Brain Research, 105 (1976) 405--422

405

© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands

SOMATOTOPIC L O C A L I Z A T I O N IN CAT M O T O R C O R T E X

A. N I E O U L L O N AND L. RISPAL-PADEL

C.N.R.S.-INP 5, 31, chemin Joseph Aiguier, 13274 Marseille Cedex 2 (France) (Accepted August 26th, 1975)

SUMMARY

Punctate intracortical stimulation of the motor cortex (areas 4 and 6), with parallel observation of the induced movements, permits description of a fine somatotopic organization of the motor control areas for different parts of the musculature in freely moving adult cats. The results show that movements produced by electrical stimulation of the motor cortex are always single and non-repetitive, regardless of the duration and intensity of the stimulation. These movements are restricted to a very precise part of the musculature, and experiments show that this localization is related to the exact position of the tip of the stimulating electrode in the motor cortex. Other experimental data show that motor responses which disturb the animal's equilibrium are accompanied by postural adjustments. Stimulation of the cerebral cortex permits the definition of a separate motor control area for each part of the cat musculature, with an individual control area for each of the joints of the forelimb. This was not possible for the hindlimb, which is always activated in its entirety. These results establish a new representation of the somatotopic organization of the cat motor cortex. This diagram shows that area 6 controls the more axial parts of the musculature, while area 4 controls the proximal and distal parts of the limb muscles. This map was compared to numerous previous data on the somatotopic organization in the cat motor cortex, especially to the map of Woolsey37.

INTRODUCTION

Somatotopic organization of cat motor cortex has been defined to a large extent as a result of experiments on anaesthetized animals, where the stimulating current was applied directly to the surface of the motor cortexS,13,21,2a,as,aT. When maps of the somatotopic organization of the cat's motor cortex from dif-

406 ferent studies are compared many contradictions are evident in the localization of command areas of the different parts of the body musculature. Faced with such divergent results, appreciation of the exact limits of the various motor control areas is difficult. A knowledge of these boundaries is essential in anatomical and physiological research, where such maps are used to define the functional roles of other parts of the nervous system related to motor function. Recently, using intracortical microstimulation, Asanuma and Sakata 5 demonstrated the existence of an extremely fine cortical control of the distal musculature of the forelimb. However, their study is limited to this part of the musculature. It would be of interest to know if such a fine control system also exists for the axial and proximal parts of body musculature. Furthermore, very little research has been done on the somatotopic organization in area 6 of the motor cortex and descriptions of the exact motor sites situated therein lack precision. It would also be interesting to know if electrical stimulation of area 6 produces movements and, if so, what type, and whether a fine somatotopic organization exists in that cortical area. The authors feel that the above-mentioned reasons justify a new study of the somatotopic organization of cortical motor localizations in areas 4 and 6 of the cat cerebral cortex. In our experiments we have benefitted from the results of Asanuma et al. 6 and Sakata and Miyamoto al where muscle contractions were produced by discrete intracortical microstimulation. In our study we stimulated the motor cortex directly using a less discrete stimulus than that of Asanuma. The use of many electrodes in the same awake animal permitted a comparative analysis of the various sites stimulated.

METHODS

Chronic experiments were performed on adult cats. Implantation of electrodes was done under chloralose anaesthesia but the stimulations were carried out only after the effects of the anaesthetic had completely disappeared. In order to stimulate different parts of the motor cortex in the same animal, 15 or 16 electrodes were implanted in the motor cortex through tiny trephine holes 2 m m apart. This technique permits the exploration of the whole of cytoarchitectonic areas 4 and 6 as defined by the maps of Hassler and Muhs-Clement is. The electrodes were implanted perpendicularly to the cortical surface and placed intracortically at a depth of 1.5 mm, which put their tips near the pyramidal cell layer (layer V in area 4). The electrodes used were sharpened nickel-chrome wire, 250/~m in diameter and varnished except at the tip (resistance 50-70 k,Q). Each electrode was cemented to the bone and connected to an electrical socket rigidly attached to the animal's skull. Ten cats were prepared in this manner. The motor cortex of the freely moving cat was stimulated between the two adjacent electrodes; each electrode being successively cathodic and anodic. It was observed that at the level of the implanted electrode tips cathodic stimulation was more

407 effective in exciting cortical cells. This agrees with results obtained by Stoney e t al. a3 and Rispal-Padel and Massion 29. In some experiments, this bipolar stimulation technique was compared with a monopolar one. A cathodic current was passed between the electrode implanted in the motor cortex and a larger electrode cemented to the skull. Motor responses and thresholds of movement evocation remained the same with either type of stimulation. The stimulus used was a train of shocks generated by a constant-current stimulator. Stimulation parameters were: train duration = 100 msec, duration of each shock = 0.5 msec, frequency ----300 Hz. In establishing cortical maps for somatotopic motor localization, only responses produced by threshold currents equal to or lower than 100 #A were considered in order to limit the effects of current spread. It was also verified that for this current intensity (100 #A) the diffusion of the stimulation effects extended less than 1 mm around the tip of the electrode. A 100 #A cathodic stimulation, applied alternately by two electrodes placed 1 mm apart, consistently produced different motor responses when bipolar and monopolar stimulation techniques were used. This shows that stimulation at the two sites does not activate the same efferent pool of cortical cells. Movements produced by intracortical stimulation were analyzed by means of muscle palpation and after the experiments by visualization of movements recorded on moving film. The threshold parameters of stimulation for each movement were also noted. After many test sessions, where the reproducibility of these phenomena was noted, the animals were sacrificed and perfused with 10 ~ formalin containing potassium ferrocyanide. Before perfusion, the state of the motor cortex was ascertained in some cases by its response to selective stimulation of the contralateral cerebellar nuclei. Under these conditions, cortical electrodes still recorded good evoked potentials surmounted with numerous spikes, demonstrating that the motor cortex had not been affected by the implantation of the electrodes several weeks previously. The exact position of each electrode tip was then marked by passing a 50/~A anodic current for 30 msec. The nickel--chrome alloy from which the cortical electrodes were made contained sufficient traces of iron to leave a deposit, which yielded a Prussian blue stain when the animal was perfused. Each brain was photographed frontally after marking the stimulation sites on the surface of the motor cortex with India ink. The exact position of the electrode tips was ascertained from sagittal histological sections of the motor cortex coloured with cresyl violet. Boundaries of cytoarchitectonic areas 4 and 6 were not always verified histologically, but were determined by referring to the Hassler and Muhs-Clement maps tS. RESULTS

In this experimental situation (Fig. 1), stimulation of a particular motor cortex site with threshold current produced muscle contractions around only one joint or in a localized part of body musculature. The location of the contracting muscles was closely linked to the exact position of the stimulating electrodes in the motor cortex.

408

Fig. 1. Analysis of the somatotopic organization of the motor cortex in the chronic cat. Upper left: photograph of brain showing surface position of the stimulating electrodes implanted in the motor cortex several weeks previously. The surface positions of the electrodes are indicated with India ink. White arrow shows the cortical point stimulated during a particular experiment. Upper right: location of the site marked with an arrow in the photograph on the left, transferred onto a diagram of the motor cortex. The recording of all stimulation sites was done under standard conditions. They were then transferred to a standard diagram of the cat motor cortex where the different sulci and the boundaries of cytoarchitectonic areas 4 and 6 (dotted lines, as defined by Hassler and MuhsClement15) are shown, d., postcruciate dimple; cr., cruciate sulcus; cor., coronalis sulcus and pr. syl., presylvian sulcus. Bottom: movement provoked by the stimulation of this cortical point; left is control and right shows flexion movement of contralateral elbow joint muscles produced by cortical stimulation. The exact threshold current intensity o f each e v o k e d response was noted the m o m e n t observers could discern the finest muscle c o n t r a c t i o n p r o d u c e d as current intensity was progressively decreased to the threshold value. The localization of responses shown on the maps o f the m o t o r cortex was n o t related to the threshold muscle contraction, but was defined when stimulating current slightly over threshold intensity p r o d u c e d a clear m o v e m e n t involving a particular articulation.

Characteristics of cortical motor control All muscle responses p r o d u c e d by intracortical stimulation o f the m o t o r cortex have certain c o m m o n characteristics as follows.

409 These motor responses are restricted to a precise part of the musculature and are not repetitive; each stimulation train produces only one response. Regardless of the cortical site activated or joint mobilized, the evoked limb movements were flexions and, very exceptionally, extensions. We also established that movements which induce a perturbation in equilibrium are always accompanied by a postural adjustment which brings the animal into a new equilibrium in the course of the movement. Although cortical stimulation always produced the same motor response in a given animal, in different animals we elicited different types of movements when the same muscle pool was activated. For instance, electrical activation of cortical sites related to the control of the wrist produced dorsiflexion responses, hand supination or pronation movements. We also noted that threshold cortical stimulation never produces a coordinated motor act involving different parts of the musculature, i.e. forelimb and hindlimb muscles, in the same motor response. However, in some cases we obtained these complex responses when the stimulating current was applied behind the motor cortex area, in the cortical region situated around the dimple sulcus. These responses were then generalized throughout the entire body musculature and upset the animal's equilibrium. Repeated observation of these direct evoked muscle contractions, and the consistency of their distribution permitted the establishment of somatotopic organization of the motor cortex in the chronic cat.

Analysis of motor response thresholds When suprathreshold stimulation produced motor responses, current intensity was progressively decreased in order to locate precisely the muscles which were activated at threshold. Threshold intensity was noted when two observers established by palpation or visually the finest muscle contraction. The thresholds of all motor responses were recorded in this manner, but only those responses evoked by currents less than 100 # A were considered in order to preserve the point-to-point localization of effects. Under our experimental conditions the minimum current intensity required to elicit a motor response was 10/~A. This detailed analysis of each response permitted the establishment of some important differences between the threshold values as a function of two principle factors: the site of the activated muscle and the location of the cortical area stimulated. Generally, the lowest threshold responses (current intensity lower than 50/~A) were head movements (neck and face), and contraction of the distal muscles of the forepaw (elbow, wrist and claw movements). On the other hand, other parts of the body musculature were frequently activated by stimulation of higher intensity (50100 #A). This was the case for the muscles of the back, hindlimb and forelimb shoulder. The transposition of the exact location of the sites of stimulation to standard diagrams of the cat motor cortex established that the threshold values were partly a function of the cortical area stimulated. These results permit the delineation of two cortical regions. Within the first, which includes the lateral part of area 4 and the ros-

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Fig. 2. Distribution on standard diagrams of cortical sites which when stimulated induce motor response. These responses are related to their threshold intensities. A: spatial representation of cortical sites from which movements are evoked at stimulation thresholds of less than 50/~A. These sites are primarily located on the lateral and rostral parts of area 4 and the rostral part of area 6. B: spatial representation of cortical sites from which motor responses are evoked with current intensities between 50 and 100/~A. These sites occupy the caudal part of area 6 in the precruciate region, and the most medial part of area 4 in the pre- and postcruciate zones.

tral p a r t o f area 6, responses were p r o d u c e d at low threshold (equal to or less than 50/~A). I n contrast, m o t o r responses to s t i m u l a t i o n o f the medial pre- a n d postcruciate p a r t s o f a r e a 4 and o f the caudal p a r t o f area 6, have higher thresholds (501 0 0 # A ) (Fig. 2).

Somatotopic organization of the cat motor cortex (areas 4 and 6) as established under chronic experimental conditions All muscle c o n t r a c t i o n s observed have been catalogued and related to the exact cortical p o s i t i o n s f r o m which they were evoked. Sites f r o m which a p a r t i c u l a r type of m o v e m e n t could be evoked by stimulation were plotted on a s t a n d a r d d i a g r a m o f the m o t o r cortex. The b o u n d a r i e s o f each zone which exercises a selective c o n t r o l over specific parts of the musculature were established by s u p e r i m p o s i n g m a p s from each individual case. This p r o c e d u r e was repeated for each m o v e m e n t evoked. To achieve m a x i m u m precision in plotting the cortical stimulation sites, these points were d r a w n on d i a g r a m s relating their positions to the interhemispheric and cruciate sulci which have a c o n s t a n t location in the a d u l t cat cerebral cortex TM. F i n a l d i a g r a m s o f s o m a t o t o p i c o r g a n i z a t i o n o f the various m o t o r control locations in the cerebral cortex (areas 4 a n d 6) were done with figurines to indicate the different muscle structures mobilized by individual cortical stimulations. The depths o f the cortical sulci were n o t studied except for the cruciate sulcus where stimulating electrodes were i n t r o d u c e d into the hidden u p p e r p a r t o f the postcruciate m o t o r cortex ( p a r t of area 4, f r o m Hassler a n d Muhs-ClementlS).

Cortical control areas for back and neck muscles (Fig. 3) Electrical s t i m u l a t i o n in different m o t o r cortex sites p r o d u c e d muscle c o n t r a c tions involving axial musculature. These are d o r s o v e n t r a l bending m o v e m e n t s o f the back which are difficult to lateralize. By progressively decreasing the intensity o f the

411 BACK

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Fig. 3. Cortical control areas of the different parts of the cat musculature. The small dots represent the aggregate of the cortical sites stimulated in the course of all the experiments. The large black dots indicate the cortical sites, which, when stimulated electrically, activate a particular and restricted part of the musculature, respectivelyas shown. Certain electrodes (surface emplacement in the hatched area) were inserted into the deep hidden part of the cruciate sulcus (see Fig. 4).

stimulations to threshold, the activation of back muscles was less diffuse and it is possible to exactly situate the muscle contractions either in the higher rostral part or the lower caudal section of the back. These results demonstrate the existence of a fine control of the back musculature. These muscle contractions were evoked by stimulating the caudal part of area 6 and the medial part of area 4 at the level of the anterior sigmoid gyrus. Electrical activation of other sites in this cortical field produced rotation or elevation of the head, involving neck and nape musculature. The cortical control area for this part of the musculature is the rostral prolongation of the cortical control area for the back in area 6 and the medial part of area 4 at the periphery of the presylvian suicus. Cortical control area f o r f a c e m u s c u l a t u r e (Fig. 3)

Stimulation of the explored cortical area produced three kinds of evident face

412 muscle contractions. Most frequent were ear or eyelid lowering, but movements of the vibrissae were also evoked. Ear and eyelid reactions were exclusively contralateral to the cortical stimulation. In these experiments, definite jaw or tongue movements, or evident vegetativc reactions such as dilatation of the pupils or abundant salivation, were never observed. Neither did electrical stimulation of the cortical field under exploration produce any ocular movements. The cortical area the stimulation of which produces these facial reactions, is located rostrally to the neck control area and occupies the whole of the rostral part of area 4 and a part of the adjacent zone in area 6. The hidden motor cortex inside the presylvian sulcus was not explored in these experiments.

Cortical control area for forelimb musculature (Fig. 3) In the cat motor cortex there exists a wide area which, when stimulated, induces contralateral forelimb movements. Electrical stimulation of different sites in this cortical region selectively activates different forelimb joints. The cortical control area for the forelimb occupies almost the whole of area 4 at the level of the anterior and lateral sigmoid gyri and part of this same area 4 in the lateral part of the posterior sigmoid gyrus. It extends into the lateral part of area 6, between the cortical control regions of the back and neck. It is in this wide zone between the median and middle parts of the anterior sigmoid gyrus and the lateral part of the posterior sigmoid gyrus that the cortical sites are located which, when stimulated, produce shoulder movements. More laterally, at the level of the anterior lateral sigmoid gyrus, is located the cortical control field for the elbow muscles, while stimulation of the cortical region near the lateral end of the cruciate sulcus evoked wrist movements. Lastly, the most distal part of the forepaw musculature is activated by stimulation of the caudal and lateral regions of area 4 at the level of the lateral sigmoid gyrus. Threshold stimulation here can activate a very restricted part of the musculature limited to the movement of a single claw of the forepaw. Cortical control areas for the proximal muscles of the forelimb are located in the middle and median parts of area 4; and as sites progressively further from these regions in the direction of the most lateral and caudal parts of the cortex are stimulated, progressively more distal parts of the forelimb are controlled.

Cortical control area for hindlimb musculature (Figs. 3 and 4) Hindlimb movements were evoked by stimulation of a wide cortical field, but contrary to the forelimb results, a total mobilization of the contralateral hindlimb was consistently observed. Stimulation usually resulted in flexion movements. Although the standard diagrams show only the surface of the motor cortex, the median and middle postcruciate localizations are images of the corporeal representation situated on the surface and in the interior of the posterior cruciate sulcus. The exact positions of the tips of the stimulating electrodes were verified by parasagittal histological sections, and were

413

Fig. 4. Detailed study of the explored cortical control area for hindlimb musculature. Upper left: distribution on the surface of the motor cortex of the aggregate of the sites which when stimulated induce hindlimb movements. Black dots indicate the stimulation sites of the superficial layer of pyramidal cells of the postcruciate motor cortex. The starred circles represent the point of entry into the motor cortex of electrodes whose tips penetrated into the deep cellular layers of the upper fold of the postcruciate cerebral cortex. Lower left: microphotograph of a parasagittal histological section of the motor cortex (cresyl violet colouring). The site of the penetration of the electrode into the posterior sigmoid gyrus (starred circle), the trace left by its removal and the exact location of its tip (blackened area) where electrical stimulation was applied, are visible on the photograph. Electrical stimulation with this electrode activated the cellular layer situated inside the upper fold of the hidden motor cortex buried in the cruciate sulcus. Right: standard diagram of the cytoarchitectonic organization of the motor cortex within the cruciate sulcus, according to Hassler and Muhs-Clement TM. The starred circles represent the penetration sites on the surface of the motor cortex. The black dots show the exact positions of the stimulation sites (at the tips of these electrodes). This shows that all stimulations were applied in area 4 of the motor cortex, in the superficial part or in the region which forms the upper bank of the cruciate sulcus. always located either in the superficial postcruciate layer or in the deep region of the m o t o r cortex. This last layer of cells corresponds to part of area 4 according to Hassler a n d M u h s - C l e m e n t is.

Cortical control area f o r the thorax muscles (Fig. 3) S t i m u l a t i o n of certain cortical sites will produce contractions of the pectoral muscles. However, these reactions were exceptional. The cortical sites which when stim u l a t e d produced these responses are located in a zone limited to part of the posterior sigmoid gyrus, between the c o n t r o l areas of the shoulder a n d h i n d l i m b m o v e m e n t s a n d overflowing into the middle of the anterior sigmoid gyrus.

Somatotopic organization in cat motor cortex area The results of these experimental data are presented schematically in Fig. 5

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Fig. 5. Schematic drawing of the somatotopic organization in the cat motor cortex. This diagram summarizes the results of the experiments in all chronic cats. Each figurine is an image of one part of the musculature activated by the electrical stimulation of the cortical area on which it lies. The disposition of the figurines is drawn from the results established in Fig. 3. This facilitates identification, successively, of the cortical control areas for back and neck musculature in the precruciate medial part of the motor cortex; the face area, with 3 distinct regions for the external ear, vibrissae and eyelid control in the rostral part of the cortex; the forelimb area (the largest) from the medial to the lateral parts, with separate zones for shoulder, elbow, wrist and claw control; and finally the representation of the motor area for thorax and hindlimb control. The detailed organization of this last appears in Fig. 4.

by means of figurines superimposed on a single map to give an interpretation of the somatotopic organization of the cat motor cortex. The two major axes of the body are represented in this diagram. The axo-proximo-distal axis is shown extending from the medial part of the motor cortex which controls the axial and proximal musculature to the more lateral zones of the motor cortex, where the control areas of the distal forepaw muscles are located. The rostrocaudal axis is located in the medial part of the cortex where the control area for face movements is located and progressively more caudally those which control neck, nape and back movements. The cortical control field for the hindlimb muscles lies behind the cruciate sulcus on the posterior sigmoid gyrus. This completes the diagram of the corporeal localizations in the cat motor cortex. DISCUSSION

Discrete electrical stimulation of the motor cortex of the freely moving cat induces precise muscular contractions. The localization of these contractions is directly linked to the exact position of the stimulating electrode tip in the cerebral cortex. The repertoire of all movements obtained by precisely controlled stimulation indi-

415 cates the existence of a fine organization of cortical motor control in the cat. Each pool of neurones relates to only a small group of muscles. These cortical units are so disposed as to indicate a precise somatotopic organization of the cat motor cortex.

Characteristics of cortical stimulation parameters The experimental results show that electrical stimulation applied in the cat motor cortex is very localized. Muscle responses are not modified by variation of stimulation parameters other than current intensity, in agreement with the results of Lilly et al. 2°. In our experimental situation, total absence of anaesthetic and direct intracortical stimulation favoured the use of lower intensity stimulating currents and permitted a better appreciation of cortieomotor localization. Indeed, the numerous stimulation experiments which have previously established the detailed cortical representation of the cat motor cortex were for the most part produced in anaesthetized animals and in most cases by surface stimulation 13,1s,21,23,aS,aT,which excites only low threshold cortical cells, when using currents of threshold intensity 1°. The results of Asanuma and his co-workers 4-7 with an intracortical microstimulation technique selectively activating only a small number of cortical cells, show the existence of an extremely fine organization in the cat motor cortex where pools of cells, arranged in columns, control corresponding pools of spinal motoneurones which, in turn, control muscles in the distal part of the forepaw. We have used efficient intracortical stimulation, not as fine as that of Asanuma, but the motor responses evoked in our experiments were comparable to those produced in parallel conditions by intracortical microstimulationak This intracortical stimulation technique permitted the use of current intensities much lower than those utilized in previous experiments where the surface of the cerebral cortex was stimulated. Nevertheless, recent investigations ~7 show that the consequence of intracortical microstimulation is not simple direct excitation of the pyramidal cells, but that the weakest stimulation produces only a transsynaptic activation of these cortical cells by the excitation of their afferent fibers. These results would lead one to think that if the total effect obtained by intracortical microstimulation is in part linked to the arrangement of the pyramidal cells inside the motor cortex, then it could also be related to the spatial organization of the afferent fibers joined to these same cells. This suggestion limits all interpretations of the organization of the motor control based on experiments using intracortical microstimulation. Nevertheless, in our experiments, in spite of the possible spreading of the effects due to the transsynaptic activation of the efferent fibers of the motor cortex, we have been able to distinguish narrow areas, which are all evidently functionally different motor fields. The selectivity of the induced responses permits the description of a fine organization in the localization of the cortical motor control areas for different parts of the cat musculature. This fine control exists in particular for face and forelimb muscles and especially for the distal parts of that limb. But the presence of discrete responses of the axial musculature, as indeed of the entire musculature, reflects the existence of preferential cortical motor areas controlling the different body parts.

416 These punctate results may indicate that using stimulating electrodes less selective than those of Jankowska ~vit is possible to obtain overall effects of motor cortex intracortical stimulation which are less 'sensitive' to the diffusion caused by the activation of the afferent motor cortical fibres.

Muscle response characteristics The use of very low intensity stimulating current allowed us to produce very limited muscular contractions, and especially to define within the cortical control area for forepaw musculature, that field which is related to the command of the more distal part of the forepaw; a detail overlooked by many previous authors 11-13,16,21,23,35. We were not able to reproduce the rhythmic movements described by Ward and Clark 35 and Delgado xa, nor the vegetative reactions frequently described in the literature. It is possible that all these reactions could be a consequence of intense stimulations of overlong duration, producing activation in intracortical and subcortical circuits of the neuronal complex. Electrical stimulation of the motor cortex induced primarily contralateral flexion and rarely extension of the limbs tl-a3,3s. Other experimental data agree with this general finding. Lundberg and Voorhoeve 2z have shown that pyramidal excitation produces an activation in flexor muscle motoneurones and an inhibition in the extensors. Furthermore, Adkins et al? have shown that precruciate motor cortex lesions are followed by a dominant extension in contralateral limbs, which is equivalent to the hypoflexion following pyramidectomy 36. In chronic cat preparations, Delgado u noticed that cortical stimulation of that part of the motor cortex hidden in the folds of the cruciate sulcus induces movement accompanied by postural adjustments. This reaction, reproduced in our experiments, has never been observed when the tests are performed under anaesthesia. This is a generalized reaction which accompanies all movements inducing a disturbance of equilibrium. The precise activation of a cortical pool of cells related to a well-defined movement simultaneously activates other muscles which balance the movement and allow the animal to preserve its equilibrium. Experiments still in progress demonstrate that this postural reaction is part of the motor control. Analysis of threshold responses Our results show that the threshold current intensity necessary to produce motor responses varies in relation to two parameters: the part of the musculature activated and the cortical area stimulated. We have ascertained that the muscle groups engaged in the finest movements (involving wrist, claws, external ear, vibrissae or eyelids) were activated by lower intensity currents and that the current intensity must be increased to mobilize muscles which are used in more general movements (hindlimb or axial movements). This suggests that activation of axial and proximal musculature requires the excitation of a cortical cell population larger than that necessary to activate other parts of the musculature, particularly those of the face and the distal part of the forepaw. In the cat, cortical control of axial and proximal musculature would seem to originate from

417 larger areas than the discrete colonies which control the muscles of the distal part of the forepaw. This agrees with previous resultsZ7, 38 in the monkey. Examination of the topographical distribution of threshold responses on standard diagrams of the cat motor cortex shows a zonal distribution of responses having different thresholds. Low threshold responses were recorded from stimulation applied to rostral and lateral parts of the motor cortex, while stimulation in caudal and medial areas produced responses with higher thresholds. It is interesting to note that, with regard to cortical stimulations, a similarity exists between different parts of areas 4 and 6 (Fig. 2). In particular our attention was drawn by the fact that cortical stimulation in the medial precruciate part of area 4 (near the cruciate sulcus) induces the same high threshold responses as those produced by stimulation of the adjacent part of area 6. These zones are never involved in cortico-rubro-spinal projections 25, cortico-cerebello-interposito projections 24 or direct corticospinal projections 2. Other work 28 shows that the cortical afferents from contralateral cerebellar nuclei to these parts of areas 4 and 6 are also comparable. In summary, although areas 4 and 6 are cytoarchitecturally distinct, no difference in motor function seems to exist between the two areas, but rather between more restricted zones within these two parts of the motor cortex. Somatotopic organization of the cat motor cortex The comparison of our results summarizing the somatotopic organization of the cat motor cortex with previous reports showed some differences, particularly in the localization of back, neck and face cortical control areas. We therefore feel it necessary to analyze individually the boundaries of the various motor control fields in order to compare our results with those obtained from previous experiments using different methods. Cortical control areas for back and neck muscles Results obtained from present experiments show that the cortical control areas for back and neck musculature are to a large extent localized in area 6, in the medial part of the anterior sigmoid gyrus. These findings are not new. Many previous authors, Woolsey 37 in particular, considered that the medial parts of the precruciate motor cortex control the axial musculature. However, in only a few reports were we are able to find a detailed description of this cortical area, which is described principally by authors who have studied head movements. Among them only a few identified a cortical control area for the back a,x4,za,aT. This may be due to the fact that most of the cortical sites for axial movements were located in area 6. Bucy 9 reported that responses induced from cortical stimulation in area 6 were very sensitive to anaesthesia and for this reason contractions of axial muscles were probably unobservable in most experiments performed under anaesthesia. Cortical control area for face musculature In our experiments this cortical field was restricted to the rostral parts of areas 4 and 6, and corresponded to motor control regions for vibrissae, eyelid and external

418 ear muscles. These data do not agree with previously published results of other authors. Interestingly, GaroP 3 noticed contradictions in the literature as early as 1942. Some authors described a large motor control area for the face, overflowing the coronalis sulcus laterally and rostrally~3.35, 3v, but it should be noted that they particularly studied jaw contractions and tongue movements, and not movements of the eyelid and external ear. In agreement with us, other authors, when describing the same motor responses observed in our experiments, limit the face motor control area to the rostral parts of areas 4 and 611,12,14,21,23. Our results also agree with the anatomical reports from Strick 34. It is important to note, however, that the possibility that a part of the cortical control area for face musculature is buried in the presylvian sulcus is not excluded. Moreover, the area which controls jaw contractions and tongue movements has been located laterally to coronal sulcus and extends down almost to the rhinal sulcus 37. This part of the cortex was not investigated here. Finally, we have never induced ocular movements by cortical stimulation of the explored area. This result agrees with the reports of Schlag and Schlag-Rey 32 who limit the 'cortical frontal eye field' to the medial and rostral parts of the motor cortex in cytoarchitectonic area 8.

Cortical control area for .forelimb musculature Two essential facts must be borne in mind when examining maps of the cortical area controlling forelimb musculature. First, this zone is very extensive, occupying almost the whole of area 4 in the anterior and lateral sigmoid gyri and part of the lateral region of area 6. Second, a very fine control, limited to only a few muscles, exists in the cat and hence it is possible to plot the control areas related to each particular joint of the forelimb musculature on a map of the motor cortex. Our results agree with the cortical representation for the forelimb described by most of the previous authors. However, the cortical control area for shoulder musculature has not always been placed within the same boundaries in the different reports considered. The extension of the representation of the shoulder control region into area 6 agrees with Delgado 1~, Delgado and Livingston lz MacKibben and Wheelis z3 and Strick 34. Its prolongation into the medial part of the posterior sigmoid gyrus concurs with the boundaries given by GaroP 3 and Ward and Clark 35. These last observations were also noted by Borge 8. No previous reports examined indicate the presence of a separate motor control for the different segments of the forelimb in the manner permitted by our experiment. Sometimes one finds a description of motor control areas of two or three separate segments, as is the case of Garo113, who differentiates between cortical control areas for elbow and wrist musculature. Other studies were limited to the control area of the distal part of the forepaw3,~k Only Borge 8 and Woolsey 37 localized distinct control areas for each joint of the forelimb without, however, determining their respective boundaries.

419 Cortical control area for hindlimb musculature Examination of the cortical area controlling hindlimb musculature shows that these muscles are under the control of cells in the medial part of the posterior sigmoid gyrus within area 4. Also indicated behind the surface boundary of area 4 are stimulation sites efficacious in provoking motor responses from the hindlimb. These are in reality located deep in the folds of the cruciate sulcus in the hidden part of area 4 is. This agrees with the results of Delgado 1~ who especially investigated this region, and with the results of Borge s, Delgado and Livingston 12, and Woolsey3~; and with the anatomical data of Strick 34 who locates the motor control zone of the hindlimb within the larger part of area 4 buried within the cruciate sulcus. We have not been able to reproduce the detailed representation for the different joints of the hindlimb described by Borge s and GaroP 3, each threshold stimulation here producing only flexion of the whole limb. Nevertheless, this also may indicate that we have not explored the entire cortical area, which when stimulated produces hindlimb movements. Lastly, we have never observed the motor representation of hindlimb musculature in the anterior sigmoid gyrus as described by Ward and Clark as. Their results may have been due to the horizontal diffusion of suprathreshold stimulating currents to the adjacent part of area 4 hidden in the cruciate sulcus. Cortical control area for thorax musculature Contractions of the thoracic musculature by electrical stimulation of the cat motor cortex are difficult to produce, and it is possible that the difficulty of making such observations has led to some confusion in the localization of this area in previous studies. Some authors localize the cortical control area for trunk movements within the presylvian sulcus11,14 while others describe it as hidden in the cruciate SUIcus 12, 13,23,37. We obtained contractions of pectoral muscles from stimulation of this last part of the motor cortex, but the few results we have do not permit exclusion of other foci controlling the thoracic musculature in the cat. CONCLUSION

The results of our experiments permit us to describe a very fine organization o f the cat's motor control in cortical areas 4 and 6. This logical arrangement of different foci of control of the musculature gives a picture of the organization of the motor cortex which is in agreement with those previously established, especially with that of Woolsey37. The use of a localized and efficient stimulation technique also permitted the definition within area 4 of the arrangement of the motor control area for the distal part of the forelimb musculature. This agrees with localizations by Asanuma and Sakata 5 and Sakata and Miyamoto 31 who identified and studied this fine control. Our study establishes that the control area for the distal part (wrist and claws) of the forepaw occupies a large area in the motor cortical representation. The clear individualization of this control area, already marked in carnivores, accentuated in the primates and still

420 more in man (where each of the fingers has its own control area), is related to the phylogenetie increase in the use of these muscles 26 which play an important role in the cat's comportment. Our results also demonstrate that electrical stimulation of area 6 produces muscle contractions. It is interesting to note the existence of a clear somatotopic organization within that part of the area 6 explored in our experiments, where the cortical control area for the axial musculature, with different control loci for the back, neck and certain facial muscles, is found. This detailed representation had been assumed but not demonstrated in detail by previous authors even though the medial parts of area 6 had not been explored; the study of this area was favoured here by the utilization of an unanaesthetized animal preparation. The results also show that the lateralization of the movements induced from area 6 stimulation was not as clear as for those given from area 4. The difficulty in lateralizing the motor responses for back and neck muscles is a corollary to the fact that, in the cat, area 6 never has direct corticospinal z or cortico-rubro-spinal projections19, 25. These corticobulbar projections are generally bilateral. On the other hand, the m o t o r control of facial muscles from area 6 is eontralateral, which suggests a more precise organization of the projections of area 6 onto facial motor nuclei. These experiments show that in the eat the cortical motor control of musculature is a fine topographically organized system. There exists in the motor cortex a logical arrangement of the different foci each related to a precise part of the axial, proximal or distal musculature. Thus, the entire musculature would seem to be controlled from these motor foci, each of which represents a more or less important pool of cells disposed in efferent colonies, independent of the cells in other colonies. Finally, we feel that coordinated activation of different muscle pools during a complex movement necessitating muscle synergy can be ensured only by cortical afferents simultaneously activating different foci in the motor cortex 3°. ACKNOWLEDGEMENTS

The authors thank Dr. J. Massion for his advice and criticism during the course of experiments and also thank Miss A. Grangetto and Messrs. R. Haour, R. Massarino and P. Quilici for their technical assistance.

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Somatotopic localization in cat motor cortex.

Punctate intracortical stimulation of the motor cortex (areas 4 and 6), with parallel observation of the induced movements, permits description of a f...
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