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Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey
Brain Research, 64 (1973) 85-102 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
S O M A T O S E N S O R Y P R O P E R T I E S OF N E U R O N S I N T H E P A R I E T A L C O R T E X ( A R E A 5) OF T H E RHESUS M O N K E Y
85
SUPERIOR
HIDEO SAKATA*, YOSHIO TAKAOKA* *, ATSUSHI KAWARASAKI** * AND HIDETOSHI SHIBUTANI* *** Department of Physiology, Osaka City University Medical School, Asahimachi Abenoku, Osaka (Japan)
(Accepted June 8th, 1973)
SUMMARY The response of individual neurons within Brodmann's area 5 of the parietal lobe to physiological somesthetic stimuli was studied in unanesthetized rhesus monkeys. Most neurons were sensitive to light mechanical stimulation of the skin and deep tissue and/or joint rotation. These neurons were distinguishable from those of the primary somatosensory area by several characteristics: multiple joint interaction, ipsilateral receptive field, bilateral interaction, interaction between forelimb and hindlimb or trunk, and excitatory interaction of joint and skin stimuli. Some were highly selective, in that they responded only to certain critical patterns of stimuli involving both joint and skin. The results were viewed as supporting the hypothesis that area 5 is the site of higher order processing of somesthetic information received from the lemniscal system, and may give rise to the neural code of position and form of body and tactile objects in 3-dimensional space.
INTRODUCTION Recent neurophysiological investigations in the somatosensory system concerning the neuronal mechanisms of sensory coding have indicated that the sensory information encoded in the peripheral afferents is transmitted and reproduced in the primary somatosensory cortex (S I) with considerable fidelity, both in its temporal and * Present address: Tokyo Metropolitan Institute for Neurosciences, Fuchu-city, Tokyo 183. ** Present address: Department of Neurosurgery, Nagoya University. *** Present address: Department of Neurosurgery, Osaka City University. * * * * Present address: Osaka Electro-Communication University.
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topographic patterns35, 52. Moreover, correlative studies of psychophysics and electrophysiology suggest that, for certain simple aspects of somesthesia, the neural events in the cortex are closely related to the subjective sensory events3'5, 3v. These findings contrast with recent ones in the visual system, where there appears to be a drastic modification of the sensory messages between the periphery and the primary visual cortex, suggesting that the visual cortex may occupy a more advanced stage of hierarchical processing than does the primary somatic sensory cortex26;"v. In recent experiments in unanesthetized monkeys, a few neurons in the S I were found to be sensitive to the direction of movement of a cutaneous stimulus, a property not possessed by primary afferents. This opens the possibility that a further processing or elaboration of its input may occur in the S I z7,48,54. However, these neurons are relatively rare in the S i, and no other form of elaborate processing has yet been found. This stimulated us to initiate a study of neural activity beyond the level of the S I, to survey the cortical mechanism of somesthetic perception in areas in which a further hierarchical processing of somatic sensory input may occur. The posterior parietal cortex (areas 5 and 7) has long been known to be concerned with the perception of tactile objects, body form and extrapersonal space11,14. This has been suggested by ablation experiments in monkeysS,16,~0,3a,40, 4~, and by clinical studies of the 'parietal lobe syndrome '~3. Although certain aspects of these functions are related to vision as well as to somesthesia, and the location and extent of lesions are difficult to specify precisely in both ablation experiments and in humans with brain injury, there is strong evidence that this region is the site of higher-order processing of somatosensory information. Indeed, recent anatomical studies of corticocortical connections have demonstrated a heavy projection from the S I to area 5~s,3s. In the present work we have studied some of the response characteristics of area 5 neurons to physiological somesthetic stimulation. The results suggest that such a high-order processing occurs in area 5, and that it may be related to tactile pattern recognition. These results have been the subjects of previous notes 45-47, and are in basic agreement with those described recently in the short communication by Duffy and Burchfie119. METHODS
Twenty experiments were done in monkeys, Macaca mulatta, weighing between 2.8 and 5.5 kg. On the day before the start of recording, the metal chamber of the microdrive, as well as the tracheal cannula, was implanted under pentobarbital sodium anesthesia. The skull was exposed, and a trephine hole about 2 cm in diameter was made, centered over the superior parietal lobule. Usually, both the central sulcus and the intraparieta! sulcus could be seen through the dura, which was left intact, and they were used as landmarks for placing the chamber. The latter was fixed to the skull with screws and dental cement, and was sealed water-tight with dental impression compound. After being filled with mineral oil the chamber was covered with an acrylite cap packed with silicone rubber. The tracheal cannula was an L-shaped non-kinking rubber tubing for pediatric anesthesia trimmed short and at-
SOMATOSENSORY PROPERTIES OF AREA 5 NEURONS
87
tached with a small collar for suturing to the skin. The trachea was truncated beneath the larynx, and the cannula was introduced into its distal end and then sutured to the skin of the neck; the skin was in turn sutured to the periostium of the sternum to get a good fixation. All skin incisions were sutured so that no operational procedure was left except for the excision of dura. The latter was proved to be pain-free, for no dilatation of the pupils or piloerection was observed during dural incision. On the morning of the experiment the animal was immobilized with Flaxedil, injected intraperitoneally (8 mg/kg). As soon as the monkey showed difficulty in breathing, the tracheal cannula was connected to the respirator. End-tidal CO2 was adjusted between 3.5 and 4 . 0 ~ , and rectal temperature was kept at a normal level throughout the experiment. The chamber was fixed to a metal frame by a 4-mm screw passing into a tapped hole in an arm of the chamber. The animal was seated on a small padded bench and kept in the upright position, which allowed freedom to manipulate all 4 limbs and the trunk. Usually, the animal remained in good condition for more then 24 h, but we took an intermission of several hours at night, as the E E G showed a drowsy pattern toward midnight, and responsiveness of area 5 neurons tended to decline along with increasing somnolence of the animal. After excision of the dura, mapping of the surface-evoked potential was made in the S I to get some idea of somatotopical location of area 5, assuming the latter might correspond approximately to that of the S I in the same sagittal plane. A modified Davis micromanipulator with a glass plate was fixed with 3 metal clamps and sealed hydraulically with a packing ring of silicone rubber. The sites of penetration were determined under microscopic observation and were noted on an enlarged photograph of the exposed cortex. The microelectrodes were electrolytically sharpened tungsten wire 125 # m in diameter and insulated with polyurethane lacquer. The impedance was adjusted between 3 and 10 M ~ at 1000 Hz by passing negative current in saline under the microscope, to break the insulation up to 10-20 # m from the tip. The electrical signs of impulses in neurons were recorded from an extracellular position via a conventional pre-amplifier and CRT, with the aid of a differential amplitude discriminator. All data were stored on magnetic tape. In 7 later experiments, post-stimulus time (PST) histograms were made with the averaging computer (ATAC501, Nihonkohden) summing 10-20 trials. Stimulation was mostly applied manually, except for sine-wave oscillations generated by a mechanical vibratory stimulator and delivered to the skin. For light deformation of the skin, fingers or acrylite cylinder and plate were used as well as glass probes. Joint rotation was also applied manually; we checked carefully the effect of deformation of adjacent skin and deep tissue. The cooperation of two experimenters was sometimes necessary to test the interlimb interaction or other complicated patterns of stimulation. Usually, the onset and end of stimulation were registered with a microswitch. Sometimes, we used a potentiometer to measure the joint movement.
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H. SAKATAet al.
Histological method At the end of each experiment a guide wire was inserted through the microdrive into the brain to indicate the orientation of penetrations, and the brain was removed and fixed in 10 % formalin. Serial celloidin sections 50/~m thick were stained with thionine. The surface of the section was made vertical to the axis of the superior parietal lobule so as to be suitable for cytoarchitectural study. Identification of electrode track and depth of recording was facilitated by the electrolytic lesion by passing negative current of 5/~A for 5-10 sec through the electrode tip. The cortex through which the electrode passed was classified according to the cytoarchitectonic criteria of Brodmann 6. The boundary between areas 2 and 5 was most clearly indicated by the change of thickness of layer III as described by Powell and Mountcastle 42 in rhesus monkeys, and by Hassler and Muhs-Klement 24 in cats. Sites of unit recording were plotted on tracings of histological sections at a magnification of × 20. Shrinkage of the brain was found to be negligible with the use of acetic acid-ethanol mixture as a mordant.
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Fig. 1. Upper: lateral view of cerebral hemisphere of Macaca mulatta showing site of lower drawing. Lower: site of entry of electrode penetrations. Filled circles: penetrations passed through area 5. Open circles: penetrations entered area 2 on the surface and passed into area 5 in the depth diagonally. Filled triangles: penetration in area 2. The boundary of Brodmann's area is indicated by dotted lines. CS, central sulcus; PCS, postcentral sulcus; LF, lateral fissure; STS, superior temporal sulcus; IPS, intraparietal sulcus; LS, lunate sulcus.
89
S O M A T O S E N S O R Y P R O P E R T I E S OF A R E A 5 N E U R O N S
RESULTS
(1) General response characteristics o f area 5 neurons Sixty microelectrode penetrations were directed to traverse Brodmann's area 5 in the superior parietal lobule, a triangular region between the postcentral and intraparietal sulci including the anterior bank of the latter sulcus. Another 10 penetrations were made in the posterior part of the postcentral gyrus to study neurons in area 2 for comparison. Four hundred and seventy-seven neurons were isolated and studied in sufficient detail to allow a definition of the adequate stimuli for excitation of each. In those penetrations for which precise histological identifications of electrode penetration in regard to cytoarchitectonic boundaries were made, 245 neurons were located in area 5, and 54 in area 2. The site of entry of 43 penetrations in which these area 5 neurons were recorded is shown in Fig. ! including those that passed through area 2 on the surface to reach the buried portion of area 5. In general, neurons of area 5 were activated by physiological somesthetic stimuli, although most of them were not sensitive to stationary point stimulation of skin and deep tissue, in contrast with those of the S I. The adequate stimulus was often a complicated pattern of touch and joint rotation, rather than a simple localized stimulus of one or another submodality. We have classified area 5 neurons into 6 categories, as shown in Table I. We assumed that the responses to the light tactile stimuli we used were cutaneous in origin, when there was no evidence to indicate additional driving by stimulation of deep tissue, and that driving by joint rotation or position was related to the joint afferents. However, the criteria were operational and somewhat arbitrary, so that this does not exclude the possible participation o f other afferent inputs, including the muscle afferents. Class 1 and 2 neurons are those that were activated by superficial tactile stimulation of the skin without any modification by joint positioning. Neurons of class 1 displayed directional selectivity similar to that of cells of the S 137,48,53; neurons of class 2 showed no directional sensitivity. Class 3 is composed of a group of neurons activated by the rotation of a single joint, and therefore comparable to the joint
TABLE I CLASSIFICATION OF AREA 5 NEURONS
Contralateral lpsilateral Class 1 - Class 2 - Class 3 - Class 4 - Class 5 - Class 6 - Total
%
Skin (directional) Skin (non-directional) Joint (single) Joint (combination) Deep - - others Joint and skin
Bilateral
Total
13 10 29 35 5 50
1 2 13 I0 0 12
8 2 -18 10 27
22 14 42 63 15 89
142
38
65
245
15.5
26.5
58.0
% 9.0 5.7 17.2 25.7 6.1 36.3
H. SAKATAet al.
90
neurons in the S I ~6` except that many were activated by rotation of the ipsilateral joint. Class 4 neurons are those that showed interactions of two or more joints so that certain combinations of joint rotation and/or position were necessary for optimal driving. Class 5 are the neurons activated by stimulation o f subcutaneous tissues other than the joints. Class 6 includes all those neurons in which various types of interaction between joint rotation and skin stimulation were observed. As a whole, joint input seems to be predominant in area 5, for class 3 plus class 4 made up 42.9 and class 6 (mixed type) 36.3 ~ . Skin neurons (class 1 plus 2) were only 14.7 ~. These percentages do not necessarily represent the true distribution of neuronal types in the total population in area 5, for we passed over many unclassified neurons not listed in here.
(2) Skin neurons (directional or non-directional) Neurons in area 5 that were activated only by cutaneous stimulation did not show any striking differences from the skin neurons in the S I. However, they usually had wider receptive fields than do S I neurons, and bilateral receptive fields as well as ipsilateral receptive fields were observed. Moreover, directional selectivity was observed in nearly two-thirds (22/36) of these area 5 neurons, a proportion much greater than in the S I. Fig. 2 illustrates one such neuron with bilateral receptive fields. Directional selectivity was very prominent: gentle rubbing of the skin from left to right elicited a vigorous continuous discharge, whereas the opposite movement from right to left produced minimal response or even suppression of spontaneous discharge. Most of the non-directional skin neurons were also difficult to drive by stationary pressure or vibration. Their sensitivity to moving stimulation was similar to that of neurons in the rostral part o f the second somatic sensory area (S II/r) 53, but none of them had the bilaterally symmetrical receptive field found for S II neurons.
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Fig. 2. Receptive field and responses of an area 5 neuron that showed directional selectivity to the moving cutaneous stimulation. Upper and lower traces are the discharges of the neuron during consecutive trials of stimulation applied in the middle part of receptive field shown in the left drawing. Direction and timing of stimulus is indicated by horizontal bars below the trace: L -+ R, left to right, R -+ L, right to left. Negativity is upward in this and following records of impulses.
SOMATOSENSORY PROPERTIES OF AREA 5 NEURONS
91
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Fig. 3. Responses of an area 5 neuron during 4 sequences of rotations and positionings of ipsilateral wrist and elbow, as indicated on two drawings on the left. A: elbow flexion was superimposed on steady wrist flexion. B: elbow flexion during steady wrist extension. C: wrist flexion during steady elbow flexion. D: wrist flexion during steady elbow extension. Horizontal bars indicate the rotation of the second joint; the joint was moved during the initial several hundred msec and then maintained in the end position.
(3) Joint combination neurons Various types o f interaction o f multiple joint rotations were observed in 63 neurons belonging to this class. Fig. 3 illustrates a typical example o f this class o f neuron, which was related to b o t h wrist and elbow o f the ipsilateral side. In this example either the wrist or the elbow was m o v e d while the other joint was fixed in a certain position. Elbow flexion elicited a sustained response when the wrist was fixed in the flexed position (Fig. 3A). On the other hand, very little response was evoked by the same movement o f the elbow when the wrist was kept extended (Fig. 3B). Likewise, wrist flexion elicited a g o o d response if the elbow was flexed (Fig. 3C), but almost no response if the elbow was extended (Fig. 3D). Therefore, the best response was obtained with a combination o f wrist flexion and elbow flexion. The m o r e peculiar examples were neurons that were maximally activated by the bilateral interaction o f joints, as illustrated in Fig. 4. Of course, it is difficult to prove that the simultaneous rotation o f joints on both sides is prerequisite for maximal activation o f the neuron, for there are so m a n y possible contaminating stimuli during such a movement. However, we excluded such stimuli carefully, especially the effect o f rotation or bending o f the backbone and neck. Indeed, we identified 8 neurons driven by the latter stimulation. In Fig. 4 the discharge o f a neuron is shown in a sequential time histogram. The 'best' stimulus for this unit was a parallel rotation o f both arms f r o m right to left (sketch on the left). The vigorous discharge produced
H. SAKATAet al.
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Fig. 4. Response of an area 5 neuron to bilateral shoulder rotations, displayed in impulse time histograms. Upper: response to parallel rotation of left and right arms to the left as shown in the insert drawing. Middle: separate rotation of right arm (inner rotation of right shoulder). Lower: separate rotation of left arm (outer rotation of left shoulder). Ordinate is number of impulse, abscissa time in sec, bin size 100 msec. Joint rotation is indicated by arrow and steady positioning by dotted line above each histogram. R, about 60° to the right; L, about 60° to the left.
by this movement, and the considerable duration of the sustained discharge when the arms were held towards the left side are shown in the upper histogram. Apparently the main components were the inner rotation of the right shoulder and outer rotation of the left shoulder, while the angle of elbow or wrist did not modify the response of this unit. On the other hand, separate rotation of either arm was much less effective, as the inner rotation of the right shoulder alone elicited only a small discharge (second graph), and the outer rotation of the left shoulder evoked no response (third graph). We found many joint combinations other than those illustrated here, and some of them showed summation rather than antagonistic interaction of two or more joints. Moreover, some neurons were activated in a narrow range of intermediate joint angle rather than at the extremes of rotation.
(4) Joint and skin units The interaction of joint rotation and skin stimulation was characteristic of some neurons of area 5. The degree of complexity of the maximally effective stimulus combination varied greatly for different neurons. Fig. 5 shows one of the simplest types of interaction; i.e., the combination of elbow flexion and stimulation of the skin on the back of the hand of the contralateral side. As illustrated in the upper trace, elbow flexion alone elicited only a limited and unstable response. The response to the rubbing of the skin of the dorsum of the hand was also relatively
93
SOMATOSENSORY PROPERTIES OF AREA 5 NEURONS
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Fig. 5. Response of an area 5 neuron which showed excitatory interaction of joint rotation and cutaneous stimulation. Upper trace: discharges of unit during contralateral elbow flexion. Middle trace: response to a moving cutaneous stimulation on the back of contralateral hand. Lower trace: response to simultaneous elbow flexion and cutaneous stimulation, as indicated in the left drawing. The joint was moved slowly during the period indicated by horizontal bars.
weak (second trace). The combination of elbow and skin stimulation, however, elicited a vigorous response (third trace). In some cases, the effect of joint rotation was marked even in the steady position, as illustrated in Fig. 6. The 'best' response of this neuron was obtained by the gentle moving stimulus on the skin of the contralateral forearm in the direction from proximal to distal, with the shoulder adducted, as shown in the PST histogram on the left. A cutaneous stimulus moving in the opposite direction, with the shoulder in the same position, produced much less response (middle histo-
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Fig. 6. Effect of antagonistic joint positions upon the response of an area 5 neuron to moving cutaneous stimulation. Each histogram shows the average firing rate of 10 trials. Left histogram: response to cutaneous stimulus moving from proximal to distal on the ventral side of contralateral forearm during steady adduction of the shoulder. Middle histogram: response to the stimulus moving from distal to proximal in the same arm position. Right histogram: cutaneous stimulus from proximal to distal during steady shoulder abduction. A r m position and approximate receptive field is shown in the drawing above each histogram, and the direction and period of cutaneous stimulation is given underneath.
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Fig. 7. Upper: effect of difference in direction of moving cutaneous stimulation upon the response of an area 5 neuron. Each bar indicates the total number of impulse of 10 consecutive trials. Direction and receptive field in the ipsilateral forearm is shown in the drawing on the right; D, distal; P, proximal; M, preaxial; L, postaxial, The arm was held in front of the animal and at 90° to the body axis. Lower: effect of change in arm position upon the response of the same neuron to the moving cutaneous stimulation in the optimal direction (distal to proximal). Each bar indicates the total number of impulses of 10 trials at the angle given on the abscissa. Number of degrees indicates the angle of shoulder rotation from vertical axis pointing below; posterior rotation is marked with a minus sign.
gram). O n the o t h e r hand, a l m o s t no response was elicited when the shoulder was a b d u c t e d even when the skin was s t i m u l a t e d in the o p t i m a l direction ( h i s t o g r a m on the right). Fig. 7 shows a m o r e detailed study o f the effect o f a change in j o i n t p o s i t i o n on a n a r e a 5 n e u r o n which was m a x i m a l l y driven b y m o v i n g c u t a n e o u s s t i m u l a t i o n o f the f o r e a r m in the direction f r o m distal to p r o x i m a l with the shoulder a n t e r i o r l y elevated. The directional selectivity is clearly seen in the u p p e r g r a p h which shows the responses o f this n e u r o n to a c u t a n e o u s stimulus m o v i n g in a n u m b e r o f directions with the a r m fixed in front o f the a n i m a l (90 ° in the lower diagram). The response to the o p t i m a l d i r e c t i o n o f c u t a n e o u s m o v e m e n t was then r e c o r d e d at a n u m b e r o f a r m positions, as shown in the lower graph. The exact angle o f the shoulder was n o t so critical as long as the a r m was raised to some extent (45-135°). The m a x i m a l response o f this n e u r o n was n o t o b t a i n e d at the extreme a n t e r i o r elevation (180°), b u t at some i n t e r m e d i a t e p o s i t i o n (135°). M a r k e d facilitation b y c u t a n e o u s s t i m u l a t i o n was occasionally observed in a n e u r o n t h a t was driven b y a c o m b i n a t i o n o f j o i n t positions, as illustrated in Fig. 8.
95
SOMATOSENSORY PROPERTIES OF AREA 5 NEURONS Impulse/sec
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Fig. 8. Response of an area 5 neuron to bilateral shoulder rotation and its enhancement by skin contact. Left 3 PST histograms depict the responses, from above to below, to ipsilateral shoulder adduction, to contralateral shoulder adduction, and to bilateral shoulder adduction. Right histogram indicates responses to the combination of cutaneous stimulation and bilateral shoulder adduction as shown in the upper drawing. The period of stimulation is given at the bottom; the shoulder was rotated during the initial several hundred msec and then maintained in the end position.
This neuron was driven by shoulder adduction of either the left (ipsilateral) or right side, respectively (upper two histograms on the left), and the simultaneous adduction of both shoulders elicited slightly more discharge than did the separate stimulation (lower left). Marked enhancement of response was observed by adding the skin contact of hands and forearms of both sides to the joint combination (right histogram). The 'best' stimulation was found to be 'rubbing' the forearms and palms of both sides on each other. Therefore, this is a rather peculiar type of joint and skin interaction involving two limbs. The skin receptive field, however, was difficult to determine precisely, because almost no response was elicited by cutaneous stimulation alone. A similar type of highly complicated joint and skin interaction was also found between the forelimb and hindlimb or the limb and trunk in some other neurons. We called these 'matching neurons', because the 'best' stimulus for them was to bring a part of a limb in contact with a part of another limb or the trunk, as if to match two body regions to each other. Fig. 9 shows another example of a matching neuron which responded even more selectively to a specific pattern of stimulation than the neuron
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Fig. 9. Response of an area 5 neuron which required a complicated pattern of combination of joint and skin stimulation for optimal driving. Left histogram: PST histogram of 10 trials to depict the response to 'best' stimulus as illustrated in insert drawing; rubbing the ipsilateral forearm in flexed position with contralateral palm and fingers from proximal to distal. Upper right: response to moving cutaneous stimulation on the left forearm from proximal to distal with experimenter's hand. Lower right: response to combined joint rotation imitating 'best' stimulus without contacting two skin regions; left elbow flexion and right elbow flexion with shoulder pronated.
o f Fig. 8. The 'best' stimulation was 'rubbing' the left (ipsilateral) forearm, which was flexed at the elbow, with the right palm and fingers in the direction from proximal to distal (histogram on the left). The cutaneous stimulation on the left forearm did evoke a small discharge (upper right), whereas the stimulation of the right hand elicited no response. The combined joint rotation in the same pattern o f movement as the 'best' stimulation without contacting two areas evoked only a small response (lower right). On the other hand, we confirmed that the right elbow extension had a strong suppressive effect on this neuron. Thus the 'best' stimulus could not be analyzed into individual excitatory components in this case, in contrast to the neuron of Fig. 8. This was often true o f 'matching' neurons, and therefore they were likely to be overlooked as undrivable in earlier experiments. DISCUSSION
(1) Characteristics o f area 5 neurons In contrast with previous observations in anesthetized animals 4a, we found in
SOMATOSENSORY PROPERTIES OF AREA 5 NEURONS
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the present study of unanesthetized monkeys that neurons of area 5 could be driven by natural somesthetic stimulation, if the stimuli were applied in an appropriate manner. The stimulation that activated these neurons was either joint rotation or light mechanical deformation of the skin and deep tissues such as gentle surface movement and steady light pressure. These were most likely to activate low-threshold afferents of joint and skin, suggesting that area 5 is closely related to the primary somatosensory cortex (S I) as far as the submodalities are concerned. On the other hand, a striking difference was found in regard to the spatial configuration of adequate stimuli, i.e., the receptive field organization. In general, the receptive fields of area 5 neurons are much larger than those of S I neurons, and they are not restricted to the contralateral side of the body. A considerable number of neurons showed (1) ipsilateral receptive fields, (2) multiple joint interaction, (3) bilateral interaction, (4) forelimb and hindlimb interaction, and (5) limb and trunk interactions, respectively. This indicated that there was a marked convergence of the input from different parts of the body upon these cells. However, it does not indicate that this convergence is diffuse and non-specific as suggested by previous electrophysiological studies in chloralosed animals l& On the contrary, converging input seems to be subjected to an elaborate processing which may result in higher selectivity in trigger features 3. One of the characteristic types of neuron in area 5 was that which we classified as a 'joint combination' neuron. The response characteristics of these cells were in sharp contrast with those of joint neurons in the S I which respond only to movement of one single joint in one direction a6, although we found several joint combination units located in area 2 or in the transitional zone between areas 2 and 5. There are several possible neural mechanisms underlying this phenomenon. One is the convergence of inhibitory input from some joints upon the excitatory input from others. The second is the convergence of excitatory input from two or more joints. The antagonistic type of interaction is favorable to the first explanation, whereas the summating type of interaction seems to support the second hypothesis. However, it may be more important to exclude the possibility of peripheral mechanical factors which might change the response of primary afferents innervating a single joint, owing to the difference in position or movement of adjacent joints. Besides, the intervention of muscle afferents and other deep receptors must be considered, for Burchfiel and Duffy 7 described some neurons in area 5 that were activated by direct stretch of the muscle. Another distinctive feature of area 5 neurons was the interaction of joint and skin stimulation in exciting them, which suggests a convergence of different submodalities, in contrast with the strict modality segregation in the S 134,43. The only interaction between these two submodalities observed in the S I was the 'skin to joint inhibition' described by Mountcastle and Powell a6. We also observed this type of interaction for an occasional neuron in area 5. Some of this class of neurons showed a marked suppression in certain joint positions, which might be interpreted as 'joint to skin inhibition' (e.g. Fig. 6). However, most of the joint and skin neurons required the simultaneous stimulation of the two for the optimal activation, so that the two components were both excitatory.
98
H. SAKATA e t
al.
Perhaps the most unusual and puzzling neurons in area 5 were those we termed 'matching' cells. They were driven maximally by bringing two separate parts of the body into contact. We considered both joint positioning and skin contact to be essential for the maximal activation of this type of cell, for even a simultaneous stimulation of the two corresponding regions o f skin was much less effective when they were separated than when the skin contact occurred as two parts were brought close together by a certain combination of joint positions. The specification o f individual components of the 'best' stimulation was much more difficult than with less complicated neurons and was not complete in the present study. Nevertheless, it may be emphasized that these neurons were hardly drivable at all unless we applied those highly complicated patterns of stimulation. (2) Input to area 5 neurons
There are good anatomical grounds to believe that all these topographic and submodality convergences within the somesthetic domain may occur in area 5. The recent studies of Jones and Powell ~s and Pandya and Kuypers 3s demonstrated strong cortico-cortical projections from all 3 cytoarchitectonic subdivisions of the S I (areas 3, 1 and 2) to area 5. They also showed that area 5 receives interhemispheric connections from the contralateral area 5 as well as the contralateral S I, which contrasts with the lack of such interhemispheric connections between major parts of the S I, the hand and foot regions29, 39. It is obvious, therefore, that a major portion of the somesthetic input to area 5 has undergone previous processing in the S I zs. One piece of evidence to support this hypothesis is that the ratio of skin directional neurons to the non-directional neurons was much higher in area 5 than in the S I. Even in the joint and skin neurons we often observed directional selectivity for the cutaneous stimulation. As already mentioned, directionally selective neurons are relatively rare in the S I and differ from the majority in that they suggest peculiar cortica! processing ~4. I f these neurons are pyramidal cells of layer III which give origin to the association fibers 5~, the same type of neuron may be expected to be more c o m m o n in area 5 than the non-directional type which do not show any obvious sign of cortical processing. Our observations are in good agreement with the anatomical evidence that there is no projection from the S II to area 5 zs, for we found that neither noxious nor auditory stimulation had any effect on area 5 neurons as fas as we could test them. Moreover, the bilaterally symmetrical receptive fields of cutaneous neurons, which are characteristic of S II/r in primates 5~, were seldom observed in area 5. Thus, recent anatomical studies and the present study o f single neurons coincide with the view that area 5 is a higher stage of information processing in the lemniscal system. We also observed some neurons in area 5 which responded to certain visual as well as to somesthetic stimuli 45. Although our observations are still too anecdotal to describe the characteristics of this type of neuron, it is obvious that we have to take into consideration the visual input to area 5. One of the most plausible anatomical connections for this input is the thalamocortieal projection from the nucleus lateralis posterior (LP), which is known to receive visual input 1°,12,22.
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(3) Functional role o f area 5
Hitherto, the function of the parietal association cortex has been better known through clinical studies of the parietal lobe syndrome than from studies in experimental animals. The term 'parietal lobe syndrome' covers a wide range of neurological observations, from relatively simple disorders of tactile functions (astereognosis, etc.) to the disorders of language and symbolic thought 13. However, most of the dramatic symptoms such as finger agnosia, acalculia, agraphia and alexia are related to areas 39 and 40 of Brodmann (rather than areas 5 and 7) which are not thought to have a distinct counterpart in the monkey brain. On the other hand, most of the ablation studies of the posterior parietal cortex in monkeys were mainly concerned with the deficits in tactile discrimination capacity for geometrical shape 5,2°,33,4~, for exploratory behavior and for orientation in space16, 20. The latter two deficits resemble some of the abnormalities that occur in the syndrome of 'amorphosynthesis' in the human subject with a parietal lesion of the non-dominant hemisphere ~,lv. The characteristics of area 5 neurons demonstrated in the present investigation provide some material for speculation upon the functional role of this area in perceptual processes. For example, the joint combination units might be regarded as some stage of a 'recoding' process between a level at which separate information of the position of individual joints is represented and that at which spatial position of a segment of the body is represented. This is likely to be a necessary step leading to the holistic concept of the body image. On the other hand, 'joint and skin' neurons may illustrate an essential process for the extraction of the 3-dimensional features of the object, because the sensory information of the cutaneous afferents alone is limited to the 2-dimensional plane. Moreover, some neurons of this type (especially those related to the shoulder) may give rise to the neural code of the spatial position of the tactile object relative to the body axis. At least they seem to delimit the range of 3-dimensional space within which the tactile stimulus is effective. Thus it is possible that the somesthetic information in such a code is directly correlated with visual information concerning extrapersonal space within the reach of the animal hand, and vice versa. We consider that the direct comparison of the visual and somesthetic information is essential for the perception of posture and the movement of the body as well as the control of movement projected into space. As to the 'matching' units, one may regard them as representing certain aspects of the body form somewhat more solid than joint combination units, although this does not exclude the possibility that they may be related to certain features of external objects held between two parts of the body. Finally, the present study has drawn attention to the differences between areas 5 and 7. Although the ablation experiments failed to prove any clear differences between the two, stimulation experiments of this region showed a difference in evoked movements21,sa; namely, the stimulation of area 5 elicited some bodily movements, while mainly eye movements were elicited in area 7. Moreover, area 5 may represent the 'supplementary sensory area' described in man by Penfield and Jasper, ~,41 and in the squirrel monkey by Blomquist and Lorenzini 4. This seems compatible with our observation that a majority of area 5 neurons responded only to somesthetic stimula-
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tion. Even the relatively rare n e u r o n s which we c o u l d activate visually were m o r e p o w e r f u l l y driven b y somesthetic stimuli. O n the o t h e r hand, some single unit studies o f a r e a 7 m a d e in c h l o r a l o s e d cats revealed clear visual responses 18, whereas there is no such evidence for somesthetic driving in a r e a 7. This is in g o o d a g r e e m e n t with the a n a t o m i c a l study o f Jones a n d Powell 3°, which showed the l a c k o f direct p r o j e c t i o n f r o m the S I to a r e a 7, b u t a o n e - w a y p r o j e c t i o n f r o m a r e a 5 to a r e a 7, suggesting t h a t a r e a 7 is higher in the h i e r a r c h y o f n e o c o r t i c a l processing. O u r o b s e r v a t i o n is in c o n t r a s t with the previous studies o n e v o k e d p o t e n t i a l in c h l o r a l o s e d o r curarized animalsS,10,49, 5° which showed p o l y s e n s o r y (somesthetic, visual a n d a u d i t o r y ) convergence in a s s o c i a t i o n areas in general. I n this respect, a r e a 5 is c o m p a r a b l e to the i n f e r o t e m p o r a l cortex which seems to be specifically c o n c e r n e d with visual p e r c e p t i o n as suggested b y the results o f a b l a t i o n studiesal, z2 as well as those o f a recent single unit study 23. ACKNOWLEDGEMENTS
The first p a r t o f this investigation was d o n e in the D e p a r t m e n t o f N e u r o physiology, The P r i m a t e R e s e a r c h Institute, K y o t o University. T h e a u t h o r s wish to t h a n k Drs. T. T o k i z a n e a n d K. K u b o t a o f t h a t d e p a r t m e n t for their generous s u p p o r t a n d e n c o u r a g e m e n t . The a u t h o r s also express their deep a p p r e c i a t i o n to Dr. V. B. M o u n t c a s t l e for his review a n d helpful criticism o f the m a n u s c r i p t . Finally, they are m o s t grateful to Mrs. R. A j i o k a for her histological assistance.
REFERENCES 1 AMAS$IAN,V. E., Studies on organization of a somesthetic association area, including a single unit analysis, J. NeurophysioL, 17 (1954) 539-585. 2 ALBE-FESSARD,D., ROCHA-MIRANDA,C., ET OSWALDO-CRUZ,E., Activit6s d'origine somesth6sique 6voqu6es au niveau du cortex non-sp6cifique et du centre m6dian du thalamus chez le singe anesth6si6 au chloralose, Electroenceph. clin. Neurophysiol., 11 (1959) 777-787. 3 BARLOW, H. B., Trigger features, adaptation and economy of impulse. In K. N. LEtaOVrC (Ed.), Information Processing in the Nervous System, Springer, Berlin, 1969, pp. 209-230. 4 BLOMQUIST,A. J., AND LORENZINI, C. A., Projection of dorsal roots and sensory nerves to cortical sensory motor regions of the squirrel monkey, J. Neurophysiol., 28 (1965) 1195-1205. 5 BLUM,J. S., CHOW, K. L., AND PRIBRAM, K. H., A behavioral analysis of the organization of the parieto-temporo-preoccipitalcortex, J. comp. Neurol., 93 (1950) 53-100. 6 BRODMANN,K., Beitr~ige zur histologischen Lokalization der Grosshirnrinde. Dritte Mitteilung: Die Rindenfelder der niedren Affen, J. Psychol. NearoL (Lpz.), 4 (1905) 177-226. 7 BURCHFIEL, J. L., AND DUFFY, F. H., Muscle afferent input to single cells in primate somatosensory cortex, Brain Research, 45 (1972) 241-246. 8 BUSER, P., AND BIGNALL, K. E., Nonprimary sensory projections on the cat neocortex, Int. Rev. Neurobiol., 10 (1967) 111-165. 9 BUSER, P., ET BORENSTEIN, P., R6ponses somesth6siques visuelles et auditives recueillies au niveau du cortex 'associatif' suprasylvien chez le chat curaris6 non anesth6si6, Electroenceph. clin. NeurophysioL, 11 (1959) 285-304. 10 BUSER, P., BORENSTEIN,P., ET BRUNER, J., Etude des syst~mes 'associatifs' visuels at auditifs chez le chat anesth6si6 au chloralose, Electroenceph. clin. Neurophysiol., 11 (1959) 305-324. 11 CHOW, K. L., AND HUTT, P. J., The 'association cortex' of Macaca mulatta, a review of recent contributions to its anatomy and function, Brain, 76 (1953) 625-677.
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12 CLARE, M. H., LANDAU, W. M., AND BISHOP, G. H., The relationship of optic fiber groups activated by electrical stimulation to the consequent central postsynaptic events, Exp. Neurol., 24 (1969) 400~20. 13 CRITCHLEY,M., The Parietal Lobe, Edward Arnold, London, 1953. 14 CROSBY, E. C., HUMPHREY, T., AND LAUER, E. W., Correlative Anatomy of the Nervous System, Macmillan, New York, 1962, pp. 449-451. 15 DENNY-BROWN,D., AND BANKER,B., Amorphosynthesis from left parietal lesion, Arch. Neurol. Psychiat. (Chic.), 71 (1954) 302-313. 16 DENNY-BROWN,D., AND CHAMBERS,R. A., The parietal lobe and behavior, Res. PubL Ass. herr. ment. Dis., 36 (1958) 35-117. 17 DENNY-BROWN, D., MEYER, J.S., AND HORESTEIN, S., The significance of perceptual rivalry resulting from parietal lesion, Brain, 75 (1952) 433-471. 18 Dow, B. M., AND DUBNER, R., Single-unit responses to moving visual stimuli in middle suprasylvian gyrus of the cat, J. Neurophysiol., 34 (1970) 47-55. 19 DUEEY, F . H . , AND BURCHFIEL, J.L., Somatosensory system: Organizational hierarchy from single unit in monkey area 5, Science, 172 (1971) 273-275. 20 ETTLINCER, G., AND KALSBECK,J.E., Change in tactile discrimination and in visual reaching after successive and simultaneous bilateral posterior parietal ablations in the monkey, J. Neurol. Neurosurg. Psychiat., 25 (1962) 256-268. 21 FLEralNO, J. F. R., AND CROSBY,E. C., The parietal lobe as an additional motor area: The motor effects of electrical stimulation and ablation of cortical area 5 and 7 in monkeys, J. comp. Neurol., 103 (1955) 485-512. 22 GODFRAIND,J. M., MEULDERS, M., AND VERAART,C., Visual properties of neurons in pulvinar, nucleus lateralis posterior and nucleus supra-geniculatus thalami in the cat, I. Qualitative investigation, Brain Research, 44 (1972) 503-526. 23 GROSS, C. G., ROCHA-MIRANDA,C. E., AND BENDER, D. B., Visual properties of neurons in inferotemporal cortex of the macaque, J. Neurophysiol., 35 (1972) 96-111. 24 HASSLER, R., UND MUHS-KLEMENT, K., Architektonischer Auibau des sensomotorischen und parietalen Cortex der Katze, J. Hirnforsch., 6 (1964) 377-420. 25 HECAEN,H., PENFIELD,W., AND MALMO, R., The syndrome of apractognosia due to lesion of the minor cerebral hemisphere, Arch. NeuroL Psychiat. (Chic.), 75 (1956) 400-434. 26 HUBEL, D. H., AND WIESEL, T. N., Receptive fields, binocular interaction and functional architecture in the cat's visual cortex, J. Physiol. (Lond.), 160 (1962) 106-154. 27 HUBEL, D. H., AND WIESEL,T. N., Receptive fields and functional architecture in two non-striate visual areas (18 and 19) of the cat, J. Neurophysiol., 28 (1965) 229-289. 28 JONES, E. G., AND POWELL, T. P. S., Connections of the somatic sensory cortex of the rhesus monkey. I. Ipsilateral cortical connections, Brain, 92 (1969) 477-502. 29 JONES, E. G., AND POWELL, T. P. S., Connections of the somatic sensory cortex of the rhesus monkey. II. Contralateral cortical connections, Brain, 92 (1969) 717-730. 30 JONES,E. G,, AND POWELL, T. P. S., An anatomical study of converging sensory pathways within the cerebral cortex of the monkey, Brain, 93 (1970) 798-821. 31 MtSHKIN, M., Visual mechanisms beyond the striate cortex. In R. RUSSELL (Ed.), Frontiers of Physiological Psychology, Academic Press, New York, 1966, pp. 93-119. 32 MISHKIN,M., AND PRIBRAM,K. H., Visual discrimination performance following partial ablation of the temporal lobe. I. Ventral vs. lateral, J. comp. physiol. Psychol., 47 (1954) 14-20. 33 MOFEETT,A., ETTLINGER,G., MORTON, a . B., AND PIERCY, M. F., Tactile discrimination performance in the monkey: the effect of ablation of various subdivisions of posterior parietal cortex, Cortex, 3 (1967) 59-96. 34 MOUNTCASTLE,V.B., Modality and topographic properties of single neurons of cat somatic sensory cortex, J. Neurophysiol., 20 (1957) 408-434. 35 MOUNTCASTLE,V. B., The problem of sensing and the neural coding of sensory events. In G. C. QUARTON, T. MELNECHUKAND F. O. SCHMIT(Eds.), The Neurosciences, Rockefeller Univ. Press, New York, 1967, pp. 393-407. 36 MOUNTCASTLE,V.B., AND POWELL, T. P. S., Central nervous mechanisms subserving position sense and kinesthesia, Bull. Johns Itopk. ttosp., 105 (1959) 173-200. 37 MOUNTCASTLE, V.B., TALBOT, W.H., SAKATA, H., AND HYVARINEN, J., Cortical neuronal mechanisms in flutter vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination, J. Neurophysiol., 32 (1969) 452-484.
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38 PANDYA, D. N., AND KUYPERS, H. G. J. M., Cortico-cortical connections in the rhesus monkey, Brabt Research, 13 (1969) 13-36. 39 PANDYA, D. N., AND VIGNOLO, L.A., Interhemispheric projections of the parietal lobe in the rhesus monkey, Brain Research, 15 (1969) 49-65. 40 PEELE, T. L., Acute and chronic parietal lobe ablation in monkeys, J. Neurophysiol., 7 (1944) 269-286. 41 PEN1HELD, W., AND JASPER, H., Epilepsy and the Functional Anatomy of the Human Brain, Little, Brown, Boston, 1954. 42 POWELL, T. P. S., AND MOUNTCASTLE, V. B., The cytoarchitecture of the postcentral gyrus of the monkey Macaca mulatta, Bull. Johns Hopk. Hosp., 105 (1959) 108-131. 43 POWELL, T. P. S., AND MOUNTCASTLE,V. B., Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey, a correlation of findings obtained in a single unit analysis with cytoarchitecture, Bull. Johns Hopk. Hosp., 105 (1959) 133-162. 44 RucH, T. C., FULTON, J. F., AND GERMAN, W. J., Sensory discrimination in monkey, chimpanzee and man after lesions of the parietal lobe, Arch. NeuroL Psychiat. (Chicago), 39 0938) 919-938. 45 SAKATA, H., Somatic sensory responses of neurons in the parietal association area (area 5) of monkeys. In H. H. KORNHUBER(Ed.), Somatosensory System, Georg Thieme, Stuttgart, (in press). 46 SAKATA, H., KAWARASAKI, A., AND SHIBUTANI, H., Functional organization of the parietal association area (area 5) related to the somatic sensation, Jap. J. Physiol., 33 (1971) 445-446. 47 SAKATA, H., AND TAKAOKA, Y., Somatic sensory response of neurons in the parietal association area of monkeys, Jap. J. Physiol., 32 (1970) 403-404. 48 SCHWARZ, D. W. F., AND FREDRICKSON, J . M . , Tactile directional sensitivity of area 2 oral neurons in the rhesus monkey cortex, Brain Research, 27 (1971) 397-401. 49 THOMPSON, R. F., JOHNSON, R. H., AND HOOPES, J. J., Organization of auditory, somatic sensory and visual projection to association fields of cerebral cortex in the cat, J. Neurophysiol., 26 (1963) 343-364. 50 THOMPSON, R. F., SMITH, H. E., AND BLISS, D., Auditory, somatic sensory and visual response interactions in association and primary cortical fields of the cat, J. Neurophysiol., 26 (1963) 365-378. 51 VOLT, /~.., UND VOCT, O., Allgemeinere Ergebnisse unserer Hirnforschung. Vierte Mitteilung: Die physiologische Bedeutung der architektonischen Rindenfelderung auf Grund neuer Rindenreizungen. J. Psychol. Neurol. (Lpz.), 25 (1919) 279-462. 52 WERNER, G., The topology of the body representation in the somatic afferent pathway. In F. O. SCHMITT (Ed.): The Neurosciences, Second Study Program, Rockefeller Univ. Press, New York, 1971, pp. 605-629. 53 WHITSEL, B. L., PETRUCELLI, L. M., AND WERNER, G., Symmetry and connectivity of the map of the body surface in somatosensory area II, J. Neurophysiol., 32 (1969) 170-183. 54 WmTSEL, B. L., ROPPOLO, J. R., AND WERNER, G., Cortical information processing of stimulus motion on primate skin, J. Neurophysiol., 35 (1972) 691-717.
S O M A T O S E N S O R Y P R O P E R T I E S OF N E U R O N S I N T H E P A R I E T A L C O R T E X ( A R E A 5) OF T H E RHESUS M O N K E Y
85
SUPERIOR
HIDEO SAKATA*, YOSHIO TAKAOKA* *, ATSUSHI KAWARASAKI** * AND HIDETOSHI SHIBUTANI* *** Department of Physiology, Osaka City University Medical School, Asahimachi Abenoku, Osaka (Japan)
(Accepted June 8th, 1973)
SUMMARY The response of individual neurons within Brodmann's area 5 of the parietal lobe to physiological somesthetic stimuli was studied in unanesthetized rhesus monkeys. Most neurons were sensitive to light mechanical stimulation of the skin and deep tissue and/or joint rotation. These neurons were distinguishable from those of the primary somatosensory area by several characteristics: multiple joint interaction, ipsilateral receptive field, bilateral interaction, interaction between forelimb and hindlimb or trunk, and excitatory interaction of joint and skin stimuli. Some were highly selective, in that they responded only to certain critical patterns of stimuli involving both joint and skin. The results were viewed as supporting the hypothesis that area 5 is the site of higher order processing of somesthetic information received from the lemniscal system, and may give rise to the neural code of position and form of body and tactile objects in 3-dimensional space.
INTRODUCTION Recent neurophysiological investigations in the somatosensory system concerning the neuronal mechanisms of sensory coding have indicated that the sensory information encoded in the peripheral afferents is transmitted and reproduced in the primary somatosensory cortex (S I) with considerable fidelity, both in its temporal and * Present address: Tokyo Metropolitan Institute for Neurosciences, Fuchu-city, Tokyo 183. ** Present address: Department of Neurosurgery, Nagoya University. *** Present address: Department of Neurosurgery, Osaka City University. * * * * Present address: Osaka Electro-Communication University.
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topographic patterns35, 52. Moreover, correlative studies of psychophysics and electrophysiology suggest that, for certain simple aspects of somesthesia, the neural events in the cortex are closely related to the subjective sensory events3'5, 3v. These findings contrast with recent ones in the visual system, where there appears to be a drastic modification of the sensory messages between the periphery and the primary visual cortex, suggesting that the visual cortex may occupy a more advanced stage of hierarchical processing than does the primary somatic sensory cortex26;"v. In recent experiments in unanesthetized monkeys, a few neurons in the S I were found to be sensitive to the direction of movement of a cutaneous stimulus, a property not possessed by primary afferents. This opens the possibility that a further processing or elaboration of its input may occur in the S I z7,48,54. However, these neurons are relatively rare in the S i, and no other form of elaborate processing has yet been found. This stimulated us to initiate a study of neural activity beyond the level of the S I, to survey the cortical mechanism of somesthetic perception in areas in which a further hierarchical processing of somatic sensory input may occur. The posterior parietal cortex (areas 5 and 7) has long been known to be concerned with the perception of tactile objects, body form and extrapersonal space11,14. This has been suggested by ablation experiments in monkeysS,16,~0,3a,40, 4~, and by clinical studies of the 'parietal lobe syndrome '~3. Although certain aspects of these functions are related to vision as well as to somesthesia, and the location and extent of lesions are difficult to specify precisely in both ablation experiments and in humans with brain injury, there is strong evidence that this region is the site of higher-order processing of somatosensory information. Indeed, recent anatomical studies of corticocortical connections have demonstrated a heavy projection from the S I to area 5~s,3s. In the present work we have studied some of the response characteristics of area 5 neurons to physiological somesthetic stimulation. The results suggest that such a high-order processing occurs in area 5, and that it may be related to tactile pattern recognition. These results have been the subjects of previous notes 45-47, and are in basic agreement with those described recently in the short communication by Duffy and Burchfie119. METHODS
Twenty experiments were done in monkeys, Macaca mulatta, weighing between 2.8 and 5.5 kg. On the day before the start of recording, the metal chamber of the microdrive, as well as the tracheal cannula, was implanted under pentobarbital sodium anesthesia. The skull was exposed, and a trephine hole about 2 cm in diameter was made, centered over the superior parietal lobule. Usually, both the central sulcus and the intraparieta! sulcus could be seen through the dura, which was left intact, and they were used as landmarks for placing the chamber. The latter was fixed to the skull with screws and dental cement, and was sealed water-tight with dental impression compound. After being filled with mineral oil the chamber was covered with an acrylite cap packed with silicone rubber. The tracheal cannula was an L-shaped non-kinking rubber tubing for pediatric anesthesia trimmed short and at-
SOMATOSENSORY PROPERTIES OF AREA 5 NEURONS
87
tached with a small collar for suturing to the skin. The trachea was truncated beneath the larynx, and the cannula was introduced into its distal end and then sutured to the skin of the neck; the skin was in turn sutured to the periostium of the sternum to get a good fixation. All skin incisions were sutured so that no operational procedure was left except for the excision of dura. The latter was proved to be pain-free, for no dilatation of the pupils or piloerection was observed during dural incision. On the morning of the experiment the animal was immobilized with Flaxedil, injected intraperitoneally (8 mg/kg). As soon as the monkey showed difficulty in breathing, the tracheal cannula was connected to the respirator. End-tidal CO2 was adjusted between 3.5 and 4 . 0 ~ , and rectal temperature was kept at a normal level throughout the experiment. The chamber was fixed to a metal frame by a 4-mm screw passing into a tapped hole in an arm of the chamber. The animal was seated on a small padded bench and kept in the upright position, which allowed freedom to manipulate all 4 limbs and the trunk. Usually, the animal remained in good condition for more then 24 h, but we took an intermission of several hours at night, as the E E G showed a drowsy pattern toward midnight, and responsiveness of area 5 neurons tended to decline along with increasing somnolence of the animal. After excision of the dura, mapping of the surface-evoked potential was made in the S I to get some idea of somatotopical location of area 5, assuming the latter might correspond approximately to that of the S I in the same sagittal plane. A modified Davis micromanipulator with a glass plate was fixed with 3 metal clamps and sealed hydraulically with a packing ring of silicone rubber. The sites of penetration were determined under microscopic observation and were noted on an enlarged photograph of the exposed cortex. The microelectrodes were electrolytically sharpened tungsten wire 125 # m in diameter and insulated with polyurethane lacquer. The impedance was adjusted between 3 and 10 M ~ at 1000 Hz by passing negative current in saline under the microscope, to break the insulation up to 10-20 # m from the tip. The electrical signs of impulses in neurons were recorded from an extracellular position via a conventional pre-amplifier and CRT, with the aid of a differential amplitude discriminator. All data were stored on magnetic tape. In 7 later experiments, post-stimulus time (PST) histograms were made with the averaging computer (ATAC501, Nihonkohden) summing 10-20 trials. Stimulation was mostly applied manually, except for sine-wave oscillations generated by a mechanical vibratory stimulator and delivered to the skin. For light deformation of the skin, fingers or acrylite cylinder and plate were used as well as glass probes. Joint rotation was also applied manually; we checked carefully the effect of deformation of adjacent skin and deep tissue. The cooperation of two experimenters was sometimes necessary to test the interlimb interaction or other complicated patterns of stimulation. Usually, the onset and end of stimulation were registered with a microswitch. Sometimes, we used a potentiometer to measure the joint movement.
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Histological method At the end of each experiment a guide wire was inserted through the microdrive into the brain to indicate the orientation of penetrations, and the brain was removed and fixed in 10 % formalin. Serial celloidin sections 50/~m thick were stained with thionine. The surface of the section was made vertical to the axis of the superior parietal lobule so as to be suitable for cytoarchitectural study. Identification of electrode track and depth of recording was facilitated by the electrolytic lesion by passing negative current of 5/~A for 5-10 sec through the electrode tip. The cortex through which the electrode passed was classified according to the cytoarchitectonic criteria of Brodmann 6. The boundary between areas 2 and 5 was most clearly indicated by the change of thickness of layer III as described by Powell and Mountcastle 42 in rhesus monkeys, and by Hassler and Muhs-Klement 24 in cats. Sites of unit recording were plotted on tracings of histological sections at a magnification of × 20. Shrinkage of the brain was found to be negligible with the use of acetic acid-ethanol mixture as a mordant.
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Fig. 1. Upper: lateral view of cerebral hemisphere of Macaca mulatta showing site of lower drawing. Lower: site of entry of electrode penetrations. Filled circles: penetrations passed through area 5. Open circles: penetrations entered area 2 on the surface and passed into area 5 in the depth diagonally. Filled triangles: penetration in area 2. The boundary of Brodmann's area is indicated by dotted lines. CS, central sulcus; PCS, postcentral sulcus; LF, lateral fissure; STS, superior temporal sulcus; IPS, intraparietal sulcus; LS, lunate sulcus.
89
S O M A T O S E N S O R Y P R O P E R T I E S OF A R E A 5 N E U R O N S
RESULTS
(1) General response characteristics o f area 5 neurons Sixty microelectrode penetrations were directed to traverse Brodmann's area 5 in the superior parietal lobule, a triangular region between the postcentral and intraparietal sulci including the anterior bank of the latter sulcus. Another 10 penetrations were made in the posterior part of the postcentral gyrus to study neurons in area 2 for comparison. Four hundred and seventy-seven neurons were isolated and studied in sufficient detail to allow a definition of the adequate stimuli for excitation of each. In those penetrations for which precise histological identifications of electrode penetration in regard to cytoarchitectonic boundaries were made, 245 neurons were located in area 5, and 54 in area 2. The site of entry of 43 penetrations in which these area 5 neurons were recorded is shown in Fig. ! including those that passed through area 2 on the surface to reach the buried portion of area 5. In general, neurons of area 5 were activated by physiological somesthetic stimuli, although most of them were not sensitive to stationary point stimulation of skin and deep tissue, in contrast with those of the S I. The adequate stimulus was often a complicated pattern of touch and joint rotation, rather than a simple localized stimulus of one or another submodality. We have classified area 5 neurons into 6 categories, as shown in Table I. We assumed that the responses to the light tactile stimuli we used were cutaneous in origin, when there was no evidence to indicate additional driving by stimulation of deep tissue, and that driving by joint rotation or position was related to the joint afferents. However, the criteria were operational and somewhat arbitrary, so that this does not exclude the possible participation o f other afferent inputs, including the muscle afferents. Class 1 and 2 neurons are those that were activated by superficial tactile stimulation of the skin without any modification by joint positioning. Neurons of class 1 displayed directional selectivity similar to that of cells of the S 137,48,53; neurons of class 2 showed no directional sensitivity. Class 3 is composed of a group of neurons activated by the rotation of a single joint, and therefore comparable to the joint
TABLE I CLASSIFICATION OF AREA 5 NEURONS
Contralateral lpsilateral Class 1 - Class 2 - Class 3 - Class 4 - Class 5 - Class 6 - Total
%
Skin (directional) Skin (non-directional) Joint (single) Joint (combination) Deep - - others Joint and skin
Bilateral
Total
13 10 29 35 5 50
1 2 13 I0 0 12
8 2 -18 10 27
22 14 42 63 15 89
142
38
65
245
15.5
26.5
58.0
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H. SAKATAet al.
90
neurons in the S I ~6` except that many were activated by rotation of the ipsilateral joint. Class 4 neurons are those that showed interactions of two or more joints so that certain combinations of joint rotation and/or position were necessary for optimal driving. Class 5 are the neurons activated by stimulation o f subcutaneous tissues other than the joints. Class 6 includes all those neurons in which various types of interaction between joint rotation and skin stimulation were observed. As a whole, joint input seems to be predominant in area 5, for class 3 plus class 4 made up 42.9 and class 6 (mixed type) 36.3 ~ . Skin neurons (class 1 plus 2) were only 14.7 ~. These percentages do not necessarily represent the true distribution of neuronal types in the total population in area 5, for we passed over many unclassified neurons not listed in here.
(2) Skin neurons (directional or non-directional) Neurons in area 5 that were activated only by cutaneous stimulation did not show any striking differences from the skin neurons in the S I. However, they usually had wider receptive fields than do S I neurons, and bilateral receptive fields as well as ipsilateral receptive fields were observed. Moreover, directional selectivity was observed in nearly two-thirds (22/36) of these area 5 neurons, a proportion much greater than in the S I. Fig. 2 illustrates one such neuron with bilateral receptive fields. Directional selectivity was very prominent: gentle rubbing of the skin from left to right elicited a vigorous continuous discharge, whereas the opposite movement from right to left produced minimal response or even suppression of spontaneous discharge. Most of the non-directional skin neurons were also difficult to drive by stationary pressure or vibration. Their sensitivity to moving stimulation was similar to that of neurons in the rostral part o f the second somatic sensory area (S II/r) 53, but none of them had the bilaterally symmetrical receptive field found for S II neurons.
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Fig. 2. Receptive field and responses of an area 5 neuron that showed directional selectivity to the moving cutaneous stimulation. Upper and lower traces are the discharges of the neuron during consecutive trials of stimulation applied in the middle part of receptive field shown in the left drawing. Direction and timing of stimulus is indicated by horizontal bars below the trace: L -+ R, left to right, R -+ L, right to left. Negativity is upward in this and following records of impulses.
SOMATOSENSORY PROPERTIES OF AREA 5 NEURONS
91
Wrist
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Fig. 3. Responses of an area 5 neuron during 4 sequences of rotations and positionings of ipsilateral wrist and elbow, as indicated on two drawings on the left. A: elbow flexion was superimposed on steady wrist flexion. B: elbow flexion during steady wrist extension. C: wrist flexion during steady elbow flexion. D: wrist flexion during steady elbow extension. Horizontal bars indicate the rotation of the second joint; the joint was moved during the initial several hundred msec and then maintained in the end position.
(3) Joint combination neurons Various types o f interaction o f multiple joint rotations were observed in 63 neurons belonging to this class. Fig. 3 illustrates a typical example o f this class o f neuron, which was related to b o t h wrist and elbow o f the ipsilateral side. In this example either the wrist or the elbow was m o v e d while the other joint was fixed in a certain position. Elbow flexion elicited a sustained response when the wrist was fixed in the flexed position (Fig. 3A). On the other hand, very little response was evoked by the same movement o f the elbow when the wrist was kept extended (Fig. 3B). Likewise, wrist flexion elicited a g o o d response if the elbow was flexed (Fig. 3C), but almost no response if the elbow was extended (Fig. 3D). Therefore, the best response was obtained with a combination o f wrist flexion and elbow flexion. The m o r e peculiar examples were neurons that were maximally activated by the bilateral interaction o f joints, as illustrated in Fig. 4. Of course, it is difficult to prove that the simultaneous rotation o f joints on both sides is prerequisite for maximal activation o f the neuron, for there are so m a n y possible contaminating stimuli during such a movement. However, we excluded such stimuli carefully, especially the effect o f rotation or bending o f the backbone and neck. Indeed, we identified 8 neurons driven by the latter stimulation. In Fig. 4 the discharge o f a neuron is shown in a sequential time histogram. The 'best' stimulus for this unit was a parallel rotation o f both arms f r o m right to left (sketch on the left). The vigorous discharge produced
H. SAKATAet al.
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Fig. 4. Response of an area 5 neuron to bilateral shoulder rotations, displayed in impulse time histograms. Upper: response to parallel rotation of left and right arms to the left as shown in the insert drawing. Middle: separate rotation of right arm (inner rotation of right shoulder). Lower: separate rotation of left arm (outer rotation of left shoulder). Ordinate is number of impulse, abscissa time in sec, bin size 100 msec. Joint rotation is indicated by arrow and steady positioning by dotted line above each histogram. R, about 60° to the right; L, about 60° to the left.
by this movement, and the considerable duration of the sustained discharge when the arms were held towards the left side are shown in the upper histogram. Apparently the main components were the inner rotation of the right shoulder and outer rotation of the left shoulder, while the angle of elbow or wrist did not modify the response of this unit. On the other hand, separate rotation of either arm was much less effective, as the inner rotation of the right shoulder alone elicited only a small discharge (second graph), and the outer rotation of the left shoulder evoked no response (third graph). We found many joint combinations other than those illustrated here, and some of them showed summation rather than antagonistic interaction of two or more joints. Moreover, some neurons were activated in a narrow range of intermediate joint angle rather than at the extremes of rotation.
(4) Joint and skin units The interaction of joint rotation and skin stimulation was characteristic of some neurons of area 5. The degree of complexity of the maximally effective stimulus combination varied greatly for different neurons. Fig. 5 shows one of the simplest types of interaction; i.e., the combination of elbow flexion and stimulation of the skin on the back of the hand of the contralateral side. As illustrated in the upper trace, elbow flexion alone elicited only a limited and unstable response. The response to the rubbing of the skin of the dorsum of the hand was also relatively
93
SOMATOSENSORY PROPERTIES OF AREA 5 NEURONS
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Fig. 5. Response of an area 5 neuron which showed excitatory interaction of joint rotation and cutaneous stimulation. Upper trace: discharges of unit during contralateral elbow flexion. Middle trace: response to a moving cutaneous stimulation on the back of contralateral hand. Lower trace: response to simultaneous elbow flexion and cutaneous stimulation, as indicated in the left drawing. The joint was moved slowly during the period indicated by horizontal bars.
weak (second trace). The combination of elbow and skin stimulation, however, elicited a vigorous response (third trace). In some cases, the effect of joint rotation was marked even in the steady position, as illustrated in Fig. 6. The 'best' response of this neuron was obtained by the gentle moving stimulus on the skin of the contralateral forearm in the direction from proximal to distal, with the shoulder adducted, as shown in the PST histogram on the left. A cutaneous stimulus moving in the opposite direction, with the shoulder in the same position, produced much less response (middle histo-
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Fig. 6. Effect of antagonistic joint positions upon the response of an area 5 neuron to moving cutaneous stimulation. Each histogram shows the average firing rate of 10 trials. Left histogram: response to cutaneous stimulus moving from proximal to distal on the ventral side of contralateral forearm during steady adduction of the shoulder. Middle histogram: response to the stimulus moving from distal to proximal in the same arm position. Right histogram: cutaneous stimulus from proximal to distal during steady shoulder abduction. A r m position and approximate receptive field is shown in the drawing above each histogram, and the direction and period of cutaneous stimulation is given underneath.
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Fig. 7. Upper: effect of difference in direction of moving cutaneous stimulation upon the response of an area 5 neuron. Each bar indicates the total number of impulse of 10 consecutive trials. Direction and receptive field in the ipsilateral forearm is shown in the drawing on the right; D, distal; P, proximal; M, preaxial; L, postaxial, The arm was held in front of the animal and at 90° to the body axis. Lower: effect of change in arm position upon the response of the same neuron to the moving cutaneous stimulation in the optimal direction (distal to proximal). Each bar indicates the total number of impulses of 10 trials at the angle given on the abscissa. Number of degrees indicates the angle of shoulder rotation from vertical axis pointing below; posterior rotation is marked with a minus sign.
gram). O n the o t h e r hand, a l m o s t no response was elicited when the shoulder was a b d u c t e d even when the skin was s t i m u l a t e d in the o p t i m a l direction ( h i s t o g r a m on the right). Fig. 7 shows a m o r e detailed study o f the effect o f a change in j o i n t p o s i t i o n on a n a r e a 5 n e u r o n which was m a x i m a l l y driven b y m o v i n g c u t a n e o u s s t i m u l a t i o n o f the f o r e a r m in the direction f r o m distal to p r o x i m a l with the shoulder a n t e r i o r l y elevated. The directional selectivity is clearly seen in the u p p e r g r a p h which shows the responses o f this n e u r o n to a c u t a n e o u s stimulus m o v i n g in a n u m b e r o f directions with the a r m fixed in front o f the a n i m a l (90 ° in the lower diagram). The response to the o p t i m a l d i r e c t i o n o f c u t a n e o u s m o v e m e n t was then r e c o r d e d at a n u m b e r o f a r m positions, as shown in the lower graph. The exact angle o f the shoulder was n o t so critical as long as the a r m was raised to some extent (45-135°). The m a x i m a l response o f this n e u r o n was n o t o b t a i n e d at the extreme a n t e r i o r elevation (180°), b u t at some i n t e r m e d i a t e p o s i t i o n (135°). M a r k e d facilitation b y c u t a n e o u s s t i m u l a t i o n was occasionally observed in a n e u r o n t h a t was driven b y a c o m b i n a t i o n o f j o i n t positions, as illustrated in Fig. 8.
95
SOMATOSENSORY PROPERTIES OF AREA 5 NEURONS Impulse/sec
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Fig. 8. Response of an area 5 neuron to bilateral shoulder rotation and its enhancement by skin contact. Left 3 PST histograms depict the responses, from above to below, to ipsilateral shoulder adduction, to contralateral shoulder adduction, and to bilateral shoulder adduction. Right histogram indicates responses to the combination of cutaneous stimulation and bilateral shoulder adduction as shown in the upper drawing. The period of stimulation is given at the bottom; the shoulder was rotated during the initial several hundred msec and then maintained in the end position.
This neuron was driven by shoulder adduction of either the left (ipsilateral) or right side, respectively (upper two histograms on the left), and the simultaneous adduction of both shoulders elicited slightly more discharge than did the separate stimulation (lower left). Marked enhancement of response was observed by adding the skin contact of hands and forearms of both sides to the joint combination (right histogram). The 'best' stimulation was found to be 'rubbing' the forearms and palms of both sides on each other. Therefore, this is a rather peculiar type of joint and skin interaction involving two limbs. The skin receptive field, however, was difficult to determine precisely, because almost no response was elicited by cutaneous stimulation alone. A similar type of highly complicated joint and skin interaction was also found between the forelimb and hindlimb or the limb and trunk in some other neurons. We called these 'matching neurons', because the 'best' stimulus for them was to bring a part of a limb in contact with a part of another limb or the trunk, as if to match two body regions to each other. Fig. 9 shows another example of a matching neuron which responded even more selectively to a specific pattern of stimulation than the neuron
96
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Fig. 9. Response of an area 5 neuron which required a complicated pattern of combination of joint and skin stimulation for optimal driving. Left histogram: PST histogram of 10 trials to depict the response to 'best' stimulus as illustrated in insert drawing; rubbing the ipsilateral forearm in flexed position with contralateral palm and fingers from proximal to distal. Upper right: response to moving cutaneous stimulation on the left forearm from proximal to distal with experimenter's hand. Lower right: response to combined joint rotation imitating 'best' stimulus without contacting two skin regions; left elbow flexion and right elbow flexion with shoulder pronated.
o f Fig. 8. The 'best' stimulation was 'rubbing' the left (ipsilateral) forearm, which was flexed at the elbow, with the right palm and fingers in the direction from proximal to distal (histogram on the left). The cutaneous stimulation on the left forearm did evoke a small discharge (upper right), whereas the stimulation of the right hand elicited no response. The combined joint rotation in the same pattern o f movement as the 'best' stimulation without contacting two areas evoked only a small response (lower right). On the other hand, we confirmed that the right elbow extension had a strong suppressive effect on this neuron. Thus the 'best' stimulus could not be analyzed into individual excitatory components in this case, in contrast to the neuron of Fig. 8. This was often true o f 'matching' neurons, and therefore they were likely to be overlooked as undrivable in earlier experiments. DISCUSSION
(1) Characteristics o f area 5 neurons In contrast with previous observations in anesthetized animals 4a, we found in
SOMATOSENSORY PROPERTIES OF AREA 5 NEURONS
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the present study of unanesthetized monkeys that neurons of area 5 could be driven by natural somesthetic stimulation, if the stimuli were applied in an appropriate manner. The stimulation that activated these neurons was either joint rotation or light mechanical deformation of the skin and deep tissues such as gentle surface movement and steady light pressure. These were most likely to activate low-threshold afferents of joint and skin, suggesting that area 5 is closely related to the primary somatosensory cortex (S I) as far as the submodalities are concerned. On the other hand, a striking difference was found in regard to the spatial configuration of adequate stimuli, i.e., the receptive field organization. In general, the receptive fields of area 5 neurons are much larger than those of S I neurons, and they are not restricted to the contralateral side of the body. A considerable number of neurons showed (1) ipsilateral receptive fields, (2) multiple joint interaction, (3) bilateral interaction, (4) forelimb and hindlimb interaction, and (5) limb and trunk interactions, respectively. This indicated that there was a marked convergence of the input from different parts of the body upon these cells. However, it does not indicate that this convergence is diffuse and non-specific as suggested by previous electrophysiological studies in chloralosed animals l& On the contrary, converging input seems to be subjected to an elaborate processing which may result in higher selectivity in trigger features 3. One of the characteristic types of neuron in area 5 was that which we classified as a 'joint combination' neuron. The response characteristics of these cells were in sharp contrast with those of joint neurons in the S I which respond only to movement of one single joint in one direction a6, although we found several joint combination units located in area 2 or in the transitional zone between areas 2 and 5. There are several possible neural mechanisms underlying this phenomenon. One is the convergence of inhibitory input from some joints upon the excitatory input from others. The second is the convergence of excitatory input from two or more joints. The antagonistic type of interaction is favorable to the first explanation, whereas the summating type of interaction seems to support the second hypothesis. However, it may be more important to exclude the possibility of peripheral mechanical factors which might change the response of primary afferents innervating a single joint, owing to the difference in position or movement of adjacent joints. Besides, the intervention of muscle afferents and other deep receptors must be considered, for Burchfiel and Duffy 7 described some neurons in area 5 that were activated by direct stretch of the muscle. Another distinctive feature of area 5 neurons was the interaction of joint and skin stimulation in exciting them, which suggests a convergence of different submodalities, in contrast with the strict modality segregation in the S 134,43. The only interaction between these two submodalities observed in the S I was the 'skin to joint inhibition' described by Mountcastle and Powell a6. We also observed this type of interaction for an occasional neuron in area 5. Some of this class of neurons showed a marked suppression in certain joint positions, which might be interpreted as 'joint to skin inhibition' (e.g. Fig. 6). However, most of the joint and skin neurons required the simultaneous stimulation of the two for the optimal activation, so that the two components were both excitatory.
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Perhaps the most unusual and puzzling neurons in area 5 were those we termed 'matching' cells. They were driven maximally by bringing two separate parts of the body into contact. We considered both joint positioning and skin contact to be essential for the maximal activation of this type of cell, for even a simultaneous stimulation of the two corresponding regions o f skin was much less effective when they were separated than when the skin contact occurred as two parts were brought close together by a certain combination of joint positions. The specification o f individual components of the 'best' stimulation was much more difficult than with less complicated neurons and was not complete in the present study. Nevertheless, it may be emphasized that these neurons were hardly drivable at all unless we applied those highly complicated patterns of stimulation. (2) Input to area 5 neurons
There are good anatomical grounds to believe that all these topographic and submodality convergences within the somesthetic domain may occur in area 5. The recent studies of Jones and Powell ~s and Pandya and Kuypers 3s demonstrated strong cortico-cortical projections from all 3 cytoarchitectonic subdivisions of the S I (areas 3, 1 and 2) to area 5. They also showed that area 5 receives interhemispheric connections from the contralateral area 5 as well as the contralateral S I, which contrasts with the lack of such interhemispheric connections between major parts of the S I, the hand and foot regions29, 39. It is obvious, therefore, that a major portion of the somesthetic input to area 5 has undergone previous processing in the S I zs. One piece of evidence to support this hypothesis is that the ratio of skin directional neurons to the non-directional neurons was much higher in area 5 than in the S I. Even in the joint and skin neurons we often observed directional selectivity for the cutaneous stimulation. As already mentioned, directionally selective neurons are relatively rare in the S I and differ from the majority in that they suggest peculiar cortica! processing ~4. I f these neurons are pyramidal cells of layer III which give origin to the association fibers 5~, the same type of neuron may be expected to be more c o m m o n in area 5 than the non-directional type which do not show any obvious sign of cortical processing. Our observations are in good agreement with the anatomical evidence that there is no projection from the S II to area 5 zs, for we found that neither noxious nor auditory stimulation had any effect on area 5 neurons as fas as we could test them. Moreover, the bilaterally symmetrical receptive fields of cutaneous neurons, which are characteristic of S II/r in primates 5~, were seldom observed in area 5. Thus, recent anatomical studies and the present study o f single neurons coincide with the view that area 5 is a higher stage of information processing in the lemniscal system. We also observed some neurons in area 5 which responded to certain visual as well as to somesthetic stimuli 45. Although our observations are still too anecdotal to describe the characteristics of this type of neuron, it is obvious that we have to take into consideration the visual input to area 5. One of the most plausible anatomical connections for this input is the thalamocortieal projection from the nucleus lateralis posterior (LP), which is known to receive visual input 1°,12,22.
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(3) Functional role o f area 5
Hitherto, the function of the parietal association cortex has been better known through clinical studies of the parietal lobe syndrome than from studies in experimental animals. The term 'parietal lobe syndrome' covers a wide range of neurological observations, from relatively simple disorders of tactile functions (astereognosis, etc.) to the disorders of language and symbolic thought 13. However, most of the dramatic symptoms such as finger agnosia, acalculia, agraphia and alexia are related to areas 39 and 40 of Brodmann (rather than areas 5 and 7) which are not thought to have a distinct counterpart in the monkey brain. On the other hand, most of the ablation studies of the posterior parietal cortex in monkeys were mainly concerned with the deficits in tactile discrimination capacity for geometrical shape 5,2°,33,4~, for exploratory behavior and for orientation in space16, 20. The latter two deficits resemble some of the abnormalities that occur in the syndrome of 'amorphosynthesis' in the human subject with a parietal lesion of the non-dominant hemisphere ~,lv. The characteristics of area 5 neurons demonstrated in the present investigation provide some material for speculation upon the functional role of this area in perceptual processes. For example, the joint combination units might be regarded as some stage of a 'recoding' process between a level at which separate information of the position of individual joints is represented and that at which spatial position of a segment of the body is represented. This is likely to be a necessary step leading to the holistic concept of the body image. On the other hand, 'joint and skin' neurons may illustrate an essential process for the extraction of the 3-dimensional features of the object, because the sensory information of the cutaneous afferents alone is limited to the 2-dimensional plane. Moreover, some neurons of this type (especially those related to the shoulder) may give rise to the neural code of the spatial position of the tactile object relative to the body axis. At least they seem to delimit the range of 3-dimensional space within which the tactile stimulus is effective. Thus it is possible that the somesthetic information in such a code is directly correlated with visual information concerning extrapersonal space within the reach of the animal hand, and vice versa. We consider that the direct comparison of the visual and somesthetic information is essential for the perception of posture and the movement of the body as well as the control of movement projected into space. As to the 'matching' units, one may regard them as representing certain aspects of the body form somewhat more solid than joint combination units, although this does not exclude the possibility that they may be related to certain features of external objects held between two parts of the body. Finally, the present study has drawn attention to the differences between areas 5 and 7. Although the ablation experiments failed to prove any clear differences between the two, stimulation experiments of this region showed a difference in evoked movements21,sa; namely, the stimulation of area 5 elicited some bodily movements, while mainly eye movements were elicited in area 7. Moreover, area 5 may represent the 'supplementary sensory area' described in man by Penfield and Jasper, ~,41 and in the squirrel monkey by Blomquist and Lorenzini 4. This seems compatible with our observation that a majority of area 5 neurons responded only to somesthetic stimula-
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tion. Even the relatively rare n e u r o n s which we c o u l d activate visually were m o r e p o w e r f u l l y driven b y somesthetic stimuli. O n the o t h e r hand, some single unit studies o f a r e a 7 m a d e in c h l o r a l o s e d cats revealed clear visual responses 18, whereas there is no such evidence for somesthetic driving in a r e a 7. This is in g o o d a g r e e m e n t with the a n a t o m i c a l study o f Jones a n d Powell 3°, which showed the l a c k o f direct p r o j e c t i o n f r o m the S I to a r e a 7, b u t a o n e - w a y p r o j e c t i o n f r o m a r e a 5 to a r e a 7, suggesting t h a t a r e a 7 is higher in the h i e r a r c h y o f n e o c o r t i c a l processing. O u r o b s e r v a t i o n is in c o n t r a s t with the previous studies o n e v o k e d p o t e n t i a l in c h l o r a l o s e d o r curarized animalsS,10,49, 5° which showed p o l y s e n s o r y (somesthetic, visual a n d a u d i t o r y ) convergence in a s s o c i a t i o n areas in general. I n this respect, a r e a 5 is c o m p a r a b l e to the i n f e r o t e m p o r a l cortex which seems to be specifically c o n c e r n e d with visual p e r c e p t i o n as suggested b y the results o f a b l a t i o n studiesal, z2 as well as those o f a recent single unit study 23. ACKNOWLEDGEMENTS
The first p a r t o f this investigation was d o n e in the D e p a r t m e n t o f N e u r o physiology, The P r i m a t e R e s e a r c h Institute, K y o t o University. T h e a u t h o r s wish to t h a n k Drs. T. T o k i z a n e a n d K. K u b o t a o f t h a t d e p a r t m e n t for their generous s u p p o r t a n d e n c o u r a g e m e n t . The a u t h o r s also express their deep a p p r e c i a t i o n to Dr. V. B. M o u n t c a s t l e for his review a n d helpful criticism o f the m a n u s c r i p t . Finally, they are m o s t grateful to Mrs. R. A j i o k a for her histological assistance.
REFERENCES 1 AMAS$IAN,V. E., Studies on organization of a somesthetic association area, including a single unit analysis, J. NeurophysioL, 17 (1954) 539-585. 2 ALBE-FESSARD,D., ROCHA-MIRANDA,C., ET OSWALDO-CRUZ,E., Activit6s d'origine somesth6sique 6voqu6es au niveau du cortex non-sp6cifique et du centre m6dian du thalamus chez le singe anesth6si6 au chloralose, Electroenceph. clin. Neurophysiol., 11 (1959) 777-787. 3 BARLOW, H. B., Trigger features, adaptation and economy of impulse. In K. N. LEtaOVrC (Ed.), Information Processing in the Nervous System, Springer, Berlin, 1969, pp. 209-230. 4 BLOMQUIST,A. J., AND LORENZINI, C. A., Projection of dorsal roots and sensory nerves to cortical sensory motor regions of the squirrel monkey, J. Neurophysiol., 28 (1965) 1195-1205. 5 BLUM,J. S., CHOW, K. L., AND PRIBRAM, K. H., A behavioral analysis of the organization of the parieto-temporo-preoccipitalcortex, J. comp. Neurol., 93 (1950) 53-100. 6 BRODMANN,K., Beitr~ige zur histologischen Lokalization der Grosshirnrinde. Dritte Mitteilung: Die Rindenfelder der niedren Affen, J. Psychol. NearoL (Lpz.), 4 (1905) 177-226. 7 BURCHFIEL, J. L., AND DUFFY, F. H., Muscle afferent input to single cells in primate somatosensory cortex, Brain Research, 45 (1972) 241-246. 8 BUSER, P., AND BIGNALL, K. E., Nonprimary sensory projections on the cat neocortex, Int. Rev. Neurobiol., 10 (1967) 111-165. 9 BUSER, P., ET BORENSTEIN, P., R6ponses somesth6siques visuelles et auditives recueillies au niveau du cortex 'associatif' suprasylvien chez le chat curaris6 non anesth6si6, Electroenceph. clin. NeurophysioL, 11 (1959) 285-304. 10 BUSER, P., BORENSTEIN,P., ET BRUNER, J., Etude des syst~mes 'associatifs' visuels at auditifs chez le chat anesth6si6 au chloralose, Electroenceph. clin. Neurophysiol., 11 (1959) 305-324. 11 CHOW, K. L., AND HUTT, P. J., The 'association cortex' of Macaca mulatta, a review of recent contributions to its anatomy and function, Brain, 76 (1953) 625-677.
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