological litera-ture has been replete with clues pointing in these directionssince the turn of the century.

Anatomical studies of Kohnstamm and Quensel,2,3

N E U R A L S U B S T R A T E S O F A T T E N T I O N M E C H A N I S M S 577



which suggested pooling of a number of afferent and ef-erent systems upon the reticular core, led them to proposehis area as a "centrum receptorium" or "sensorium commue" - a common sensory pool for the neuraxis. Al-hough their attempts to interpret these data within ainical frame were not entirely convincing, implications of

heir thesis included the integration of heterogeneous con-ergent stimuli and an alternative centripetal path lashedn parallel with the classical long sensory tracts—both

stonishingly contemporary conceptions. At about the same time, Golgi chrome-silver studies by

Held4 and Cajal5 emphasized characteristics of input-out-ut systems and the possibilities for a spectrum of interac-ons between reticular cells and intrinsic axonal systems.ajal called attention to the characteristic bifurcating axo-al output of a number of reticular neurons and their pro-ction toward more rostral and caudal areas of the neu-

axis. The caudal-flowing system was established as pro-cting upon spinal cord by retrograde studies of Kohn-

am6

and van Gehuchten,7

and by anterograde (Marchi)tudies in the hands of Lewandowsky.8 However, the clas

sic Marchi study was that of Papez,9 who described threemajor descending (rcticulo-spinal) tracts, their apparentorigins in the brain stem, and their approximate terminallocations in the cord. This work, later to be amplified by anatomical studies of Niemer and Magoun,10 Torvik andBrodal,11 and Nyberg-Hansen,12 provides the hodological ( fiber bundle or tract) substrate for reticular modulation of spinal mechanisms.

The studies of Allen" offered a highly intuitive preview

of the physiological role of the core in modulating rostraland caudal structures. Allen was primarily an anatomist,so his conclusions were largely speculative. Furthermore,the time was not ripe for such ideas, and his paper was tobe forgotten for over a decade.

Equally pregnant was the discovery of Bremer,13,14

made only three years later, regarding the relation of brainstem to cortex. He noticed that after decerebration theelectrocorticogram of the resultant "cerveau isolé" prepara-tion swung into and maintained a high-voltage, slow-

wave rhythm that was maintained as long as the animalsurvived. Such rhythms had just been identified by

FIGURE 1 Schematic representation of the relations of thereticular core of the brain stem (black) with other systems of the brain. Collaterals pour in from long sensory and motortracts (thin lines) and from the cerebral hemispheres (arrowsdirected downward into reticular core). The core acts in turn

on cerebral and cerebellar cortices (upward-directed arrows)

and associated structures, on spinal cord (long, downward-directed arrow), and on central sensory relays (striped ar-rows). (From F. Worden, and R. Livingstone, 1961. Brainstem reticular formation, in Electrical Stimulation of theBrain [D. Sheer, editor], Univ. of Texas Press, Austin, pp.

263-276.)

78 BRAIN ORGANIZATION



omis, Harvey, and Hobart" and by Gibbs, Davis, andnnox" as consonant with sleep; so Bremer was able toch a conclusion of signal importance to experimentalurology. The cerebral cortex needs tonic sensory influxmaintain the wakeful state and, by implication, one of

e important roles of the long sensory tracts was to main-n, via continuous stimulus bombardment, a state of cor-al—and accordingly, organismic—vigilance. The bril-nce of this interpretation was scarcely marred by

emer's error in identifying the agency involved.The group around Alexander Forbes was the first to es-blish some of the physiological characteristics of thetral end of the extra-lemniscal (reticular) system. A sig-icant series of papers spanning the period 1936-1943 de-

mited its probable location within the thalamus, thedespread nature of its projection upon cortex, and thearacteristic pattern of recruitment waves that followedstimulation at low frequency.17'18 Following the war,se studies were expanded by Jasper and his associates."-"

ho defined in greater detail the probable anatomical

ths and electrophysiological characteristics of this sys-m. An interpretative capstone was placed on this grow-body of data with the suggestion by Penfield22 that thencephalic intralaminar system might well serve as a "

ntrencephalon" for all neural activity. The classicalchings ofHughlings Jackson23 as to the ultimate status of e cerebral cortex in the neuraxial hierarchy was thuspplanted. It had now become penultimate to the upperd of the reticular core, and the principle of thalamo-rtico-thalamic circulation already proposed by Cajal,'mpion," and by Dusser de Barenne and McCulloch25

ned support and experimental verification.In the meantime, the range of autonomic control exert-by brain-stem reticular mechanisms had been investi-ed by Ranson and his colleagues,26.27 thereby extending

e work of early investigators in this area, and culminat-in concepts of overlapping medullo-pontine fields sub-

ving respiratory and circulatory patterns. Out of thisveloped the observations of Magoun and Rhines28-3° onain-stem reticular override (inhibition and facilitation)ongoing spinal motor activity, with subsequent con-

ptual modifications by Sprague and Chambers." Short-

thereafter followed the epochal report of Moruzzi andagoun,32 describing reticular control over cortical ac-ity and its relation to the spectrum of conscious statesm attentive awareness to deep sleep. These workers at-

buted such effects to ascending polysynaptic conductioner successive chains of short-axoned cells. That theseenomena, in reality, depended importantly on high-ority conduction in oligosynaptic and, in some cases,onosynaptic channels to cortex was suggested by ourolgi studies33 and more recently by intracellular analyses

of Magni and Willis."Results of selective destruction of lemniscal and extra -

lemniscal (reticular) systems by Magoun and a group of collaborators35,36now placed the original findings ofBremer","in correct perspective, as it became increasingly clear thatextralemniscal, rather than direct sensory-tract volleys, were crucial to maintenance of cortical tonus. By implication, sleep remained a passive process consequentto decrementing levels of reticular activity, despite earlier

studies by Hess,

37,33

which had shown that it could be ob-tained by stimulation of appropriate brain-stem sites. It re-mained for Jouvet33," and Rossi41,42 to document a complexof interrelated states and to focus attention on an anatomicalinterface in the rostral pons separating areas apparently productive of rhombencephalic (activated) sleep fromclassical slow-wave sleep (see Jouvet, this volume).

Still another significant facet of reticular-core activitieshas been revealed by Galambos43,44 and Hernandez-Pe6n,45, 48

who have been able to relate the size of sensory evokedpotentials to the focus of active interest momentarily ex-

pressed by implanted, freely mobile animal. Our ownGolgi investigations33,47 have revealed a suitable substrate inthe penetration of most first- and second-order sensory stations by reticular collaterals. Notwithstanding a recentdisclaimer by Worden and Marsh,'" it is generally con-ceded that, aside from modulation of tonic and phasiccomponents that comprise the activated state,'" the reticu-lar core mediates specific delimitation of the focus of con-sciousness with concordant suppression of those sensory inputs that have been temporarily relegated to a secondary role.

Knowledge of the intimate physiology of the core hasbeen gleaned from extracellular microelectrode studies by a number of investigators,'°-52 and most recently by alimited number of intracellular analyses34,53," that haveexamined in some detail the problems of convergence of sensory signals, habituation (response attenuation) of in-dividual units to iterative stimuli,55.56 and a cyclical alter-nation of unit sensitivity to the stimulus array.57 At thesame time, a group of Golgi studies has revealed muchabout the relevant substrate,33,58-" and in providing circuitparadigms for a system with this order of functional com-

plexity, has also suggested program modes applicable tocomputer design.62

The core as a mosaic

In the tradition of the great cortical cytoarchitectonicists ( i.e., Brodmann," the Vogts," von Economo," etc.), anumber of attempts have been made to subdivide the re-ticular core of the brain stem into component nuclei on




the basis of its appearance after aniline staining. The mostdetailed essay in this direction is that of Olszewski and hiscollaborators," who have identified more than 40 nu-clear entities in man, and almost as many in rabbit, in theinterval between the spino-medullary junction and therostral mesencephalon. The most obvious advantage of such a system is the moderate degree of uniformity pro-vided in an invariant vocabulary for descriptions of vari-ous portions of the core. Thus, all who are acquainted

with Olszewski's atlas will visualize approximately thesame sector when asked to consider, for example, the nu-cleus reticularis pontis caudalis. However, the originalbases for cytoarchitectonic identifications are often ar-bitrary, and individual judgments vary as to where a pat-tern of somal morphology or distribution becomes suf-ficiently different to merit recognition as another nucleus.The problem is particularly vexing in the reticular core,where obvious transitions are the exception rather thanthe rule, and cells of many sizes are intermingled.

The significance of somal size and distribution can be

questioned as adequate criteria for isolation of a nuclearfield. In a complex territory like the brain stem, it is at bestan assumption that these factors will mirror differences ininput arrangements, efferent destinations, local specializa-tion of the microchemical environment, presence of spe-cific synaptic mediators, etc. A more likely disclaimer tothe validity of such parceling is the appearance of theseareas when impregnated by one of the Golgi modifica-tions. The long, relatively unramified dendrites character-istic of cells of the reticular core stream in all directions, es-pecially when studied in transverse section. Such processes

transcend the cytoarchitectonically determined nuclearlimits, projecting into neighboring and even remote nu-clear subdivisions. Examination of a number of species in-dicates that the total extent of the dendritic domain of asingle cell may exceed one-third of the total cross-sectionalarea of the stem.68 The processes of such a cell can easily in-vade as many as half a dozen extraneous nuclear pools.

We may conclude that the apparent isolation of eachcore nucleus from its neighbor is entirely an artifact or, al-ternatively, that the relative segregation of cell bodies andthe mingling of dendrite shafts express fundamental dif-

ferences in the physiology of these entities (Purpura, thisvolume). As is usual in cases such as this, truth will prob-ably be found to lie somewhere between.

Dendritic apparatus

The morphology and patterning of dendrites has been asubject of interest since the initial studies of Golgi.69 Withthe exception of the lateral reticular nucleus (noyau du

cordon lateral'),dendrites of reticular core cells appear rela-

tively straight, long, and unramified. The uniqueness of this pattern has been remarked by a number of investiga-tors,5,70,71 and referred to as isodendritic by one group," who see in its similarity to archaic patterns a relation to in-tegrative rather than differcntiative or comparative func-tion. Such dendrites are characteristically thick (3 to 8 mi-crons) at the somal junction, and may taper over a courseof several hundred microns or more to terminal segmentsonly a fraction of a micron in diameter. Golgi sections sug-

gest, and electron micrographs show, that the dendritetips may be quite as densely covered with presynapticstructures as more proximal portions of the shafts. Thefunctional significance of terminal structures committed tosections of postsynaptic membrane so distant from thepresumed spike-trigger area around the axon hillock re-mains a question of more than theoretical interest (Pur-pura, this volume, and Note 78).

The available dendritic (postsynaptic) membrane islarge, often constituting 85 to 95 per cent of the total re-ceptive surface of the neuron." Such a figure agrees with

estimates of Sholl74 and others for the fraction of post-synaptic membrane represented by the dendritic segmentof cortical neurons. The surface of these processes is irreg-ular, often nodular, and unevenly covered by hairy pro-tuberances, or "spines." The reality of the spiny apparatushas been attested by electron micrographs by Gray" andothers, with the suggestion of elaborate intraspinous struc-tures—at least in cortical spines—and a special populationof presynaptic junctions effected at the apex or base of thespine. Although these structures are not so numerous (0.1to 0.3 per linear micron) as in cortex (0.4 to 0.7 per linear

micron)," their presence is virtually invariant and indi-cates an as-yet-unknown specialization of postsynapticmembrane.

If the dendrites radiate widely, as seen in cross section,their appearance is very different in sagittal planes. Themajority of reticular neurons over the medial two-thirds of the core continue to show impressive degrees of spread inthe transverse dimension (dorso-ventral and latero-lateral),but little or no projection in the rostro-caudal dimension. The appearance is one of marked compression along thelong axis of the stem, resulting in a series of flattened den-dritic domains, piled one on another like a stack of pokerchips. We originally suggested33 that this configuration in-troduced a significant dimension of localization of input,because each cell thereby "looked" only at a limited seriesof inputs from a single level along the input continuum. This seemed especially likely, as presynaptic componentsinvariably parallel the postsynaptic (dendritic) surface, and virtually all terminating axonal elements pour into thecore at right angles to the long axis. The modular nature of this "stack of chips" organiza-

580 BRAIN ORGAN I ZAT ION



Tr.sP.

.r. -

N.mes.V-p.Br

.e e-

ros ra

RI.

NV

.

.

N.XII cau a

V P

N.Ir.sp.V

.s.act:-

IGURE 2 A series of equally spaced drawings of transverseNissl-stained sections through the brain stem of the cat to

how the grouping of cells in the reticular core. Various-zed dots on the right indicate specific cell bodies, whileotted lines on the left indicate approximate boundaries of

major reticular nuclei. Terminology and nuclear areas areased on the studies of Olszewski in the rabbit, with minor

modifications. The following list of abbreviations refernly to structures making up the reticular core: a,

Accessory group of paramedian reticular nucleus: d, Dorsalroup of paramedian reticular nucleus; h, region poor inells of Meesen and Olszewski surrounding motor

igeminal nucleus; k, cell group k of Mecsen and

group m of Meesen and Olszewski; N. ic., Nucleus inter-calatus ; N. in., Nucleus interpositus; N. r. 1., Lateral reticu-lar nucleus; N. r. p., Nucleus reticularis paramedianus ;N. r. t., Nucleus reticularis tegmenti pontis; N. t. d., Dorsaltegmental nucleus; N. t. v., Ventral tegmental nucleus;P. g. Periaqueductal gray; P. h., Nucleus prepositus hypo-glossi ; R. gc., Nucleus reticularis giganto-cellularis ;Nucleus reticularis lateralis (of Meesen and Olszewski); R .mes, Reticular formation of mesencephalon; R.n., Nucleusof the raphe; R.p.c., Nucleus reticularis parvocellularis ; R.p.o., Nucleus reticularis pontis oralis ; R.v., Nucleusreticularis ventralis; v, Ventral group of paramedian reticu-

lar nucleus. (From Brodal, Note 80)




FIGURE 3 Cross section through upper medulla ofnew-bornkitten, stained by the Golgi method, showing the generalappearance of reticular cell bodies and dendrites at this level.

There is marked variation in size and shape of both den-drites and cell bodies. The dendrite systems tend to radiatein all directions in this plane of section and sometimes to in-

vade a fiber bundle from which they receive excitation. Ab-breviations : C. Rest., restiform body; n VIII (Deft.), Deitersnucleus of the vestibular complex; n.VIII (Schw.),Schwalbe's nulceus of the vestibular complex; MLF, mediallongitudinal fasciculus ; n.V.d., descending nucleus of thetrigeminal nerve; Tr. Pyr., pyramidal tract.

onal pattern has recently been exploited by Kilmer andMcCulloch,62 who have used it as a paradigm for a new eneration of computers, which will show increased de-rees of flexibility in dealing with data influx, will habitu-e over time to iterative stimuli, etc. Although the con-

ept of a reticular core made up of a subinfinite number of modules as numerous as its cellular complement may seemverly divisive, it shows a rather good conceptual fit witheas emerging from single-unit analysis of the structure 5°_52

As we will stress again, most neurons appear to receivepon their soma-dendrite surfaces an appreciable, but not

nlimited, convergent sampling of the many inputs af-rent to the core. Each neuron receives its own idiosyn-

ratic mix—in terms of afferent selection and loading— om the total influx, so it has seemed appropriate to somef us52 to consider each neuron as an integrating subcenter,perating upon its own peculiar combination of afferents.he sum of these neuronal subcenters would, in turn,

make up the total mosaic of the operating reticular core,n which each element performed operations upon oneegment of the total envelope.

If we accept each reticular element as one of a family

that samples a limited and idiosyncratic fraction of thetotal reticular afferent supply, we might pause to con-sider the relative significance of neuronal soma and den-drite, respectively, in servicing the presynaptic array. The

widely ranging dendritic apparatus has already been seento penetrate areas rather remote from that of the parent cellbody, in quest of presynaptic excitation. We have suggestedelsewhere that the dendrites appear to point toward, andreach for, potent sources of influx, which suggests thattrophic or neurobiotactic forces are operant during the de-

velopmental phase. We have previously shown evidence

of clear-cut segregation of afferent terminals on variousportions of dendrite shafts in cortex" and on spinal inter-neurons." Although we do not have evidence of concen-trated afferent terminal populations on various portions of single reticular dendrites, there seems little doubt thatmany reticular cell dendrites will show marked predomi-nance of inputs, depending on the location of that shaftrelative to the spectrum of afferent sources (Figure 5).

Thus, for a cell located in the ventral-lateral quadrant of medulla, it might be appropriate to refer to shafts that are

predominantly cortico-spinal loaded, spin-thalamic load-

82 B R A I N O R G A N I Z A T I O N



FIGURE 4 Sagittal section through the lower half of thebrain stem of a 10-day-old rat. Most of the dendrite mass of reticular core cells is organized along the dorso-ventral axisas seen in this type of section, with marked compressionalong the rostro-caudal axis. This orientation places thedendrites parallel to the terminal presynaptic components

hich in this case arise from pyramidal tract (Tr. Pyr.) andfrom a single axon of a magnocellular reticular neuron (n.

retic. mag.). This type of dendrite organization, which isespecially characteristic of reticular cells of the medial2/ 3 of the core, produces sets of essentially two-dimensional mod-ular neuropil fields leading to the stack of chips analogy (seetext and inset diagram at lower left). This is contrasted withdendritic patterns in the adjacent hypoglossal nucleus (n.XII); n. inf. ol., inferior olive; n. pontis, the pons. (FromScheibel and Scheibel, Note 33)

descending trigeminal loaded, etc., thereby emphasiz-

the predominant population of afferents to be foundthat process.However, this concept suffers some dilution becauseh reticular cell lies in a matrix of fibers, largely (al-ugh not entirely) core derived and projecting for vary-distances in the rostro-caudal (and occasionally trans-se) direction. It is a characteristic property of suchns to give off collaterals at right angles more or less

ntinuously along their path.33,60 These collaterals makea spectrum of lengths; some constitute little more than

nimal specializations of the fiber in transit (boutons-en-

sage). Each reticular dendrite must thread among thehs of tens of thousands of such axons, so a considerablember of axodendritic contacts must be expected from

source, even if mere contiguity of nonspecialized axonnductors with dendritic membrane is not in itself suffi-nt for information transfer. It seems logical to expandhypothesis of sensory-annotated dendritic monads toude in each case a sprinkling of core-derived afferents.e moment-to-moment dendritic membrane loading uld thereby represent an integrate of specific and non-cific inputs. In turn, the algebraic summation of such

states for each major dendrite shaft of a specific reticular-

core neuron would represent (with additions from thesomal synaptic scale) the level of synaptic drive being ap-plied to the soma—initial segment at a specific point intime.

It seems beyond question that the output of each reticu-lar element represents a vector of this type; it thereforefollows that specific informational content, intrinsic to each of

the afferent sources, is lost in the integrative process. The out-put of each unit must represent intensity only. It may notbe out of place to suggest the analogy that a major func-tion of the core is to describe not the pageantry and color

of the passing parade, but the loudness of the shouting thataccompanies it.

The presypnatic influx

The reticular core of the brain stem may be thought of assitting athwart all incoming and outgoing information-carrying systems. The collaterals and terminals that pourin at every level receive a continuous stream of samples of the activity ongoing in these tracts. In general, archaic af-ferent and efferent systems, like the spino-thalamics and




FIGURE 5 Semi-schematic cross section through upper thirdof medulla, showing relations of a few presynaptic com-ponents to dendrites and somata of reticular neurons. Somedendrites appear to point toward the source of their mostsignificant presynaptic supply, individual fibers of whichmay effect multiple terminations along a single dendriteshaft. The nature of synaptic loading along each of a group

of dendrites radiating from a single soma may be unique.

though the apparent segregation of presynaptic supply is very obvious in this sketch, the density of presynaptic ter-minals in the core actually results in appreciable degrees of convergence of heterogenous afferents upon each shaft. Vestib. compl., vestibular nuclear complex;V. Desc., de-scending trigeminal; Lem. sp., lemniscus spinalis (spino-thalamic tract); Tr. Pyr., pyramidal tract; MLF, medial

longitudinal fasciculus.

extrapyramidals, are more thoroughly represented thanthe phylogenetically newer tracts, such as the dorsal col-umn—medial lemniscus and pyramid. The former (medialemniscus), in fact, probably contributes no collaterals tothe core, thus suggesting that information with a high de-gree of locus and mode specificity is not crucial to the op-

eration of the reticular mosaic. A fairly massive spino-reticular system introduces af-ferent activity into medullo-pontine levels, along the long axis of the tract, as do descending components in the cen-tral tegmental fasciculus and the brachia efferent fromcerebellum. The most consistent afferent source, however,appears to be the collaterals that pour in from sagittally coursing fillets along the ventral and lateral aspects of thestem and on each side of midline.5,33 In general, the ag-gregate of reticulopetal fibers (fibers afferent to the reticu-ar core) may be divided into several categories, which in-

dude: (1) fibers from more rostrally placed centers (cere-bral cortex, basal ganglia, diencephalon, and limbic or al-locortex) ; (2) fibers ascending from the spinal cord; (3) fi-bers originating in the cerebellum and other brain-stemstructures such as the geniculate bodies, colliculi, etc.

These data are discussed in comprehensive form in several

places.79,80

Accordingly, only a few summarizing state-ments will be made here.

THE CORTICO-RETICULAR PROJECTION This makes upthe most dramatic, if not the largest, descending system.

The fibers originate in an area centering on the sensor-motor strip, but extend rather widely into adjacent corti-cal areas, and terminate in "nucleus reticularis giganto-cel-lularis, more rostally than caudally, while the pontine ter-minal region is found in the nucleus reticularis pontis oralisand the nucleus reticularis pontis caudalis, chiefly in its




stral part."" Some terminations are also found in nu-us reticularis tegmenti pontis.Of particular interest are the components descending in-ectly from the limbic system upon midline tegmentaluctures, a projection studied in some detail by Nauta.82

seems clear that several routes are taken through thala-us and hypothalamus, with the eventual focus upon theesencephalic nuclear fields of Bechterew and Gudden,m which arise an ascending system to complete a mas-

e limbic-midline circuit. Informational by-products of ivity in this circuit may also be disseminated laterally

roughout the tegmentum and central tectum by themewhat enigmatic radiation first described by Weis-hedel.83 We are as yet unable to decide from our materialether this represents the fine-fibered lateral projectionlarge numbers of small neurons situated in the peri-

ueductal gray, or, in whole or in part, a projection of uroglial stalks, running from periependymal neurogliaat line the Aqueduct of Sylvius. If the latter possibility ould be proved, it might introduce interesting possibili-

s for neurohumoral interactions at this level of the core.

ESCENDING TECTAL COMPONENTS Originating in theliculi and pretectal area, these components terminate in

e same general areas as do cortico-reticular components,obably as part of the tecto-bulbo-spinal correlation sys-m. The terminal patterns of reticulo-petal componentsm basal ganglionar and diencephalic sites must still berked out completely, although Golgi material indicates

hierarchy of fiber lengths and terminal stations through-t the length of the core.'"

INO-RETICULAR FIBERS These fibers originate from allels of the cord,80,84 ascend in the ventro-lateral funiculus of

e cord and terminate along an extensive core of medullo-ntine tissue, roughly congruent with areas of termi-tion of the cortico-reticular projection. In addition, anpreciable fraction of spino-reticular elements projectrough, or terminate in, the lateral reticular nucleus,hich also receives many of the lower brain-stem termi-s of the spino-bulbo-thalamic system. This nucleus

ojects, in turn, upon cerebellum, while the majority of ore centrally placed reticular fields (excluding para-edian nucleus and nucleus reticularis tegmenti pontis) re-e back only to upstream or downstream centers."

HE CEREBELLO-RETICULAR CONTINGENT The con-gent enters the stem directly via the superior and in-ior cerebellar peduncles. (The former is found primarily the hooked bundle of Russell.) As summarized by Bro-," major terminal stations in the reticular formation in-de nucleus reticularis tegmenti pontis and nucleus re-

ticularis pontis caudalis, the paramedian nucleus, and por-tions of giganto-cellularis.

AFFERENT PROJECTION UPON THE RETICULAR CORE De-tails can be studied in Golgi sections through the uppermedulla, which will serve as a paradigm. Figure 6 showsthat collaterals from long ascending and descending tracts ( i.e., spino-thalamic, descending trigeminal, vestibulo-spinal, tecto-bulbo-spinal, cortico-spinal, etc.) turn into

the plane of section and terminate in overlapping patterns within the reticular core. At a higher level of resolution ( Figure 7, right side), these terminals can be seen to coverthe soma and dendrites of most neurons within the field,thereby making up the total roster of afferent supply orsynaptic scale85 upon the neuron.

The convergence of such a heterogeneous afferent array can also be demonstrated physiologically by means of oc-clusion techniques with macroelectrodes and by single-unit recording methods with the extracellular or intracel-lular microelectrode. The left side of Figure 7 shows strips

from a series of records illustrating the response of a singleunit to a group of disparate inputs, as well as its lack of re-sponse to others. Data of this sort underline the extensivebut not unlimited convergence of inputs upon each reticu-lar element. The unique quality of the synaptic "mix"upon each neuron emphasizes the mosaic-like nature of thecore, with each neuron acting as a tiny integrating subcen-ter within the complex.

Cyclic phenomena

Anatomical analysis of an input array spread over thesoma-dendrite complex of the average reticular neuron issharply and unequivocally stated when subjected to suc-cessful Golgi staining or electron micrography. Further-more, mechanical techniques that attempt the separationof synaptic boutons from the subsynaptic membrane bear

witness to the tenacity with which presynaptic endingscling to the postsynaptic ensemble. Such procedures, inthe hands of de Robertis,86,87 who has differentially cen-trifuged the various fractions of crude separata down

through a series of sucrose interfaces, reveal numerous ele-ments in the bouton fraction still clinging to fragments of postsynaptic membrane. Clearly, this is no relationshipthat can be reversibly severed by the swing of an astrocytetail, as was once hypothesized by Cajal.5

Yet, electrophysiological data that we have gatheredfrom long-term, extracellular recording from a number of medullo-pontine reticular elements suggest that no matterhow anatomically stable the synaptic relationships appearto be, their functional interactions are dynamic and cy-clic.57 In about 80 per cent of the reticular elements from




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FIGURE 6 Transverse section through the upper third of the medulla ofa 10-day-old kitten, showing the convergenceand overlapping of terminating afferent fibers in the reticu-lar core. On the left, a small group of fibers are drawn di-rectly from the microscope; on the right, as a group of overlapping sectors. Reading clockwise from the top, theafferents include the descending periventricular system (Tr.

Periventr. desc.); vestibulo-reticular fibers (Vestib. retic.) ;the uncinate fasciculus from cerebellum (f. Unc.) ; the tractof the descending fifth nerve (Tr. V desc.); lemniscus spinalis ( spinothalamic tract) (lernn. spin.); pyramidal tract (Tr.Pyr.); and midline white matter, including medial reticulo-spinal fibers (T. Rs. med., etc.). (From Scheibel and Scheibel,Note 33)

3,

which we were able to record for periods of from 10 to 12ours each, there was a succession of reactive phases dur-

ng which the cells appeared alternately sensitive to sen-ory bombardment from the external milieu (mild sciatichocks of 1 to 2 volts of M millisecond, administered at 1-er-second frequency) and from the internal milieu, asxemplified by rhythms following the respiratory cycle.

During these respiration-sensitive periods, the reticularlements were completely refractory to exteroceptive

timuli (Figure 8). Similarly, during sciatic shock sensitivehases, no traces of interoceptive-modeled activity werever seen. Each cell seemed to follow a unique temporalattern within a general order of magnitude of M to 3ours (Figure 9). There was no discernible relation of thesewings to sleep-wakefulness cycles nor were there indica-ons of general physiological changes serving as substrateo the alterations.Speculation on the mechanisms underlying this phe-omenon include hypothecated endocellular rhythms,

which periodically change the receptive sensitivities of the

subsynaptic mosaic (see notes 88 and 89 for empirical dataof possible relevance to this problem). An alternative sug-gestion regarding mechanisms is the presence of a popula-tion of pacemaker neurons that controls postsynaptic re-sponse either through presynaptic manipulation90,91 or viainteraction of satellite oligoglia, which we have shown re-ceive terminating collaterals from the same preterminalsthat innervate the neuron.92 Each suggestion carries with itits own intrinsic problems, the most intriguing of which

endow our speculations on the pacemaker.In a cellular matrix as complex as the reticular forma--'

tion, if one hypothesizes a pacemaker elite that comprises a;,

fraction of the mass of followers, the quest for order sug-gests a hyper-elite to pace the pacemakers, and so on to theultimate absurdity of one supreme, pontifical neuron. Atmore attractive variant of this hypothesis involves mobile a

nd redundant command, which temporarily vests pacinactivities on those local arrays whose information loadinis of a more biologically urgent nature than that of adojacent, more indecisive domains. As this content-mosai






FIGURE 8 Bulbar reticular unit showing responsiveness first toendogenous, then to exogenous stimuli. Strips A through Gshow a bulbar unit driven by respiratory activity but totally non-responsive to sciatic stimulation (1/sec, 2 volts, 1/2 msec). StripH shows activity of the same unit 1/2 hour later. It is now highly responsive to the same type of sciatic stimulation but shows noevidence of being driven by respiratory activity. (From Scheibeland Scheibel, Note 57)

The axonal outflow

The axonal outflow of the reticular core consists of a spec-trum of conducting systems projecting in three main di-rections—caudally upon spinal cord, rostrally upon sub-cortical and cortical centers, and dorsally to cerebellum.In addition, a vast and complex pattern is generated by theoutput of the core operating upon itself through collat-erals en passage. Axonal collaterals of greater length also

penetrate sensory and motor nuclei of cranial nerves enroute. The first three projections can be demonstrated withsome degree of rigor by the usual hodological methodsemploying retrograde or anterograde degeneration. Using modifications of the latter, Broda80 has shown that a systemof reticulo-cerebellar projections originates from the lateraland paramedian nuclei and from the nucleus reticularistegmenti pontis, which differ appreciably in their terminalstations. Use of the same technique has shown that thereticulo-spinal projection arises from cells spread along themedial two-thirds of medulla and pons, with particular

reference to nuclei pontis oralis et caudalis, nucleusreticularis giganto-cellularis, and reticularis ventralis.Similarly, ascending reticular axons identified by lesionsat the meso-diencephalic junction (Figure 10) arise fromthe same general nuclear fields, suggesting either an in-

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F I G U R E 1 0 A lesion at the meso-diencephalic junction of cat brain stem and the position of cell bodies originally send-ing rostral-coursing axons through the site as determined by retrograde techniques (see text). Notice that a predominantly unilateral lesion results in degenerating cell bodies (dots) onboth sides of the stem more caudally, and as far posteriorly as the middle third of the medulla. S.n., substantia nigra ;III, third nerve nucleus and nerve; Elm., medial longitudi-nal fasciculus; N.r., nucleus ruber ; P, pons; C. s., superiorcolliculus; IV, fourth nerve nucleus; N.r.t., nucleus re-

ticularis tegmenti; C.i., inferior colliculus; N. mes. V,mesencephalic root of the fifth nerve; N.t.d., dorsal teg-mental nucleus; N.1.1., nucleus of lateral lemniscus ; VI, sixthnerve nucleus ; N VII, seventh nerve; N.n.V, sensory trigeminal nucleus; N.c., cochlear nucleus; 01.s., superiorolive; P.h., perihypoglossal nucleus; N.f.c., cuneate nu-cleus; N.c.e., external cuneate nucleus; T.s., solitary tractand nucleus; N.m.X, motor tenth nerve nucleus (Vagus); Tr. sp. V., descending trigeminal tract and nucleus; N. XII,twelfth nerve; 01.i., inferior olive. (From Brodal, Note 80)

N E U R A L S U B S T R A T E S O F A T T E N T I O N M E C I I A N I S M S 589



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GURE 11 Distribution of reticular cells sending axons rostrad ( ft) and caudad (right) is indicated in two semi-schematic sagit-sections of brain stem of cat. Although there is a good deal of

verlapping, caudally directed axons appear to arise somewhatore rostral than rostrally directed fibers. The arrows at the side

f the figures indicate that all axon systems are both crossed andncrossed, except fibers descending from pons, which are un-ossed. Abbreviations as in previous figures. (From Brodal,ote 80)

scriminate mingling together of rostral- and caudal-rojecting cells, or a source in common from many of theme neurons (Figure 11). Our Golgi studies indicate thatoth of these alternatives exist.Anterograde studies, employing modifications of theielschowsky reduced-silver method, allow certain state-ents to be made as to terminal stations of ascending andescending projections. Reticulo-spinal fibers have beenollowed in ventral and lateral funiculi to termination in

pinal laminae 7 and 8.12 In some cases, Golgi preparationsf spinal cord show such fibers terminating along den-rites and somata of internuncials and occasionally along e outer segments of motoneuron dendrites. In the latter,

he anatomical material is not sufficiently precise to dif-rentiate alpha from gamma motoneurons."Rostral projections have been followed by a number of

workers using Marchi, Glees-Bielschowsky, and Nautaethods (Figure 12). There is general consensus that thecending system projects dorsally into the thalamic

FIGURE 12 Degeneration of ascending fiber systems, as seen insagittal section following a lesion in the caudal midbrain teg-mentum, visualized by means of the Nauta method of antero-grade degeneration. Large dots represent fibers of passage; fine

stipple represents probable preterminal axons. LM, medial lem-niscus ; IP, interpeduncular nucleus; MI, massa intermedia ; CS,superior colliculus; NR, nucleus ruber ; MT, mamillothalamictract; V, ventral nuclear complex; L.DL., lateral dorsal nucleus;DM, dorsomedial nucleus; BC, brachium conjunctivum; SN,substantia nigra; AD, anterior drosal nucleus; AM, anteriormedial nucleus; f, fornix; CA, anterior commissure; CP, pos-terior commissure; PM, mamillary peduncle; CM, mamillary body; Pc, paracentral nucleus; CI, inferior colliculus. (FromNauta and Kuypers, Note 95)




nar system, especially to the paracentral and centralal nuclei and possibly as far rostrally as the nucleusularis thalami. Although there are some reasons—bothomical and physiological—for expecting terminationsntre median, it has also been suggested that degenera-granules found in this area are purely of en passage ty and do not represent functional preterminal ele-ts." The ventral prolongation of this system can be

ed into the zona incerta of hypothalamus and the fields

orel. Lesions placed progressively more rostrally andrally in mesencephalic tegmentum reveal axonal sys-that reach preoptic, septal, basal-forebrain, and basal-

lionar stations. The vexing problem of whether directosynaptic connections are established with cortex by of these elements has not yet received a satisfying an-from these techniques 9 5

useful as these tracking methods have proved to be,mains for the Golgi methods to demonstrate the rich-

ness and complexity of reticular projection systems— preferably viewed in sagittal sections of postnatal mice andrats (Figure 13). Although admittedly "simpler" thancarnivores and primates, the rodent brain stem can wellserve as a paradigm for higher forms, while escaping muchof the circuit redundancy that makes Golgi analysis of larger brains so difficult. The axons of reticular neurons form a spectrum of con-

ductors of many lengths. Some neurons appear to project

rostrally only; and others only caudally, but a significantnumber of medium-sized and large reticular elements gen-erate the familiar bifurcating axon (Figure 14) that may project to distant stations both upstream and down. Vir-tually all of these are characterized by collaterals of vary-ing lengths that leave the main stem perpendicularly andpenetrate into adjacent reticular areas. Longer collateralsmay reach cranial nerve nuclei and/or sensory relay andextrapyramidal motor fields. A number of fiber counts

FIGURE 1 3 Sagittal section of an entire mouse brain (7 daysold) showing 2 reticular cells in the magnocellular nucleusof rostral medulla. Both cells emit axons that bifurcate andcourse rostrad and caudad. A number of collaterals are givenoff by each axon, some of which reach cranial nerve nuclei,such as Deiter's component of the vestibular complex, n.D.;

both inferior and superior colliculi, I.C. and S.C.; and pre-

tectum, Pt. Other abbreviations include CM, centre me-dian; LP, lateral posterior; LG, lateral geniculate; LD,lateral dorsal; CL, central lateral; AV, anterior ventral; V,

ventral complex; VA, ventral anterior; R , nucleus reticu-laris thalami; ZI, zona incerta; and SN, substantia nigra. ( From Scheibel and Scheibel, Note 33)




FIGURE 14 Sagittal section through the brain of a young rat showing the axonal trajectory of a single neuron of thenucleus reticularis giganto-cellularis, R. The rostral-coursing axonal component supplies collaterals to inferiorcolliculus, j ; the region of the III and IV nerve nuclei, i;mesencephalic tegmentum, h; posterior nuclear complex of thalamus, f; dorsal, intralaminar and ventral thalamic nucleirespectively, e, d, and c; zona incerta of hypothalamus, g;nucleus reticularis thalami, b; and basal forebrain area, a.

directed component sends collaterals into the substance of the reticular core, m; the hypoglossal nucleus (XII), k; thenucleus gracilis, 1; and the intermediate gray matter of thespinal cord, n. (This illustration was originally prepared forpublication in Brazier, M. A. B., "The Electrical Activity of the Brain"; Third Edition, New York, The MacmillanCompany; in press, and is reproduced here with permissionof the author.)

have suggested to us that, on the average, each reticularxon releases one collateral of approximately 100-micronength for each 100 microns of trajectory." This does notnclude large numbers of smaller, bulb-like enlargementslong the course of the axon, called by Cajal boutons-en-- assage 5 and representing, according to electron-micro-

graphic analysis, centers especially rich in mitochondriand other intra-axonal organelles. The picture that emerges is one of continuous, intensive

nteraction between large numbers of conductors and theurrounding matrix of core neurons. The nature of theseontacts must vary, depending on the presence or absence

of a myelin sheath and the frequency of axonal specializa-ions. No definite statement can be made about the func-ional significance of the untold numbers of contacts es-ablished among structures without discernible axonal (or

postsynaptic) specialization. It is currently fashionable todiscount the significance of such membrane appositions aseen in electron micrographs if there is no evidence of

membrane thickening, increased opacity to the electronbeam, or presence of synaptic vesicles behind one of the

apposed membranes. However, the presence of trans-membranal electrogenic effects has been shown to exist atleast in invertebrates,96.97 and Nelson and Frank havemapped a considerable field effect around spinal motoneu-rons in the cat." Pending more rigorous analysis with re-cording techniques of higher resolution, no definitivestatements can be made about the presence or absence of aspectrum of field interactions and threshold manipulatory effects in a dense complex of long conductors and axoden-

dritic neuropil such as the reticular core.However, the patterns of connectivity that can be traced

out through the core suggest a circuit scheme so richly redundant that convincing arguments could be advancedfor almost any conceivable loop or chain. Figure 15 sum-marizes three alternatives. The first depends largely onpolysynaptic chains of short-axon elements similar to thescheme originally suggested by Moruzzi and Magoun.2

The second illustrates the collateral-rich, long-projecting,high-priority axon now known to characterize many re-t i c u l a r

neurons. The third combines a group of these, geo-graphically staggered, so that each is activated somewhat




GURE 15 Schematic showing three possible circuit paradigmsrough the reticular core of the brain stem. a: the chaining of ort-axoned cells as suggested by Moruzzi and Magoun. b : a

ngle long-axoned, high-priority conductor reaching from lowerain stem (left) at least as far as diencephalon (right) withoutna tic interru tion. This resembles a t e of reticular axonctually found in large numbers in the core. c: an ensemble of uch long axons, whose collateral systems, playing upon adjacentements similar in nature, but geographically staggered, can re-

ult in a s ectrum of conduction latencies and diver ence of in-mation. (From Scheibel and Scheibel, Note 33)

er in time, resulting in appreciable degrees of spatial andmporal dispersion. Such an array could also account fore appearance of a family of response latencies over intra-

ticular conducting paths, as demonstrated by Adey,gundo, and Livingston."The rostral course of axonal elements of medullo-pon-ne and mesencephalic tegmental neurons has already en mentioned in part. While the dorsal thalamic leaf

most certainly projects no farther than the intralaminarlds and nucleus reticularis thalami, the ventral leaf, ex-nding through ventrolateral hypothalamus, in someses may be traced to, and through, the basal forebrain aread ventral caudate-putamen. By using very thick sections (

00 micron) of perinatal mouse, we have been able to

ace a limited number of axons from brain-stem reticularrmation to the base of the anterior third to half of cortex.

We estimate that the number of such monosynaptic corti-petal conductors is relatively modest—perhaps of theder of 5 to 10 per cent. Although we are still working onis problem, it is of interest that Magni and Willis34 havecently succeeded in antidromically activating smallumbers of micropipette-impaled, brain-stem reticularurons via cortical stimulation. They consider their datansistent with the presence of some reticular elementsat project monsynaptically upon cortex.

The thalamic system

The nonspecific system of the thalamus differs in organiza-tional pattern and functional role from the remainder of the brain-stem reticular core. It is also partially isolatedfrom reticular structures of the lower two thirds of thestem, so it seems appropriate to deal with it separately. Ac-cording to Jasperm100 "the thalamic reticular system isthe dorsal limb of the cephalic end of the brain stemreticular formation. . . . [It] is sometimes identified with theunspecific thalamocortical projection system. This may not be accurate, since unspecific projections may be only one important property of the thalamic reticular system."Generally included within its domain is the calyx of medialand intralaminar nuclei that run forward from the centremedian-parafascicular field to surround the dorso-medial complex and separate it from the ventro-lateralfields just outside. Mpre rostrally, the system includes—atleast at a functional level—portions of antero-medial and

ventral-anterior nuclei and the nucleus reticularis thalami

(Figure 16). The group of small cell masses making up theinternal medullary lamina itself includes central-medial,paracentral, central-lateral, and a group of more variablemidlinebridging nuclei, i.e. reuniens, rhomboidalis,interanteromedialis. Previous descriptions of these areasmay be found in various studies,5,101,101 while adequatesummarizing statements of their functional capabilities havebeen offered by Jasper100,105 More recent discussions of problems inherent in the experimental analyses of thesystem have also been provided.94,106

The present discussion is limited to data that haveemerged from our analysis of thalamic nonspecific sys-tems, using Golgi methods. It is worth passing commentthat problems in visualization of the intricate neuropil of this system were noted by Cajal 60 years ago5 and probably have been largely responsible for the dearth of informationon structural substrates of this intriguing area. Our ownmaterial is presently based on analysis of approximately 2000 rodents, cats, and a few primates, and can be consid-ered introductory.

Expressed in terms of its constituent neuropil as revealed

by the Golgi chrome-silver, Golgi-Cox, and ancillary techniques, the thalamic nonspecific system consists of agroup of fields stacked along the rostro-caudal axis, andconnected by a dense feltwork of axons of varying lengthsand diverse projections. We shall consider the centre me-dian-parafascicular complex as the common caudal com-ponent, despite rather compelling evidence that the centremedian is a relatively late phylogenetic acquisition and is

virtually absent in rodents. From this complex, axons pourrostrally (Figure 17), fanning out both laterally and medial-ly; the latter elements bridge midline somewhat more




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FIGURE 16 The electrophysiologically determined limits of the nonspecific (reticular) system of the thalamus. AD, an-tero-dorsal nucleus; aHd, dorsal hypothalamic area; AL,ansa lenticularis; AM, antero-medial nucleus; AV, antero-

ventral nucleus; BC1, brachium of the inferior colliculus ;CC, corpus callosum; Cd, caudate nucleus; Cl, claustrum ;CL, central lateral nucleus ; CM, centre median nucleus ; CP,posterior coinmissure; Da, nucleus of Darkschewitsch; En,entopeduncular nucleus; Fil, filiform nucleus; fsc, subcallo-sal fasciculus; FT, thalamic fasciculus; Fx, fornix; GC, cen-tral gray matter; GM, medial geniculate body; HbL, lateralhabenular nucleus; HbM, medial habenular nucleus; Hi,field of Fore1; HL, lateral hypothalamus; Hp, posterior hy-pothalamus; IAM, interanteromedial nucleus; IP, inter-peduncular nucleus; Is, interstitial nucleus; LD, lateraldorsal nucleus; Lim, nucleus limitans; LM, medial

lemniscus ; LME, external medullary lamina; LP, lateral

cleus ; mc, pars magnocellularis ; MD, medial dorsal nucleus;MFB, medial forebrain bundle; NCM, central medial nu-cleus; NCP, posterior commissural nucleus; NR, red nu-cleus; P, posterior nucleus; Pc, paracentral nucleus; Ped,

cerebral peduncle; Prt, praetectum; Pt, parataenial nucleus;Pul, pulvinar ; PVA, anterior periventricular nucleus; PVH,periventricular hypothalamic nucleus; R, reticular nucleus;RE, nucleus reuniens ; S, medullary stria; SG, supragenicularnucleus; Sm, submedian nucleus; SN, substantia nigra ; Spf,subparafascicular nucleus; ST, terminal stria; THP, habenu-lopeduncular tract; TMT, mammillothalamic tract; TO,optic tract; 'FTC, central tegmental tract; VA, ventral an-terior nucleus; VL, ventral lateral nucleus; VM, ventral me-dial nucleus; VPL, ventral posterolateral nucleus; VPM, ventral posteromedial nucleus; ZI, zona incerta. (Figure andcaption from Jasper, Note 100)




FIGURE 17 Horizontal sagittal section through diencepha-lon of 12-day-old mouse, showing certain aspects of rostral-coursing axonal projections from the thalamic nonspecificsystem and the brain stem reticular core. The latter, f. Rt.,runs through the lateral aspect of the intralaminar nuclei,giving off collaterals to, and lying in parallel with, the pro-jection of the thalamic system that here is limited to a small

number of fibers pictured issuing from the centre median-parafascicular, CM-Pf complex, although the amount of centre median tissue present in the rodent is uncertain (seetext). Collateralization of these systems appears to be bothipsilateral and contralateral, extending into specific andnonspecific nuclear masses. Most of these fibers are shown

terminating no farther rostral than the nucleus reticularisthalami (Retic.), although there is some evidence that ele-ments among them may reach striatum and even cortex ( see text). One such fiber is shown at a, while LS. represent asmall group of specific thalamo-cortical elements. Other ab-breviations include: Pt, parataenial nucleus; AV, anterior

ventral nucleus; AM, anterior medial nucleus; IAM, in-

teranteromedial nucleus; PC, paracentral nucleus; CeM,central medial nucleus; CL, central lateral nucleus; IV, in-terventricular nucleus; GL, lateral geniculate; GM, medialgeniculate; Rh., rhinencephalon. (From Scheibel andScheibel, Note 33)

rally in the reuniens and rhomboidalis components of massa intermedia. Rostro-lateral components peel off

rcs, flowing through or around more lateral nuclearses to reach putamen and caudate.lthough it has generally been agreed that no axons of

posterior half of the thalamic nonspecific system reachex, more sensitive tracking methods in the hands of e investigators1136 now suggest that delicate corticalections may, in fact, exist. Golgi methods have notbled us to trace such axons to their destination, al-ugh there seems no question about cortical termina-s for more rostrally situated elements. The Golgi

hods do, however, show the intensive collateralizationhese caudal and rostral components, which provide a

rich substrate for interaction among the various fields of the nonspecific system and with adjacent specific and as-

sociational nuclei. As suggested by Figure 17, the ascend-ing axonal system from the posterior two-thirds of thebrain stem runs roughly parallel to the thalamic nonspe-cific system and provides one of its most important sourcesof afferent excitation. This relationship is shown more clearly in Figure 18,

where a dense collateral mass infiltrates the intralaminarsystem from ascending brain-stem reticular fibers as wellas from the adjacent, much attenuated spino-thalamictract. Individual elements of this influx penetrate not only

the entire ipsilateral intralaminar system, but reach someof the contralateral fields—at least in the rodent (specifical-




y rats and mice). We have not yet been able to identify he entire category of afferents to this system, nor is suchnformation available from degeneration and/or evoked-potential studies. However, we have identified axonal ele-ments from basal ganglia; the fields of Forel; colliculi andpretectum; from adjacent associational nuclei such as lat-ral posterior and pulvinar; hypothalamus; the anterior

nuclear complex; the stria medullaris-habenula-fascicu-us-retroflexus complex; and a massive, fine-fibered con-

ingent from (at least) orbito-frontal cortex. The nature of his afferent array suggests that the thalamic nonspecificields are more sheltered from the onslaught of externally

derived data than is the reticular mosaic of the lower braintem. This presynaptic influx reaches the thalamic fields along

two predominant axes, rostro-caudal and transverse. Themajority of dendritic elements of this system appear to beorganized transversely (see Figure 19); so we must assumethat those conductors with terminal elaborations in therostro-caudal axis either develop less potent synaptic drivealong the dendrites or terminate preferentially on somata.

Although the Golgi evidence is suggestive in this regard,the data cannot yet be considered definitive.

Intensive pentration of adjacent, specific thalamic

fields is a common feature of this system. Figure 20shows a number of such elements entering the neuropil massof the ventral-lateral (VL) nucleus, whose main afferentsupply comes from cerebellum via brachiumconjunctivum. Physiological support of this relationshipis supplied by Purpura, et al., who have found a

FIGURE 18Mass of collateral and terminal fibers from as-

cending reticular components (AR) and spino-thalamic

tract (Sp) terminate in the posterior half of the intralaminar

fields, including parafascicular (Pf); paracentral (Pc); central

lateral (CL); central medial (CeM), and project contralat-

erally via the reuniens nucleus (Re). Other abbreviations in-clude Aq, aqueduct of Sylvius ; Pv, periventricular fibers;and fr, fasciculus retroflexus. Ten-day-old rat. Rapid Golgimodification.




FIGURE 1 9 Axonal and dendritic organization of portionsof the thalamic nonspecific system. Orientation of den-

drite masses of neurons in paracentral (Pc), central lateral ( C1), and anterior medial (Am) appears largely transverse oroblique, thus paralleling contralateral axonal inputs, b, andcollaterals from descending centrifugal fibers, d. Some in-tralaminar axons, like e, seem to remain largely ipsilateral,connecting adjacent nuclei, while others, such as f, projectlaterally into adjacent fields of the ventral nuclear complex

(see figure 20). A number of intralaminar-derived axonssuch as c and d collateralize contralaterally and then project

rostrad toward striatum and/or cortex. Similar patterns arefound in axons from cells of anterior ventral (AV) and ven-tral anterior (VA), which are not included in the intralami-nar complex. The two axons marked a follow trajectoriesof this type. Other abbreviations include Aq, aqueduct of Sylvius ; and fr, fasciculus retroflexus. Twenty-day-oldmouse. Rapid Golgi modification.

modulatory control exerted by intralaminar nuclei

n a background of ongoing, brachium-derived excita-in VLneurons.107

the rodent, massive commissural patterns are formedntralaminar axons. A series of fibro-nuclear massesenable intensive bilateral communication have been

cribed, including the nuclei reuniens, rhomboidalis,interantero-medialis. This allows for a massive systeme-entrant loops of varying lengths' connecting boths of the thalamus, and also facilitates communication of lear fields with both cortical hemispheres. The inten-of such crosscommunication decreases as the phylo-

etic scale is ascended and midline-bridging tissue

shrinks in size and importance. One might wonder wheth-

er this feature of rodent thalamo-cortical anatomy mightnot be substantially implicated in the phenomena of corti-cal equipotentiality described by Lashley 108 in rats (Chow,this volume). In a similar vein, with the progressive de-crease of commissural mass to the point at which 30 percent of the human thalami may be totally devoid of massaintermedia bridging,'" there may reside substrate for therise of laterality in primate and man.

It appears highly likely that a cortically directed projec-tion arises from the anterior third of thalamic nonspecificfields. In Figure 21, part of this system can be seen leaving

the critical antero-medial angle of the field. Such axons




may project rostrally, unilaterally, or bilaterally, and asthey emerge from this pool, send rich collateral masses in-to adjacent nuclei such as ventral-anterior and nucleusreticularis thalami.110,111

The latter is of special interest to us. It continues as a nu-clear plate or shell surrounding anterior, superior, and in-ferior surfaces of the thalamus, and all thalamo-corticalprojections and the greater part of the cortico-thalamic re-flux must penetrate through it. It is, accordingly, in a criti-cal position to monitor and modulate most thalamo-cor-tico-thalamic interactions. Several investigators111,112 have infact, likened it to the screen grid in a vacuum tube. OurGolgi studies indicate that the dendritic ensemble of thisfield is densely intertwined and covered with long, hair-like spines, forming a net or sievelike structure throughwhich most axons of these thalamo-cortico-thalamic sys-tems perforate, either directly or with production of col-

laterals.111 Opportunities for intensive axodendritic interactions arc obvious (Figure 22).

The axonal projection of the nucleus reticularis thalamiis clearly of great physiological importance. Cajal reportedthat these axons seemed to run caudally,' but a long seriesof retrograde degeneration studies following massive, selective, cortical ablation appeared to favor a cortical ter-mination.113,114 As a result of evoked-potential studies, it

was asserted by some investigators that the nucleus reticu-laris thalami actually constituted the final common path-

way along an intralaminar polysynaptic chain to cortex.2

The importance of such data was somewhat weakenedby the inability of the stimulating electrode to differen-tiate between nucleus reticularis cells and fibers of passage.Recent Golgi studies have shown clearly that at least 95 percent of the axons of nucleus reticularis thalami cells are, infact, distributed caudally to thalamus and mesencephalic

FIGURE 20 Vignette taken from a horizontal sagittal sec-tion through the thalamus of a 7-day-old rat showing someinterrelations between thalamic nonspecific system fibers andthe ventral lateral and ventral anterior fields. Cells and fibersof the thalamic nonspecific system (Thal. Retic.)culminating in the rostral-running projection ornonspecific radiation (nsr) send terminals and collaterals intothe neuropil fields of ventral lateral (VL) and ventral anterior (

VA) nuclei, whose primary afferent sources are the

(drt) and pallido-thalamic (pt) bundles respectively. Also visible are sectors a, b, c, and d, of VA, the nucleus reticu-laris thalami (nR) more anteriorly, and the ventrobasal com-plex (VB) more posteriorly, receiving the terminating me-dial lemniscus (lem). One centrifugal fiber (ct) is seen ending in VB, while the ascending reticular system (ars) sends col-laterals toward the VA field. Rapid Golgi modification. ( From Scheibel and Scheibel, Note 110)




FIGURE 21 Horizontal section through the anterior end of the thalamus showing the area of origination of the thalamicnonspecific projection upon cortex. Collaterals and termi-nals from the ipsilateral nonspecific radiation, nsr (ips), andsome elements from the contralateral system, nsr (con) fillthe medial portion—sector a of VA. This region is alsoreached by individual elements of the pallido-thalamic bun-dle (pt), which arborizes maximally in sector c, while shortercollaterals from the ascending reticular system (ars) termi-nate in sector d. One rostrally-directed axon (vb1 ) from a

ventrobasal cell (VB) is seen, as are 3 heavy caliber and 2fine cortico-thalamic fibers (et 1-5), the first two of whichterminate in VA. Other abbreviations including those in theinset diagram include: 1, parataenial ; 2, anterior ventral,AV; 3, anterior medial, AM; 4, interantero-medial, IAM;

5, paracentral, PC; 6, central lateral nucleus, CL; 7, centremedian-parafascicular complex; 8, interventricular ; C Str,corpus striatum; Rh, Rhinencephalon. Three-day-old kit-ten. Rapid Golgi modification. (From Scheibel and Scheibel,Note 110)

mentum (Figure 23), thereby providing a hierarchy of entrant circuits." Such feedback loops appear to play neurons of both specific and nonspecific thalamic sys-

ms and may serve as substrate for recruitment poten-s.18,19 They may also provide circuitry essential to theernating excitatory postsynaptic potential (EPSP) andhibitory postsynaptic potential (IPSP) swings describedspecific thalamic cells secondary to afferent barrage."

IALAMO-CORTICAL PROJECTION The projection of lamic nonspecific systems upon cortex poses a problemt requires further investigation. Investigators do noty agree on how recruitment potentials are distributeder cortex following intralaminar stimulation," ,2° al-

though there is a consensus that the distribution trans-cends that produced by stimulation of specific thalamicnuclei. Our own investigation of this projection is still in-

complete, but the data are suggestive. In rats and mice, theaxonal outflow from the anterior third of the intralaminarfields appears to project rostrally and ventrally via the in-ferior thalamic radiation, just lateral to the mass of theseptal nuclei. The fibers can be followed forward to ap-parent simple ascending (axodendrite?) cortical termina-tions in orbito-frontal cortex. Each fiber may subdivideinto many branches while still in the subgriseal white mat-ter, and the most caudal branches may reach almost to thefrontal motor fields.

Such data appear to complement the findings of Velasco




and Lindsley,116 who observed that orbito-frontal ablationn the cat effectively blocks recruitment phenomena overhe remainder of cortex, thereby identifying orbito-fron-al fields as primary cortical distribution stations for as-

cending intralaminar control. On the other hand, Purpurahas removed large blocks of frontal cortex and underlying ubcortical tissue without disturbing recruitment phenom-

ena117 If further structural and functional studies should

bear out the importance of the orbito-frontal field as a dis-ribution center, it would be logical to suppose that thefurther backward spread of recruitment waves over cortexwould depend on a complex series of cortical chains of varying lengths.

Conclusions

Disparate but converging bodies of evidence now enableus to define certain characteristics of the reticular core of the brain. It is an archaic, centrally located mosaic of sub-centers almost completely shielded from direct contact with the self—world interface, yet continuously apprisedof all transactions crossing that interface. Its outputs, con-tinuously variable along an intensity continuum, do not

reflect stimulus mode so much as stimulus quantity. This out-put is projected simultaneously upon downstream effectorcenters, upon rostral mechanisms devoted to differen-tiation and comparation of information, upon primary

FIGURE 22 Portion of the anterior ventral sector of the nu-cleus reticularis thalami in 12-day cat as seen in sagittal sec-tion. The dense matting of the dendrite mass is seen paritcu-larly along the inner border of the nucleus, nR; a, initialintranuclear path of an axon with its primary collateral sys-tem limited to the n. reticularis; al, its caudal path; a2,penetrating the ventral anterior nucleus, VA; and a typicalbushy terminal dendrite structure, a3. Fibers b and c, arecentrifugal and centripetal elements, respectively, pene-

trating the nucleus and emitting collaterals b' and el en

passage. The entire observed course of a fiber of unknownDrigin, d, lies within the nucleus. Two cells, e and f, of the ventral anterior nucleus, show dendritic configuration typi-:al of this field. Axon g is emitted from a n. reticularis cell

hose soma remains unstained. Cell h of the n. reticularisemits dendrite h', projects into more rostral white mattercerebral peduncle), and loses its filamentous spines as itdoes ;o. Other abbreviations include VB, ventrobasalcomplex; Col. s.; superior colliculus ; Teg., Tegmentum;

Caud., caudlate. (From Scheibel and Scheibel, Note 111)




Teg. Mes.

FIGURE 2 3 Slightly schematized horizontal sagittal sectionthrough the thalamus of the mouse, showing some thalamicafferent and efferent constituents on the right, and the courseof two nucleus reticularis thalami axons on the left,elements h and i and two n. reticularis neurons. At h4 and h5

the axon of h collateralizes within n. reticularis, while h1,2,3

represent collaterals generated along the length of the axon

dal trajectory and projecting into specific and nonspecificthalamic fields. Similarly, in the case of neuron i, structuresmarked i2,3,4 represent collaterals infiltrating the thalamic

ventral and lateral nuclear masses while it represents a shortcollateral projecting rostrad into the striatum (Str). All otherabbreviations as in previous figures. (From Scheibel andScheibel, Note 111)

d secondary fields that relay raw information rostrally,d upon the remainder of the reticular core itself. Its vol-

me is small in comparison with cortex and cerebellum,d economy probably demands repeated use of its rela-ely limited amount of modular logic.62

It seems likely that stimulus patterns continuously re-culate through the millions of re-entrant loops as de-onal modes are reached. At the same time, competitionthe interest of the reticular arrays must be high, and

ural supremacy is gained for that moment in time only

by those data that are most "exotic"—or most compelling biologically. Like some stern, harried father figure, thecore has limited patience and limited time-binding re-sources. Its logic is wide but superficial, and its decisionary apparatus does not permit the luxury of hesitation.

Summary

Modern structural and operational concepts of the reticu-lar core of the brain stem have emerged over the past 60




ears, although a number of current ideas were already mplicit in studies published at the turn of the century. Theomplex may be thought of as a mosaic of subcentersaced athwart all input and output systems of the neu-xis, receiving a constant sampling of information from

ctivity ongoing in these systems. This mass of heterogene-us, convergent data is integrated along the postsynaptic

membrane of individual reticular neurons whose output

presents an algebraic summation of these inputs. Theutput of these reticular-core elements, representing in-nsity rather than mode, is then projected rostrally and

audally to modulate the degree of synaptic drive on neu-

rons spread widely throughout cortex, brain stem, spinalcord and, in some cases, as far peripherally as the first-order sensory cell.

An impressive group of physiological mechanisms arcsubserved by this structural substrate and include gating of sensory inputs; modulation of transmission along majorrostral-coursing and caudal-coursing tracts; modulationand control of spinal effector mechanisms; multileveled

control over most visceral functions; and the active manip-ulation of a spectrum of states of consciousness from deepcoma through a series of sleeping states to maximal vigi-lance.

Subcortical and Cortical Mechanisms

in Arousal and Emotional Behavior

ALBERTO ZANCHETTI

HE DIFFERENT EMPHASIS that has been placed at differentmes upon neural activity at either the cortical or the sub-

ortical level can be well exemplified by the history of re-ent theories of emotion. Psychological thinking on thisubject was dominated at the end of the last century andhroughout the first three decades of the present one by he so-called James-Lange theory.1,2 The neural basis forhis theory is schematized in the drawing of Figure 1 (left),ken from a paper by Cannon.3 As Cannon says, "accord-g to the Jarries-Lange theory an object stimulates one or

more receptors (R, in Figure 1), afferent impulses pass tohe cortex (path 1) and the object is perceived; thereuponurrents run down to muscles and viscera (path 2) and al-

r them in complex ways; afferent impulses course back o the cortex (paths 3 and 4), and when there perceivedansform the 'object-simply-apprehended' to the 'object-motionally-felt' ; 'the feeling of the bodily changes ashey occur is the emotion—the common sensational, asso-ational and motor elements explain all,' to quote James'sxpression." Obviously, then, in the James-Lange theory

L B E R T O Z A N C H E T T I Istituto di Patologia Medica, Univer-

ty di Milano, and Gruppo Nazionale di Medicina Sperimentaleel Consiglio Nazionale delle Ricerche, Milano, Italy

the cerebral cortex plays a predominant role in emotion,first in simply apprehending the object, then in feeling it

emotionally. If we want to state this somewhat differently,the cerebral cortex enjoys predominant attention in theames-Lange theory because it refers exclusively to emo-

tional feeling.Cannon3,4 strongly objected to James's and Lange's

opinions and formulated the so-called thalamic theory of emotion. The neural basis for this theory was schematizedby Cannon3 himself in the drawing reproduced in Figure1 (right), and has been conveniently summarized by Lindsley5 as follows: "An external emotion-provoking stimulus excites receptors (R) and starts impulses toward

the thalamus (path 1). . . . Thus efferent discharges are setup in path 2, either through direct activation of the thala-mus over path 1 or after impulses have passed to cortex ( path 1'), where they inactivate inhibition over path 3,

which allows patterned motor responses in the diencepha-lon to find expression in effectors via.path 2. At the sametime an upward discharge in path 4 carries to the cortexan appreciation of the pattern just released. . . . The differ-ence between this view and that of James and Lange is thatfor Cannon 'the peculiar quality of the emotion is addedto simple sensation when the thalamic processes areroused.'




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NOTES 895



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1967 - Scheibel - Anatomical Basis of Attention Mechanisms in Vertebrate Brains

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