412
Brain Research, 167 (1979) 412 416 ,:~ Elsevier/North-Holland Biomedical Press
Double representation of the distal, forelimb in cat motor cortex
C A R O L L. PAPPAS and PETER L. STRICK
Departments of Physiology and Neurosurgery, Upstate Medical Center, and Research Service, V~ A. Medical Center, Syracuse, N. Y. (U.S.A.) (Accepted January 1 lth, 1979)
The results of studies which have examined the representation of body parts in the motor cortex classically have been expressed as a map of the body displayed on the cortical surface ~,a,5,sAl. These maps, generated from studies in a variety of animal species, have several features in common. First. each body part is represented only once. Second, body parts are represented in an orderly sequence and this sequence reflects the anatomical relation of body parts to each other in the periphery. Finally, there is a clear tendency for the representation of distal limb parts to be more extensive than that of proximal body parts. Recent experiments have questioned the concept of a single representation for each body part in the motor cortex 7,9. For example, Strick and Preston demonstrated two anatomically separate representations of the hand and wrist m area 4 of the squirrel monkey 9. In their experiments microstimulation in caudal area 4 evoked predominantly hand movements. Rostral to this was a zone from which wrist movements were evoked. Just rostrat to the zone of wrist representation was a second zone of hand representation and further roxtrally was a second zone o f wrist representation. A question raised by the observations in the squirrel monkey is whether the pattern of distal representation observed in the m o t o r cortex of this animal is an isolated, species-specific phenomenon, or a more universal pattern of motor cortex organization. The results of a recent microstimulation study in the cat suggested to us that there also might be multiple representations of the forelimb in the m o t o r cortex of that animal (see ref 8, Fig. 3 ; wrist diagram). The present experiments were designed to investigate this possibility. Microstimulation at multiple, closely spaced intervals in individual animals permitted construction of detailed maps of the forelimb area of the m o t o r cortex. These maps demonstrate the existence of a double representation of the distal forelimb in area 47 of the cat motor cortex. Experiments were performed in 20 adult cats, initially anesthetized with ketamine HC1 (20 mg/kg, i.m.) and pentobarbital sodium (10 mg/kg, i.v.). Additional small doses of ketamine were given as necessary during the experiment to maintain anesthesia. The animal's head was rigidly held by a bolt secured to the skull with dental acrylic. A plastic cylinder was fixed over the forelimb area of the m o t o r cor-
413 tex3, 8. The cylinder was filled with warm mineral oil and formed the base of a closed chamber system 4. Cathodal microstimulation (12-20 pulses, 0.2 msec duration, frequency 300-400 Hz, 1-50 #A) was delivered through either platinum-iridium or elgiloy 1° glass-coated microelectrodes (0.6-1.4 M~Q). The microelectrode was advanced into the pre- and postcruciate gyri in 100 #m steps. The site of each microelectrode penetration was marked on a photograph of the brain surface. The lowest threshold points for evoking movement were found in preliminary experiments to occur at a cortical depth of 1.2-1.5 ram, in agreement with previous reports2, 8. Subsequently, microstimulation was routinely carried out at depths of 1.0-2.0 mm as estimated by the microdrive readings and later confirmed by histology. The results of stimulation were analyzed by both visual observation and electromyograms (EMGs) recorded from fine wires inserted into various forearm muscles. Initially E M G electrodes were placed in the triceps, extensor carpi radialis, extensor carpi ulnaris, palmaris longus, extensor digitorum communis and extensor lateralis digitorum muscles. If a visible response to microstimulation occurred in a distal muscle other than those already monitored, E M G electrodes were then placed in the responding muscle. Eight to 10 muscles were monitored in each experiment. The placement of' each E M G wire was verified by visually observing the muscle twitches and movements evoked upon electrical stimulation through the E M G leads. The EMGs evoked by cortical stimulation were conventionally amplified and displayed on a storage oscilloscope. In addition, EMGs were full wave rectified and averaged over 16 trials with an on-line signal averager. Microelectrode lesions were placed at selected points at the end of each experiment. The brains were fixed by perfusion through the heart with normal saline followed by a solution of 1 ~ paraformaldehyde and 1.25 °/o glutaraldehyde. In those experiments in which elgiloy microelectrodes were used, 2 °/o ferrocyanide was added to the perfusion solution to induce a Prussian Blue reaction at lesion sites TM. A block of tissue including the stimulated area was frozen sectioned at 50/~m and stained with cresyl violet. Serial sections were then analyzed to identify the cytoarchitecture 6 in the regions of the lesions. Microstimulation at closely spaced penetrations demonstrates two spatially separate representations of the distal forelimb in area 4y of the cat motor cortex. The existence of two representations is most clearly seen in maps of digit responses (Figs. 1 and 2). In all 20 animals examined, digit responses could be evoked from two regions which were separated by a field (in most cases greater than l ram) from which responses of more proximal muscles were evoked. A typical map of a single animal illustrating two digit fields is shown in Fig. 1. q-he dotted line in Fig. 1A indicates the region of cortex which was explored with microstimulation. This region appears enlarged in Fig. lB. The locations of all penetrations are indicated by dots. The large dots in Fig. 1B indicate the sites at which digit movements were evoked. Small dots indicate sites at which microstimulation evoked movement at other joints or no movement. Large vessels on the surface of the brain can cover sizable portions of the area available for microelectrode penetration.
414 A
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Fig. 1A: a portion of the cat left hemisphere with relevant sulci and gyri labelled. Dotted rectangle indicates the area explored with intracortical microstimulation. This area is enlarged in Figs. IB and 2A. B: a cortical map of penetrations in a single animal where microstimulation evoked digit movements alone from two spatially separate regions. The area of cortex illustrated is outlined in Fig. IA. Dots indicate sites of microelectrode penetrations made in a single animal. Large dots indicate sites where microstimulation evoked digit movements. Small dots indicate sites where stimulalion evoked movements at other joints or no response. The last 3 mm of the cruciate sulcUsand the coronal sulcus are included for orientation.
These vessels, which we carefully avoided, are reflected on the maps a s t h e relatively large spaces between groups o f penetrations. The m a p in Fig. 1B clearly illustrates the clustering o f digit responses into two separate regions o f the m o t o r cortex. One cluster o f digit responses was located adjacent to the lateral edge o f the cruciate sulcus. The other cluster was located more rostrally on the precruciate gyrus. The spatial distribution o f microstimulation sites evoking E M G activity in a single digit muscle (flexor digiti minimi) is shown for another animal in Fig. 2A. The dots again indicate the sites o f all penetrations. Large dots indicate the sites at which an E M G response was recorded in Flexor Digiti Minimi ( F D M ) , a flexor o f the 5th digit. Small dots indicate sites at which microstimulation evoked E M G activity in other muscles or no response. The E M G responses evoked in this m u s c l e by cortical microstimulation at 10 # A are shown in Fig. 2B. The numbers to the left o f the E M G s in Fig. 2B correspond to the numbered penetrations in Fig. 2A. T h e stimulus is indicated on the b o t t o m line o f Fig. 2B. In this animal penetrations evoking F D M responses were clustered into two separate regions o f the m o t o r cortex(Fig. 2A). One cluster was located in the postcruciate gyrus and a second cluster was located more rostrally in the precruciate gyrus. These two clusters were separated by a region (including points 7-12) in which microstimulation did not evoke responses in any digit muscle as judged by both E M G and visual observation. T h e E M G responses in Fig. 2B clearly demonstrate that the same muscle can be represented in each o f the two
415 A o1
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Fig. 2A: a cortical map of penetrations in another animal demonstrating two regions in which microstimulation evoked activity in a single digit muscle, flexor digiti minimi. Dots indicate sites of microelectrode penetrations. Large dots indicate sites where microstimulation evoked EMG activity in FDM. Small dots indicate sites where stimulation evoked EMG activity in other muscles or no activity. B: EMG responses of Flexor Digiti Minimi evoked by microstimulation of 10/~A at sites numbered in Fig. 2A. The microstimulation train (12 pulses, 0.2 msec duration, frequency 400 Hz) indicated at the bottom of the figure.
digit representations. In o t h e r e x p e r i m e n t s responses o f E L D and E C D were evoked f r o m the two digit representations. A l t h o u g h the l o c a t i o n o f the two digit zones varied f r o m a n i m a l to animal, two t o p o g r a p h i c p a t t e r n s are evident in the data. In some animals (e.g., Fig. I B) a caudal digit field was located j u s t lateral to the cruciate sulcus. In others (e.g., Fig. 2A) a c a u d a l digit field was located in the p o s t c r u c i a t e gyrus. In all cases, however, histological analysis showed t h a t b o t h digit fields were located in area 47 o f the m o t o r cortex 6. A l t h o u g h the figures illustrate only those p e n e t r a t i o n s in which digit m o v e m e n t s were elicited, in some animals separate wrist fields were located adjacent to each digit field. In contrast, s h o u l d e r responses tended to occur at stimulation points s u r r o u n d i n g
416 the regions in which m o r e distal responses were evoked. The a r r a n g e m e n t o f shoulder p o i n t s in the cat thus a p p e a r s similar to the nested-ring a r r a n g e m e n t described in the m a c a q u e (arctoides) 7 in which a central core o f finger a n d wrist p o i n t s was s u r r o u n d e d by i n c o m p l e t e rings o f elbow a n d s h o u l d e r points. Therefore, we c o n s i d e r the d o u b l e r e p r e s e n t a t i o n o f the digits a n d wrist to be a localized specialization withitl the forelimb area o f the cat m o t o r cortex. I n s u m m a r y , o u r results d e m o n s t r a t e the existence o f two spatially s e p a r a t e digit r e p r e s e n t a t i o n s in the cat m o t o r cortex. In a d d i t i o n , E M G recordings show t h a t the same muscles can be r e p r e s e n t e d in each o f the t w o digit fields. F i n a l l y , we have d e m o n s t r a t e d a p a t t e r n o f r e p r e s e n t a t i o n o f the d i s t a l f o r e l i m b in the cat m o t o r cortex similar to t h a t first o b s e r v e d in the squirrel m o n k e y 9. A l t h o u g h the differences between: the cat and p r i m a t e m o t o r systems have often been e m p h a s i z e d , the present study p o i n t s to a f u n d a m e n t a l similarity in the basic t o p o g r a p h i c a l o r g a n i z a t i o n o f their m o t o r cortices. The a u t h o r s wish to t h a n k Dr. J a m e s B. Preston for his c o n t i n u i n g s u p p o r t a n d guidance, Dr. Maxwell M. Mozell for his helpful c o m m e n t s in reviewing the m a n u s c r i p t , Ms. C a t h r y n Skretch for invaluable technical assistance, a n d Ms. C a r o l L l a d o s for secretarial assistance. This s t u d y s u p p o r t e d by U S P H S G r a n t NS02957 a n d the Veterans A d m i n i s t r a tion Medical Research Fund.
1 Asanuma, H. and Arnold, A.. Noxious effects of excessive currents used for intracortical microstimulation, Brain Research, 96 (1975) 103-107. 2 Asanuma, H. and Sakata, H., Functional organization of a cortical efferent system examined with focal depth stimulation in cats, J. Neurophysiol., 30 (1967) 35-54. 3 Borge, A. F., The Motor Cortex of the Cat, M.Sc. Thesis. Science, University of Wisconsin. 1950, 33 pp. 4 Davies, P. W., Chamber for microelectrode studies in the cerebral cortex, Science, 124 (1956) 179-180. 5 Garol, H. W., The 'motor' cortex of the cat, J. Neuropath. exp. Neurol., 1 (1942) 139-145. 6 Hassler. R. und Muhs-Clement, K., Architektonischer Aufbau des sensomotorischen und parietalen Cortex der Katze, J. Hirnforsch., 6 (t964) 377-420. 7 Kwan, H. C., MacKay, W. A., Murphy, J. T. and Wong, Y. C., Spatial Organization of Precentral Cortex in Awake Primates. 11 Motor Outputs., J. NeurophysioL, 41 (1978) 1120.-1131. 8 Nieoullon, A. and Rispat-Padel, L., Somatotopic localization in cat motor cortex, Brain Research, 105 (1976) 405-422. 9 Strick, P. L. and Preston, J. B., Multiple representation in primate motor cortex. Brain Research, 154 (1978) 366-370. 10 Suzuki, H. and Azuma, M., A glass-insulated 'elgiloy'microelectrode for recording unit activity in chronic monkey experiments, Electroenceph. clin. NeurophysioL, 41 (1976) 93-9L 11 Woolsey, C. N., Organization of somatic sensory and motor areas of the cerebral cortex. In H. F. Harlow and C. N. Woolsey (Eds.), Biological and Biochemical Basis of Behavior, University of Wisconsin Press, Madison, Wisc., 1958, pp. 63-81.
Brain Research, 167 (1979) 412 416 ,:~ Elsevier/North-Holland Biomedical Press
Double representation of the distal, forelimb in cat motor cortex
C A R O L L. PAPPAS and PETER L. STRICK
Departments of Physiology and Neurosurgery, Upstate Medical Center, and Research Service, V~ A. Medical Center, Syracuse, N. Y. (U.S.A.) (Accepted January 1 lth, 1979)
The results of studies which have examined the representation of body parts in the motor cortex classically have been expressed as a map of the body displayed on the cortical surface ~,a,5,sAl. These maps, generated from studies in a variety of animal species, have several features in common. First. each body part is represented only once. Second, body parts are represented in an orderly sequence and this sequence reflects the anatomical relation of body parts to each other in the periphery. Finally, there is a clear tendency for the representation of distal limb parts to be more extensive than that of proximal body parts. Recent experiments have questioned the concept of a single representation for each body part in the motor cortex 7,9. For example, Strick and Preston demonstrated two anatomically separate representations of the hand and wrist m area 4 of the squirrel monkey 9. In their experiments microstimulation in caudal area 4 evoked predominantly hand movements. Rostral to this was a zone from which wrist movements were evoked. Just rostrat to the zone of wrist representation was a second zone of hand representation and further roxtrally was a second zone o f wrist representation. A question raised by the observations in the squirrel monkey is whether the pattern of distal representation observed in the m o t o r cortex of this animal is an isolated, species-specific phenomenon, or a more universal pattern of motor cortex organization. The results of a recent microstimulation study in the cat suggested to us that there also might be multiple representations of the forelimb in the m o t o r cortex of that animal (see ref 8, Fig. 3 ; wrist diagram). The present experiments were designed to investigate this possibility. Microstimulation at multiple, closely spaced intervals in individual animals permitted construction of detailed maps of the forelimb area of the m o t o r cortex. These maps demonstrate the existence of a double representation of the distal forelimb in area 47 of the cat motor cortex. Experiments were performed in 20 adult cats, initially anesthetized with ketamine HC1 (20 mg/kg, i.m.) and pentobarbital sodium (10 mg/kg, i.v.). Additional small doses of ketamine were given as necessary during the experiment to maintain anesthesia. The animal's head was rigidly held by a bolt secured to the skull with dental acrylic. A plastic cylinder was fixed over the forelimb area of the m o t o r cor-
413 tex3, 8. The cylinder was filled with warm mineral oil and formed the base of a closed chamber system 4. Cathodal microstimulation (12-20 pulses, 0.2 msec duration, frequency 300-400 Hz, 1-50 #A) was delivered through either platinum-iridium or elgiloy 1° glass-coated microelectrodes (0.6-1.4 M~Q). The microelectrode was advanced into the pre- and postcruciate gyri in 100 #m steps. The site of each microelectrode penetration was marked on a photograph of the brain surface. The lowest threshold points for evoking movement were found in preliminary experiments to occur at a cortical depth of 1.2-1.5 ram, in agreement with previous reports2, 8. Subsequently, microstimulation was routinely carried out at depths of 1.0-2.0 mm as estimated by the microdrive readings and later confirmed by histology. The results of stimulation were analyzed by both visual observation and electromyograms (EMGs) recorded from fine wires inserted into various forearm muscles. Initially E M G electrodes were placed in the triceps, extensor carpi radialis, extensor carpi ulnaris, palmaris longus, extensor digitorum communis and extensor lateralis digitorum muscles. If a visible response to microstimulation occurred in a distal muscle other than those already monitored, E M G electrodes were then placed in the responding muscle. Eight to 10 muscles were monitored in each experiment. The placement of' each E M G wire was verified by visually observing the muscle twitches and movements evoked upon electrical stimulation through the E M G leads. The EMGs evoked by cortical stimulation were conventionally amplified and displayed on a storage oscilloscope. In addition, EMGs were full wave rectified and averaged over 16 trials with an on-line signal averager. Microelectrode lesions were placed at selected points at the end of each experiment. The brains were fixed by perfusion through the heart with normal saline followed by a solution of 1 ~ paraformaldehyde and 1.25 °/o glutaraldehyde. In those experiments in which elgiloy microelectrodes were used, 2 °/o ferrocyanide was added to the perfusion solution to induce a Prussian Blue reaction at lesion sites TM. A block of tissue including the stimulated area was frozen sectioned at 50/~m and stained with cresyl violet. Serial sections were then analyzed to identify the cytoarchitecture 6 in the regions of the lesions. Microstimulation at closely spaced penetrations demonstrates two spatially separate representations of the distal forelimb in area 4y of the cat motor cortex. The existence of two representations is most clearly seen in maps of digit responses (Figs. 1 and 2). In all 20 animals examined, digit responses could be evoked from two regions which were separated by a field (in most cases greater than l ram) from which responses of more proximal muscles were evoked. A typical map of a single animal illustrating two digit fields is shown in Fig. 1. q-he dotted line in Fig. 1A indicates the region of cortex which was explored with microstimulation. This region appears enlarged in Fig. lB. The locations of all penetrations are indicated by dots. The large dots in Fig. 1B indicate the sites at which digit movements were evoked. Small dots indicate sites at which microstimulation evoked movement at other joints or no movement. Large vessels on the surface of the brain can cover sizable portions of the area available for microelectrode penetration.
414 A
B CAUDAL
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•
CR LICIAYE ;~ 0" °.
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S mm
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Fig. 1A: a portion of the cat left hemisphere with relevant sulci and gyri labelled. Dotted rectangle indicates the area explored with intracortical microstimulation. This area is enlarged in Figs. IB and 2A. B: a cortical map of penetrations in a single animal where microstimulation evoked digit movements alone from two spatially separate regions. The area of cortex illustrated is outlined in Fig. IA. Dots indicate sites of microelectrode penetrations made in a single animal. Large dots indicate sites where microstimulation evoked digit movements. Small dots indicate sites where stimulalion evoked movements at other joints or no response. The last 3 mm of the cruciate sulcUsand the coronal sulcus are included for orientation.
These vessels, which we carefully avoided, are reflected on the maps a s t h e relatively large spaces between groups o f penetrations. The m a p in Fig. 1B clearly illustrates the clustering o f digit responses into two separate regions o f the m o t o r cortex. One cluster o f digit responses was located adjacent to the lateral edge o f the cruciate sulcus. The other cluster was located more rostrally on the precruciate gyrus. The spatial distribution o f microstimulation sites evoking E M G activity in a single digit muscle (flexor digiti minimi) is shown for another animal in Fig. 2A. The dots again indicate the sites o f all penetrations. Large dots indicate the sites at which an E M G response was recorded in Flexor Digiti Minimi ( F D M ) , a flexor o f the 5th digit. Small dots indicate sites at which microstimulation evoked E M G activity in other muscles or no response. The E M G responses evoked in this m u s c l e by cortical microstimulation at 10 # A are shown in Fig. 2B. The numbers to the left o f the E M G s in Fig. 2B correspond to the numbered penetrations in Fig. 2A. T h e stimulus is indicated on the b o t t o m line o f Fig. 2B. In this animal penetrations evoking F D M responses were clustered into two separate regions o f the m o t o r cortex(Fig. 2A). One cluster was located in the postcruciate gyrus and a second cluster was located more rostrally in the precruciate gyrus. These two clusters were separated by a region (including points 7-12) in which microstimulation did not evoke responses in any digit muscle as judged by both E M G and visual observation. T h e E M G responses in Fig. 2B clearly demonstrate that the same muscle can be represented in each o f the two
415 A o1
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Fig. 2A: a cortical map of penetrations in another animal demonstrating two regions in which microstimulation evoked activity in a single digit muscle, flexor digiti minimi. Dots indicate sites of microelectrode penetrations. Large dots indicate sites where microstimulation evoked EMG activity in FDM. Small dots indicate sites where stimulation evoked EMG activity in other muscles or no activity. B: EMG responses of Flexor Digiti Minimi evoked by microstimulation of 10/~A at sites numbered in Fig. 2A. The microstimulation train (12 pulses, 0.2 msec duration, frequency 400 Hz) indicated at the bottom of the figure.
digit representations. In o t h e r e x p e r i m e n t s responses o f E L D and E C D were evoked f r o m the two digit representations. A l t h o u g h the l o c a t i o n o f the two digit zones varied f r o m a n i m a l to animal, two t o p o g r a p h i c p a t t e r n s are evident in the data. In some animals (e.g., Fig. I B) a caudal digit field was located j u s t lateral to the cruciate sulcus. In others (e.g., Fig. 2A) a c a u d a l digit field was located in the p o s t c r u c i a t e gyrus. In all cases, however, histological analysis showed t h a t b o t h digit fields were located in area 47 o f the m o t o r cortex 6. A l t h o u g h the figures illustrate only those p e n e t r a t i o n s in which digit m o v e m e n t s were elicited, in some animals separate wrist fields were located adjacent to each digit field. In contrast, s h o u l d e r responses tended to occur at stimulation points s u r r o u n d i n g
416 the regions in which m o r e distal responses were evoked. The a r r a n g e m e n t o f shoulder p o i n t s in the cat thus a p p e a r s similar to the nested-ring a r r a n g e m e n t described in the m a c a q u e (arctoides) 7 in which a central core o f finger a n d wrist p o i n t s was s u r r o u n d e d by i n c o m p l e t e rings o f elbow a n d s h o u l d e r points. Therefore, we c o n s i d e r the d o u b l e r e p r e s e n t a t i o n o f the digits a n d wrist to be a localized specialization withitl the forelimb area o f the cat m o t o r cortex. I n s u m m a r y , o u r results d e m o n s t r a t e the existence o f two spatially s e p a r a t e digit r e p r e s e n t a t i o n s in the cat m o t o r cortex. In a d d i t i o n , E M G recordings show t h a t the same muscles can be r e p r e s e n t e d in each o f the t w o digit fields. F i n a l l y , we have d e m o n s t r a t e d a p a t t e r n o f r e p r e s e n t a t i o n o f the d i s t a l f o r e l i m b in the cat m o t o r cortex similar to t h a t first o b s e r v e d in the squirrel m o n k e y 9. A l t h o u g h the differences between: the cat and p r i m a t e m o t o r systems have often been e m p h a s i z e d , the present study p o i n t s to a f u n d a m e n t a l similarity in the basic t o p o g r a p h i c a l o r g a n i z a t i o n o f their m o t o r cortices. The a u t h o r s wish to t h a n k Dr. J a m e s B. Preston for his c o n t i n u i n g s u p p o r t a n d guidance, Dr. Maxwell M. Mozell for his helpful c o m m e n t s in reviewing the m a n u s c r i p t , Ms. C a t h r y n Skretch for invaluable technical assistance, a n d Ms. C a r o l L l a d o s for secretarial assistance. This s t u d y s u p p o r t e d by U S P H S G r a n t NS02957 a n d the Veterans A d m i n i s t r a tion Medical Research Fund.
1 Asanuma, H. and Arnold, A.. Noxious effects of excessive currents used for intracortical microstimulation, Brain Research, 96 (1975) 103-107. 2 Asanuma, H. and Sakata, H., Functional organization of a cortical efferent system examined with focal depth stimulation in cats, J. Neurophysiol., 30 (1967) 35-54. 3 Borge, A. F., The Motor Cortex of the Cat, M.Sc. Thesis. Science, University of Wisconsin. 1950, 33 pp. 4 Davies, P. W., Chamber for microelectrode studies in the cerebral cortex, Science, 124 (1956) 179-180. 5 Garol, H. W., The 'motor' cortex of the cat, J. Neuropath. exp. Neurol., 1 (1942) 139-145. 6 Hassler. R. und Muhs-Clement, K., Architektonischer Aufbau des sensomotorischen und parietalen Cortex der Katze, J. Hirnforsch., 6 (t964) 377-420. 7 Kwan, H. C., MacKay, W. A., Murphy, J. T. and Wong, Y. C., Spatial Organization of Precentral Cortex in Awake Primates. 11 Motor Outputs., J. NeurophysioL, 41 (1978) 1120.-1131. 8 Nieoullon, A. and Rispat-Padel, L., Somatotopic localization in cat motor cortex, Brain Research, 105 (1976) 405-422. 9 Strick, P. L. and Preston, J. B., Multiple representation in primate motor cortex. Brain Research, 154 (1978) 366-370. 10 Suzuki, H. and Azuma, M., A glass-insulated 'elgiloy'microelectrode for recording unit activity in chronic monkey experiments, Electroenceph. clin. NeurophysioL, 41 (1976) 93-9L 11 Woolsey, C. N., Organization of somatic sensory and motor areas of the cerebral cortex. In H. F. Harlow and C. N. Woolsey (Eds.), Biological and Biochemical Basis of Behavior, University of Wisconsin Press, Madison, Wisc., 1958, pp. 63-81.
