The general organization of somatotopic projections to SII cerebral neocortex in the cat

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T H E G E N E R A L O R G A N I Z A T I O N OF SOMATOTOPIC PROJECTIONS TO SII C E R E B R A L N E O C O R T E X IN T H E CAT*

JOHN R. HAIGHT** Laboratory of Comparative Neurology in the Departments of Biophysics, Psychology and Zoology, Michigan State University, East Lansing, Mich. 48823 (U.S.A.}

(Accepted March 27th, 1972)

INTRODUCTION The receptotopic organization of the somesthetic receiving areas of the mammalian neocortex has been affirmed and reaffirmed many times in the last 3 decades. The primary, or SI area, has received especial attentionl,3,e,16,~°,24,zs,z7,~s,42,43, 4s,54,Ss,59, 61,67-70.**. These studies show that a distorted projection of the animal's body can be mapped onto the cortical sheet (Fig. 1). The accuracy, or even the desirability, of presenting these projected figurines is not at issue here. The concept is introduced only to indicate the universality of agreement with respect to the orientation of the body representation on the cortical surface. In all mammals projections from the posterior quarters of the body are found lying medially, often partially within the median sagittal fissure. More cephalic structures are represented in an increasingly lateral position on the surface of the parietal cortex. Representations of the limbs and their apices are situated rostrally, with those from the body axis forming the posterior limit of the primary SI receiving area. This arrangement applies to the representation of the body on both lissencephalic and gyrencephalic brains. With the discovery of the somatotopic organization of the primary somesthetic cortex came the discovery of another, secondary, somesthetic area2,65, Bn. The small size and often cryptic location of this second area, or SII as it came to be known eg, made detailing of its exact somatotopic organization difficult with the methods then available. Moving rostrocaudally across the SII field, one encountered responses from the head region, the forelimb and the hindlimb, in that order. Finer detailing, which would have permitted a description of the specific orientation of the limbs, was not possible at that time. Figurines purporting to represent the organization of peripheral receptive fields * Portions of this paper were delivered at the meetings of the American Association of Anatomists, Philadelphia, Pa., April, 1971. ** Present address: Anatomy Department, The University of Tasmania, Hobart, Tasmania 7001, Australia. *** References are cited with representative, not comprehensive intent. Brain Research, 44 (1972) 483-502

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Fig. 1. Organization of SI neocortex in two placental mammals. A, Rat (after Woolsey and Van der LOOS71).]], Cat (after Woolsey6S).The presence or absence of gyri do not appreciably affect the general orientation of the body parts in SI neocortex. SI and SII are also seen to stand in the same relation to one another in both the lissencephalic and gyrencephalic brain.

in SII were published prior to 196143,67,68.**, but the first study specifically concerned with mapping SII did not appear until that year 7. In all cases the figurines are shown with their limb apices pointing medially and with the body axis occupying the lateral extremity of SII. This configuration has persisted in the literature 26,27,71 and in textbooks to the present day11,34, 8s,56,57. **. Recent work in the present laboratory 14 has led to a questioning of this picture of SII organization, at least in the cat. It has been observed, on the basis of detailed microelectrode mapping studies, that a reversal of the SII figurine is required with the result that the limb apices face laterally with more axial structures occupying the medial wall of the anterior ectosylvian or SII gyrus. As this finding is in conflict with the current picture of SII organization, it was thought desirable to examine the somatotopic relationships in cat SII in much greater detail than had been done heretofore. MATERIAL AND METHODS

Subjects Fifteen cats of both sexes were used in the study. All but one of these had been raised in this laboratory. The procedures to be described were carried out on 14

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animals between the ages of 6 and 9 months. The one subject of unknown age was an adult female of at least two years. Preparation

General anesthesia was induced in 12 animals by intraperitoneal injections of sodium pentobarbital (initial dosage, 32 mg/kg, potentiated by acetylpromazine injection 10 min prior to the anesthetic). Three subjects were anesthetized with 3.03.5 ~o halothane carried in 70 ~o nitrous oxide and 30~ oxygen. These subjects were paralyzed with either succinyl choline or gallamine triethiodide and artificially respired. All subjects were tracheally cannulated and their rectal temperatures were maintained between 35 and 37 °C. Exposure of the anterior ectosylvian gyrus was accomplished with the head fixed in position at an approximate 45° angle from the median sagittal plane. This procedure placed the recording site at a convenient working angle and made it easier to dam the exposure with an acrylic rim so that the exposed cortex could be covered with warm mineral oil. Finally, the exposed cortex was photographed and an 8 in. × 10 in. print made so that the electrode entry positions could be permanently noted. Recording sessions

Glass insulated, tungsten microelectrodes5 with exposed conical tips having base diameters of 40/.tm and altitudes of from 20 to 30 ~m were used to record from single cortical units and occasional clusters of units. Signals were initially amplified with a Tektronix 122 preamplifier which led to a Tektronix 502A oscilloscope for visual display and a Grass model AM-5 audio monitor. The signals were recorded on magnetic tape using a Magnecord 1028 recorder. With the 3 gas anesthetized subjects, halothane was discontinued approximately 1 h before recording was to begin. Wound areas were then kept perfused with a local anesthetic (Xylocaine). Anesthesia was maintained with a mixture of 70-80 ~ nitrous oxide and 30-20 ~o oxygen. Periodically, the paralytic agent was momentarily discontinued to determine whether the animal was struggling. Data collection

Electrode penetrations were more closely spaced than had been usual in past mapping experiments. Initial experiments were conducted with successive electrode punctures spaced at 0.5 mm within rows which were, in turn, spaced either 0.5 or 1.0 mm apart. Later experiments were conducted with punctures 0.2--0.5 mm apart. These puncture patterns were maintained at all times except where surface blood vessels lay in the path of the proposed puncture. In order to maximize the possibility of determining the somatotopic interrelations of cortical neurons the electrode entry angle was varied from experiment to experiment, though never during the course of a single experiment. Furthermore, the orientations of the electrode puncture rows were varied Brain Research, 44 (1972) 483-502

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with respect to the axis of the anterior ectosylvian gyrus (AEG) such that the gyrus was 'criss-crossed' in all directions ranging from parallel to the gyral length to perpendicular to it. 'Dimpling' of the cortical surface during penetration was avoided by using finely tapered electrodes. In addition the electrodes were not driven too deeply into the cortical mantl6. This prevented destruction of surface tissues by the ever widening electrode shaft during its descent. When mapping sulcal walls, however, it was necessary to drive the electrode deeper into tissue than when mapping the exposed portions of the gyrus. Inasmuch as this was possible, a given puncture row spanned the entire SII field. That is to say, the boundary punctures either provided no data or, in the case of the anterior SII boundary, yielded only SI face data. As the electrode was advanced into the cortex, the animal's body was stroked until a single unit response was located at its maximum amplitude. Unit clusters were not generally accepted unless data from that particular body area happened to be particularly scarce. Careful record was kept of the micrometer Vernier position of the micromanipulator for each response. The receptive field of the responding unit was accurately determined by applying light tactile stimuli such as puffs of air, drawing of fine wires across skin surfaces and lightly touching the body hairs. Vigorous or nociceptive stimuli were not employed. The extent of the receptive fields was copied onto a photograph of the appropriate body region. Anatomical reconstructions

At the end of each experiment the subject was given an additional 3-5.5 ml dose of sodium pentobarbital and perfused intracardially with 0.9 ~ saline solution followed by 10~ formol-saline. The head was removed and stored in formol-saline for at least one week after which the brain was removed, photographed and a block of neocortex containing the electrode tracks was embedded in celloidin. Serial sections, in the plane of the puncture rows, were then cut at 30 #m and alternate series were stained for cell bodies (thionin) and myelinated fibers (Weil and Sanides-Heidenhain techniques). Each electrode puncture was then identified using the data logged during the recording sessions and the cortical photograph with the entry positions marked upon it. The position of each recording locus was approximated within each puncture on the basis of the micromanipulator readings. As the puncture rows ran in virtually all directions across and along the gyrus, a well-interlocked picture of the relationships of all body regions as they were projected onto the SII field resulted. Using these maps it was possible to start at a given point within SII and follow the somatotopic organization in any direction from a given unit's response. RESULTS

The experimental sample

The second somatic sensory or SII region of the anterior ectosylvian gyrus (AEG) was penetrated a total of 421 times in the 15 subjects. These penetrations Brain Research, 44 (1972) 483-502

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Fig. 2. Localization of response types in the anterior ectosylvian gyrus (AEG) of the cat. (For orientation refer to Fig. lB.) Within the area circumscribed by the dashed line are found units with somatotopically organized receptive fields. Each unit found within this area was activated by a specific tactile stimulus whose modality and threshold remained constant over time. The tactile stimuli required for activation were not nociceptive, nor were mixed responses such as auditory-tactile found in this region. Thus, units in this area of AEG displayed properties which closely resemble those of units in the thalamic ventrobasal nuclei (Vb). The indicated overlap of this area onto the anterior suprasylvian gyrus is not real, but rather, represents the extension of SII into the suprasylvian sulcus (Ss). SII unit responses were not observed in the fundus or on the medial bank of Ss. The remainder of AEG exhibits unit activity which differs appreciably from that within the Vb region. Units drivable from the periphery were rare. When found these units displayed inconstant stimulus thresholds and changing stimulus modalities as well as irregularly defined and non-somatotopically organized receptive fields. These units had properties very similar to those described for units in the posterior group of thalamic nuclei (Po). A, B and C represent the 3 zones of AEG described by Carreras and Andersson8. Units in zone C displayed mostly 'Vb' properties; zone A units, mostly 'Po' properties; and zone B was intermediate. AE, anterior ectosylvian sulcus; Cor, coronal sulcus; Ss, suprasylvian sulcus. yielded a population o f 435 resolvable single 'cortical' units o f which 15 were later f o u n d to have been located in the underlying white matter. O f the remaining units, 413 were, by virtue o f their receptive field properties and position in the cortical tissue as determined by eventual reconstructions o f the electrode penetrations, demonstrably within the somatotopically organized, mechanoreceptive projection area o f SII. The remaining 7 were located in A E G but were ultimately determined to lie outside the somatotopically organized region o f SII (Fig. 2).

Anesthetic effects The 3 subjects that were lightly anesthetized with nitrous oxide provided a sample o f 33 ' V b ' type units. Characteristically, these subjects displayed a m u c h greater level o f continuous b a c k g r o u n d neural activity than did those anesthetized with sodium pentobarbital. This had the effect o f making single cortical units somewhat m o r e difficult to isolate. Once isolated, however, these units exhibited properties that were, for the purposes o f this study, indistinguishable f r o m the pentobarbital anesthetized subjects. Specifically, for b o t h anesthetic states: (1) there was a consistent response to slow, repetitive mechanical stimulation o f the units' receptive fields; (2) the delineated receptive field boundaries remained constant over time and did n o t migrate a b o u t on the b o d y surface; and (3) gross changes in stimulus threshold or

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response did not occur over time. As a result of these findings, it was felt that the anesthetic state of the animal had little effect in the 'Vb' portion of SI[. Tactile stimulation

Classified on the basis of their tactile response properties, two types of units were found which occupied non-overlapping areas of AEG (Fig. 2). (1) Cortical units within the somatotopically organized portion of SII responded primarily to light, mechanical stimulation of the body surfaces. Thus, very light stroking of the body hairs, mild pressure applied to the skin surfaces or movement of a fine wire or severed cat vibrissa across a glabrous skin area without visible indentation proved to be the best stimuli for activating these cortical units under both anesthetic states. Strong pressure, thumping, pinching and even harsher stimuli were no more effective in eliciting responses than were the milder stimuli. No units were observed to respond to joint movements or, unambiguously, to kneading of the underlying fascia. Over 94 ~ of the units examined responded solely to stimulation of the hair and skin. The remaining 6 ~ might have qualified as 'deep' responses except that their receptive fields, when occurring in areas where the skin was loosely attached to the deeper structures, did not remain fixed with respect to these deeper fascia, but rather, moved with the skin. A final point about units in the somatotopicaUy organized portion of AEG concerns their frequency of occurrence. Punctures that yielded no data were very rare in this region. On the average, two unit responses were found per electrode puncture. (2) Seven mechanoreceptive units were found in AEG that responded to imprecisely defined stimuli, exhibited migrating receptive field boundaries, or did not fit well into the general somatotopic organization as did units in the rest of SII. Later it was found that these units did not lie within the somatotopically organized portion of AEG but lay either posterior or lateral to that region (Fig. 2). Almost 50 electrode punctures entered this region of SII to provide the 7 observed responses. Excitatory tactile responses in this area were quite rare. Tissue injury effects

On occasion mechanoreceptive units within the somatotopically organized portions of SII would demonstrate shifting stimulus thresholds and migrating receptive field boundaries. Such units, if held for more than a few minutes, would usually stop responding altogether. Succeeding punctures, if nearby, were apt to be similarly labile or totally inactive. It gradually became apparent that this phenomenon was due to cortical damage, caused by blunt or bent electrode tips. A visible dimpling of the cortical surface upon penetration was a virtual guarantee that cortical spreading depressional,37 was in the offing. Spotty, ill-defined receptive fields would result, followed by silence (even in subjects anesthetized with nitrous oxide). Recovery from the depression was slow (0.5-1 h or more) and seldom permanent. As indicated in Materials and Methods, another cause of cortical damage was closely spaced, deep Brain Research, 44 (1972) 483-502

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cortical penetrations. If the electrode was driven in more than 3 or 4 mm, the next puncture in the row often exhibited erratic activity. When suitable precautions against tissue insult were taken, the behavior of SII neurons in the somatotopically organized region remained consistent over time with no threshold or receptive field boundary shifts. Unit activity having characteristics of the posterior group of thalamic nuclei44 was not observed in this region. Receptive fieM properties of SII neurons As had been reported in SI neocortex in the cat 54, raccoon 81, squirrel monkey6 and rhesus monkey SI164, there was a gradient of increasing receptive field size from distal to axial body areas. The smaller receptive fields were found on the apical limb regions with the larger fields occupying the trunk and upper limb areas. In the region of the head the smallest receptive fields were located peri-orally, especially in association with the lips and mystacial vibrissae. Larger fields were found more caudally on the head. Only 12 of the 403 units in the somatotopically organized area had excitatory receptive fields that were not strictly contralateral. Eleven of these were symmetrically bilateral across the body axis and one was strictly ipsilateral. Most of the bilateral receptive fields encompassed the limb girdle regions and were joined across the midline. Two units had bilateral fields which involved only the forearm regions. These were symmetric, but disjunct, across the midline. Several of the 7 mechanoreceptive units which lay outside the somatotopically organized portion of SII exhibited bilateral receptive fields comprising, say, all 4 paws. Often the receptive fields of these units were not bilaterally symmetric but would involve, for example, 3 of the 4 limbs. Other physiological properties (see Tactile stimulation section) further distinguished them from the somatotopieally organized unit population. Though single unit activity was not often activated by bilateral stimulation of the body surface, slow wave activity was. For most units examined a bilaterally evocable slow wave was associated with the strictly contralateral unit activity. Most of the strictly contralaterally driven SII units had receptive fields that were not disjunct, that is to say, the receptive fields of such units were not separated by nonresponsive areas. An important exception to this rule was found in the hand and foot representations. Stimulation of several of the glabrous finger or toe pads often activated a single cortical unit, these pads being separated by nonresponsive hairy regions of the fingers and hand or of the toes and foot. In one case at least two pads had to be stimulated simultaneously in order to activate the terminal cortical neuron. This was not usual, stimulation anywhere in the receptive field generally being sufficient for activation. It should be noted that SI neurons, on the other hand, seldom exhibit these apical limb receptive field discontinuities~4. Yet another variety of receptive field, comprising approximately 10~ of the sample, was the 'stocking-like' type. Such receptive fields were large, often involving an entire limb or, at other times, only the lower or upper limb. A few very large receptive fields formed bilateral 'body stockings'. Such fields generally fit in with the Brain Research, 44 (1972) 483-502

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receptive field organization of the smaller, 'non-stocking-like' variety. The cortical neurons subserving these fields did not demonstrate anything out of the ordinary in terms of tactile activation requirements, boundary stability or the like. Their habituation properties, however, deserve comment. Often, delivery of a repetitive tactile stimulus to the same point in such a receptive field would result in a very rapid loss of following ability on the part of the unit. If, however, the stimuli were delivered rapidly to different areas of the receptive field, the ability of the unit to follow remained unimpaired. Nonetheless, the receptive field boundaries of these units remained constant although repeated stimuli delivered at the edge of the field might lead one into thinking that the field was ill-defined.

Somatotopic organization of meehanoreceptive projections to SII The organization of receptive field in SII followed, for the most part, a reasonably orderly somatotopy, similar to that reported in cat S154, as well as in a variety of other animals (Introduction). Axial body areas lay medially along the upper bank of AEG, but mechanoreceptive projections to SII did not seem to extend all the way to the fundus of the anterior suprasylvian sulcus. The head representation faced rostrally with the ophthalmic and maxillary areas directed medially and the mandibular, laterally. The SII head region merged into the SI head representation as AEG opened into the coronal gyrus. Postcranially, it was found that the distal limb areas lay laterally on AEG and were pointed in a somewhat anterior direction. The hand and digit representations were almost surrounded by the preaxial and postaxial forearm projections (Fig. 3). Thus, the arm was partially represented as lateral to the digits and hand. It is probably this feature of the map which has been responsible for the confusion about the orientation of the body in SII. The split forearm projections curled around the hand and finger area and connected with the medially located upper arm region (Fig. 3). The leg regions appeared to be organized in a fashion similar to the arm though the area given to their representation was much smaller. Axial structures did not form a large portion of the SII map though all body regions were eventually located except the belly. Somatotopically organized projections were not found in the lateral wall of AEG and, in fact, seldom extended much beyond the medial convexity of the gyrus. Auditory responses were not observed in the area of SII occupied by somatotopically organized projections. The rules of somatotopy appeared to break down in the projection area devoted to the digits of the hand. The 3 mesial digits, numbers 2, 3 and 4, were generally to be found in the center region of the digit projection field (Fig. 3) with projections from digits 1 and 5 occupying a lateral lying crescent connecting the hand and mesial digit projections. This crescent also formed the extreme anterolateral boundary of the somatotopically organized portion of SII (Fig. 2). Within their respective areas, projections from the digits appeared in seeming random order. One puncture row would disclose receptive fields from digits 2-3-4, in that order, while another neighboring row might show a complete reversal of the sequence, i.e., 4-3-2. Even within a single puncture row a digit receptive field sequence might be seen to progress in good serial

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"4"L, J / Fig. 3. Organization of receptive fields in SII neocortex and at the periphery. Left, data are presented from one subject (70307) which almost completely mapped the postcranial SII field. The coronal rows of dots represent electrode puncture sites on AEG. All punctures which yielded data from the trunk or body are enclosed within a solid line. Similarly, the arm, hand, hand digits, leg, foot and head are enclosed resulting in a crude representation of the cat's body upon the cortical surface. The anterior portion of the map was not completed in this experiment, hence, the head, arm and hand maps are not quite complete. Nonetheless, the general organization of the body is clear. The axial body was found lying medially in the lateral wall of the suprasylvian sulcus with the limbs directed laterally toward the anterior ectosylvian sulcus. Noteworthy was the fact that the forearm representation enveloped, to a large extent, the digit and hand representation. Postaxial forearm projections extended around the posterior aspect of the hand representation to the lateralmost extremity of the mechanoreceptive, somatotopically organized portion of SII. Preaxial forearm projections (not completely shown) extended over the anteromedial quadrant of the hand representation leaving the anterolateral quadrant free of all but digit projections. Leg and foot projections were not present in as great detail, nor was the area devoted to their projections as large as that of the arm and hand though there were indications of a pre- and postaxial division. The specific organization of the arm-hand-digit projection is also of interest. The digits did not project to their area in sequential order. The mesial digits (2, 3 and 4) tended to occupy the central region of the projection while the external digits (1 and 5) were found occupying a crescent (dotted line) extending around the lateral periphery of the hand projection area. Digits 1 and 5 appeared to share the same projection area in spite of their actual physical separation on the body. Right, the organization of the hand and digit projections is clarified by examining the progression of receptive fields on the hand itself as disclosed from the cortical puncture rows. The sequence of receptive fields from the first (A) and the second (B) puncture rows in the lefthand illustration is shown projected back onto figurines of the dorsal right hand. The receptive fields are shown (fine lines) connected by a heavy line through their centers. This line then relates the direction taken by the puncture rows (arrows) with the path or trajectory 68 taken by the peripheral receptive fields disclosed within that row. Puncture row A disclosed a series of receptive fields which began at the median dorsal aspect of the wrist and extended distally to the apex of the 4th digit. Curling under digit 4, the progression proceeded across the ventral aspect (dotted lines) of digits 4, 3 and 2 at which point the sequence returned to the dorsoradial side of the hand. The trajectory of puncture row B, which lay 1.0 mm posterior to A, was shifted in a radioventral direction around the hand. The trajectory began at a more radial position on the wrist than did that of A. It traversed the dorsal hand, curled under digits 3 and 2, returned to the radial edge of the 1st and 2nd digits and finally turned under the hand to ascend up the ventral wrist and arm. Note that in each case the ascending path is shifted counterclockwise with respect to the descending path and that successively posterior puncture rows are similarly shifted. For sulcus abbreviations see Fig. 2.

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order, and then suddenly reverse. The result o f this was that one often was faced with projections from the same general area, say digit 4, occupying opposite poles o f the digit projection field. It was apparent that the ordering o f receptive field projections from the hand and its digits onto the SII cortical field did not correspond with the topographical a n a t o m y o f the hand. I f the problem is considered within the topological framework proposed by Werner 62 and his co-workers63,64, the disorderliness o f the SII hand projection is clarified. Developmentally, the tetrapod a r m and leg do not arise as terminal excrescences, but rather, are topologically continuous bulges in the segmentally organized axial body. Thus the tendency is for projections from the rostral or preaxial half o f the arm and hand to enter the spinal cord anterior to projections from the posterior or postaxial half19,47, ag, which ordering is preserved in the cortical representation also ~3,~4. Mixing o f cutaneous afferent nerve fibers in the brachial plexus results in

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Fig. 4. Receptive field sequences disclosed by a puncture row directed nearly perpendicular to the axis of the SII cortical arm and hand projection (subject 71323, nitrous oxide anesthesia). Inset, location and spacing of the puncture row in AEG. Note the 0.2 mm puncture spacing as opposed to the 0.5-4.0 mm spacing employed in the example shown in Fig. 3. The arrow points posterior. A, The receptive fields defined at the recording loci delineated 1 through 10 in the inset. Though the electrode punctures were directed in successive steps from anterior to posterior, it can be seen that the equivalently numbered receptive fields do not follow a flowing sequence. Rather, they appear to fall into 3 rows directed distoproximally as shown in B..This portion of the cortical puncture row crossed 3 trajectories as shown in Fig. 3. Note that, as in Fig. 3, the successively posterior cortical trajectories project from increasingly ulnar or postaxial structures of the hand. For sulcus abbreviations refer to Fig. 2. Brain Research, 44 (1972) 483-502

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considerable amounts of dermatomal overlap at the level of input to the neuraxis, especially in the area of the hand. As a result, projections from a given area of the hand will often enter the cord at up to 3 levels47,4L This somewhat irregular but essentially segmental mode of entry into the central neuraxis is mirrored in the representation of projections in the somesthetic cortices 82. In consequence, if the cortical representation of a succession of peripheral receptive fields from the lateral body, extending from head to tail, is considered, their sequence will be seen to progress from the neck, distally down the preaxial side of the arm, glide over the hand and digits, ascend up the postaxial arm and, finally, rejoin the trunk. The process is repeated for the leg (see ref. 64, Fig. 7). Regarded in this manner, the a:m and hand projections to cat SII were seen to take the form of dermatomal strips oriented near the transverse plane. Preaxial projections tended to occupy the anterior half of the arm and hand region while postaxial projections were usually located posteriorly and posterolaterally. In the digit area, dermatomal overlap muddied this organization resulting in the apparent random scatter of individual digit projections in that portion of the map. However, electrode puncture rows, if directed in a direction roughly parallel to the proximodistal axis of the arm projection, disclosed continuous receptive field sequences over most of the extent of the puncture row (Fig. 3). Commencing proximally on the arm, the sequence of receptive fields was observed to progress distally down the arm, cross the hand and its digits and ultimately return up the arm in a more 'postaxial' position than had been the case for the descent (Fig. 3, right). Puncture rows directed off the axis of the arm representation did not disclose receptive field sequences that could be interpreted as continuously flowing. Well ordered progressions of receptive fields were apt to be short and were often strikingly

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Fig. 5. A generalized SII figurine constructed from a cat which had a pronounced bifurcation at the anterior pole of its suprasylvian sulcus. The sulcus was very deep with the result that very little data were obtained from the exposed surface of AEG, only the head and distal aspect of the hand areas being accessible at the surface (cf. Fig. 3). For sulcus abbreviations refer to Fig. 2. Brain Research, 44 (1972) 483-502

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discontinuous. The observed receptive field sequences would follow a flowing sequence for a few punctures and then jump to a different area of the hand or perhaps return to the starting point and retrace the same sequence (Fig. 4). This feature was not observed when the puncture rows were directed close to the axial direction of the cortical limb projections. A generalized SII figurine is presented in Fig. 5. The reader should realize that such portrayals are strictly for orientation and do not pretend to literal accuracy. Variations in sulcus patterns among individual animals can be responsible for considerable divergence from the scheme presented here. This is made clear if one compares the gyral configurations of Figs. 2, 3 and 5, all of which are taken from cats used in this study. The segmental rather than topographical nature of the somatotopic organization of the SII cortical neurons further vitiate the value of this mode of organizational display. The important thing to note is the mediolateral reversal of the figurine from the manner in which it is traditionally presented. DISCUSSION

A question of technique Having established that, tbr the cat at any rate, the previously held picture of the body orientation in SII was incorrect, it becomes necessary to consider how such a misapprehension came to be. The primary culprit probably was the technique in general use in mapping studies. The early maps of the somesthetic cortexZ, e9 date from long before the microelectrode era. The usual method of mapping involved placing large, blunt macroelectrodes upon the cortical surface in a 1.0--2.0mm grid pattern. For large areas, such as cat SI, this method was able to, and indeed, did, give an accurate portrayal of the receptive field organization in somesthetic cortex. As long as the electrode lay upon an area of cortex which received many projections from a highly localized area of the body, it was possible to map these projections in some detail. Conversely, areas of the body which did not typically send dense projections t o t h e cortex, i.e., axial areas, proved more difficult to map in detail and, at times, were not located at all. Thus, details of upper limb and trunk are extremely scarce in the map of the American opossum 24, the hedgehog 27 and even in the relatively large brained macaque monkey 6s. In the much smaller SII region these problems are compounded. In the case of Berman's 7 map of cat SII, no responses are reported from body areas proximal to the knee or elbow, other than from the head. It appears that in this instance mapping continuity was inferred rather than observed. The surface area problem is aggravated by sulci in gyrencephalic animals. The banks of a sulcus are generally unavailable for examination by surface recording techniques. Aspiration of the unwanted sulcal wall has been tried 61, but this is a rather violent and unphysiologic solution to the problem. Removal of portions of the cortical mantle without damaging the underlying white matter is a difficult procedure. The fiber pathways to SII are particularly susceptible to damage when cortex medial to SII is removed by aspiration13, ~9. It is likely that Berman 7 did not observe activity

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proximal to the lower limbs because these areas were buried within the anterior suprasylvian sulcus (Fig. 5). Similar reasons may be responsible for Adrian's 2 claim that cat SII contained projections only from the claws and digit tips. Experimental material in the present study showed such variation in the shape of AEG that at times almost the entire body representation lay exposed on the gyral surface. Much more frequently, however, only the head and lower limb projections were exposed. It would seem, therefore, that failure to find representations from the upper limbs and body, coupled with the peculiar separation and wrap-around effect of the pre- and postaxial forearm representations, could easily account for the mistaken belief that the limb apices are directed medially in SII. Two evoked potential studies clearly indicated in both the dog43 and the cat 9 that projections from the trunk were found lying laterally in AEG, not medially as claimed in the present paper. These two studies, plus the present one, used sodium pentobarbital anesthesia, hence anesthetic effects cannot account for the difference in observation. It was consistently noted during the course of this study that single unit responses, drivable from the body surface, were extremely rare in the area of AEG lateral to the medial convexity. Responses from the medial half of the gyrus, the somatotopically organized half, were, on the other hand, plentiful. Very few punctures failed to provide data in the medial half of AEG, while in the lateral half, very few punctures did provide data. It is difficult to imagine how a sparse collection of nonsomatically organized cortical units could give rise to a prominent, somatotopically organized slow wave as reported by these authors. This is a good example of the difficulties encountered in trying to relate single unit activity with slow waves whose origins and physiology are obscure. The problems encountered in dealing with gyrencephalic brains are not ameliorated when lissencephalic subjects are selected. Such animals lack the physical size and somesthetic and motor specializations that appear to be so closely coupled with the gyrencephalic condition. Thus, Lende24 was only able to indicate the presence of SII in the American opossum, Didelphis marsupialis, no detailing of its somatotopic organization being possible. Though microelectrodes are capable of resolving the activity of small clusters of neural units and single units, as well as that of the slow potentials that were so long the special province of the surface techniques, their use in cortical somesthetic mapping studies has not been popular until quite recently. Only four complete studies come to mind: two in the monkey63,~4 and one each in the rat 5s and the cat 54. Considering that the microelectrode technique can, in addition, give access to previously hidden gyral depths, disclose the connectivity of adjacent cortical columnsa3,aa,e4 and permit a much closer spacing of recording sites on the cortical mantle5s, it is surprising that the technique has been neglected.

A question of emphasis The above should not be taken to indicate that single units have not been studied in somesthetic cortex. This is not the case. The properties of single units in these areas

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have been the subject of several studies such as that of Mountcastle aa which disclosed the columnar arrangement of cells in that region as well as the study of Carreras and Andersson s which dealt with the functional characteristics of single units in cat SII. The problem has been that until recently the people who were interested in the physiological properties of somesthetic cortical neurons have not been at all interested in their neighborly interrelations. Nor, have the mappers been especially intrigued by the possibilities inherent in considering both somatotopy and neuronal response properties at the same time. As a result of this, one has the example of the detailed and otherwise excellent study of Carreras and Andersson s who recorded from 5t8 single units in cat SII and failed to note that the body representation was opposite that claimed by Berman 7 some two years earlier. Bilaterality and S I I

Early evoked potential studies in somesthetic cortex disclosed that while projections to SI arose almost exclusively from the contralateral body 68-7°, SII received both contralateral and ipsilateral projections. This finding was substantiated in the present study and by other investigators (Introduction) up to the present day 26. When single units in SII are examined, the picture is not as clear. It has been reported that in the monkey some 90% of all units display bilaterally symmetric receptive fields~4. These results were obtained from unanesthetized subjects. A somewhat earlier study using barbiturated cats s reported that only about 5 % of cat SII unit responses displayed bilateral or ipsilateral receptive fields. This compares favorably with the 4% figure reported in the present study which used both deeply anesthetized (pentobarbital) and lightly anesthetized (nitrous oxide) subjects. There was no significant difference in the frequency of bilateral or ipsilateral receptive fields between the two anesthetic states. Differential anesthetic effects upon the slow wave SII activity had been reported earlier with the observation that the ipsilateral component of the wave could be reduced and eventually suppressed with deepening anesthesia 7°. It was reported in the same study that the bilateral slow wave survived the acute extirpation of the opposite somesthetic cortices. As yet unpublished results from this laboratory show that the bilateral unit activity in cat SII is unaffected by chronic ablation of the opposite cortex. This observation applies both to the frequency of occurrence of bilateral receptive fields and to the physiological properties of the SII neurons as well. When it is remembered that the anatomy of the commissural connections linking the two hemispheres is the same in both the cat 22 and the monkey 4°,41, the onus of bilaterality in SII would seem to be placed upon either a differing set of physiological properties in the commissural projections of the two animals or upon subcortical rather than commissural factors. As will be seen, the subcortical assumption leads to more problems. As with the interhemispheric connections, the thalamocortical relations of SI and SII are similar in both cats and monkeys. The primary, and probably the only, thalamic relay to SI proper is from the ventrobasal thalamic nuclear complex (Vb) 1°,~3. This is an essential projection 52. Approximately 30-50 ~ of the Vb neurons send collateral sustaining 5~ projections to SII a°,53. Not surprisingly, then, Vb neurons have Brain Research, 44 (1972) 483-502

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functional properties that are very similar to those found in SI and in the mechanoreceptive, somatotopically organized part of SIIS,85,4L Another group of thalamic nuclei, the posterior group (Po) also projects to SII in addition to the Vb collaterals17,1s,32. The Po projection does not overlap appreciably with the Vb projection but is found caudal to and lateral to the region subserved by Vb 17,1s (Fig. 2). These projections are of interest because Po neurons, unlike those of Vb, are known to receive some bilateral input from the anterolateral systems of the spinal cord 44. However, Po neurons are not somatotopically organized, nor do they exhibit tactile modality specificity or receptive field boundary constancy. Physiologically, a separation of Vb and Po type activity in the cat s and the monkeye4 has been made, the mechanoreceptive, somatotopicaUy organized area being geometrically distinct from the non-specific and non-somatotopically organized area. To recapitulate: (1) the anatomical relations of SII, based upon both anatomical and physiological evidence, appear to be the same in both cats and monkeys; (2) there is virtually no bilateral input to the somatotopically organized portion of SII from Vb (other than from peri-oral regions) which is the primary source of subcortical input to this area; (3) the anesthetic state does not appear to be an important factor with Vb responses or those of its cortical target areas. Po and its cortical target area appear to be labile to anesthetic depth 44, but Po apparently does not project to the same area of SII as does Vb; (4) extirpation of the opposite somesthetic cortices has little effect upon bilaterality in the somatotopically organized portion of SII. Yet, the cat has a very low proportion of bilaterally activated SII units while the monkey's proportion is quite high. It appears that there may be a valid species difference that might be explained by differences in the electrophysiological properties of the commissural cortical fibers or by a more pronounced admixing of anterolateral and Vb type projections in monkey SII as opposed to that observed in the cat. This, in turn, might have behavioral ramifications in that bilateral, coordinated manipulative activities are likely to be more important to the arboreal monkey than to the terrestrial cat. The electrophysiological evidence indicates that Po and Vb have separate projection areas in monkey SI164, but anatomical evidence as to the projection field of monkey Po is lacking. Stereographie representation in somesthetic cortex

Cortical mapping procedures that have relied upon surface evoked potential and unit cluster recording techniques have produced a stereographic representation of the body on the cortical mantle which reflects the actual connectivity of the body parts. Projections from the hand, for instance, will be found localized in one area of the sensory field. Digit projections will be found adjacent to the hand projection as well as being represented in serial order. Digit 3, for example, will lie between those projections devoted to digits 2 and 4 while all three will be connected with the hand representation54,5s,os, although Rube154 does note that the orderliness of the configuration breaks down at the motorsensory boundary region in adult cats. An orderly body representation has also been reported at thalamic levels in Brain Research, 44 (1972) 483-502

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monkeysa6,5°, in the opossum 46, in the cat and rabbit 51, and in the raccoon e0, as well as at medullary levels in the raccoon 21 and in the sheep 72, This caricaturing of the body at the level of the somatic sensory cortices is not universally accepted. Other recent studies have reported that the representation, while topologically intact, tends to follow the dermatomal rather than a strict topographic pattern in its projection to cortex68, 64. These studies present the apical limb projections as occupying a central position between the pre- and postaxial arm and leg projections, a finding in agreement with the present results. A recent mapping study of the spider monkey SI 4s reports a pre- and postaxial separation in the cortical representation of the leg but not of the arm. These investigators' use of a 1.0-2.0 mm mapping grid may have caused them to miss the preaxial arm area altogether. In all of these studies, whether the map shows a segmental or a topographic representation of the body, projections from a given body region are found grouped together in their cortical target area. A similar segmental representation was also observed in cat 15 and monkey SI164. The published details of the monkey study do not permit a precise assessment of SII somatotopy as has been presented in the present study. However, it appears that cat SII projections are more 'segmentally' arrayed than are the SI projections. Whereas a partial reconstruction of the 'topographical' animal is observed in the projection system subserving SI in the cat, this is much less pronounced in SII. A testable hypothesis would be that the ordering of projections to SII might follow the sequence in which the dorsal rootlets enter the central nervous system. This is a tempting speculation which is given some substance by the similarity between the total receptive field areas served by the fibers of the dorsal rootlets 47 and the 'dermatomal strips' which comprise the SII arm and hand area in the present study. Functional implications of duality in sensory cortex

We still know very little about the functional reasons for the two somesthetic cortices. The present effort bears out an earlier report that deep and joint responses are not common in SII s whereas they are in S135. This implies that SII may be more concerned with pure exteroception while SI may concern itself with input from both within and without the organism. Otherwise, both physiologically and anatomically, the similarities between SI and SII are more pronounced than their differences. The reports of behavioral effects of selective ablations of somesthetic cortex are conflicting. One group of studies reports that bilateral ablation of SII impairs tactile discrimination performance in dogs and cats4,1L In monkeys the loss of SI seems to impair tactile discrimination ability more severelya9 although agreement on this is not unanimous ~5. The middle position is also occupied; with reports that removal of either SI or SI1, but not both, produces only temporary, reversible deficits73-76. Consideration of not only the somatotopic interrelations of cortical sensory neurons, but of the interrelations of their tactile interests as well, by comparing both the somatotopic and physiological properties in SI and SII may give the needed insight into the actual significance of duality in somatic sensory cortex. Brain Research, 44 (1972) 483-502

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SUMMARY A detailed microelectrode mapping study of the second somatic sensory area (SI1) in cats anesthetized with either sodium pentobarbital or nitrous oxide disclosed that: (1) The orientation of the body representation in SII is reversed in a mediolateral direction from the way that it has been portrayed in the past. The limbs are directed laterally, not medially in the anterior ectosylvian gyrus. (2) Units in the somatotopically organized mechanoreceptive portion of SII do not commonly have bilateral receptive fields. This result is unaltered by the lightness or depth of anesthesia in the subject. It is suggested that the lack of bilateral representation in cat SII when compared with the predominance of bilaterality in monkey SII may represent a valid species difference. (3) The somatotopic organization of projections to the hand and digit areas o f cat SII does not follow the body topography. Rather, the projections form strips or chains of receptive fields which are oriented near the transverse plane. Neighboring strips in the hand projection area may not be at all similar in their receptive field makeup. It is suggested that these strips are related to the receptive field pattern encountered as the dorsal rootlets enter the central nervous system. ACKNOWLEDGEMENTS I wish to thank all of those whose assistance during the lengthy recording sessions made this study possible. Particular thanks go to John Benson, Dan Lyons, Marty Preache and Tim Smith. To Professor John I. Johnson, Jr. go particular thanks for the use of his facilities and time. Finally, to my wife, Emeline Gatewood Haight, who attended to the histological processing of seemingly myriad cat brains, I express the deepest gratitude. This study was supported by Public Health Service Fellowship GM-49222 and by N I H Research Grant NS 05982.

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