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Interhemispheric connections of the precentral motor cortex in the rhesus monkey
594
SHORT COMMUNICATIONS
Inlerhemispheric connections of the precentral motor cortex in the rhesus monkey Recent anatomical investigations have shown that in rhesus monkey the interhemispheric connections of the primary somatosensory area (SI) are limited to the areas representing the face, trunk and limbgirdles, whereas no callosal connections are found in the hand and foot representation2,5, 8. These studies 2,8 also demonstrated that SI is connected non-homotopicaUy to the opposite second somatosensory area (SII). Since the postcentral gyrus (SI) and the precentral m o t o r cortex are topographically interconnected ipsilaterally 7 it would be of interest to know whether the precentral motor cortex possesses a pattern of interhemispheric connection similar to that of SI. To investigate this, lesions were made in various parts of the precentral gyrus by the method of subpial suction in 5 rhesus monkeys. The resulting patterns of fiber degeneration in the opposite hemisphere were studied by means of the modified Nauta silver impregnation technique 6. The location and extent of each lesion were
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Fig. 1. A, D i a g r a m o f m o n k e y cortex showing t h e locations o f t h e s u p p l e m e n t a r y m o t o r (MID, the precentral m o t o r (MI), t h e postcentral p r i m a r y s o m a t o s e n s o r y (SI) a n d t h e second sensory (SII) areas as described by W o o l s e y 11. C a n d D , D i a g r a m m a t i c representation o f the lesion o f t h e rostral b a n k o f t h e central sulcus a n d adjacent part of t h e precentral g y r u s a n d resulting fiber degeneration (indicated by dots) in t h e lateral a n d medial surfaces o f the opposite hemisphere. In B, tracings o f representative sections t a k e n f r o m t h e levels (1-7) indicated in D are shown. Abbreviations: A. S. = arcuate sulcus; C. C. = c o r p u s c a l l o s u m ; C. S. = central sulcus; C I N G . S. -cingulate sulcus; I. O. S. -- inferior occipital sulcus; I. P. S. -- intraparietal sulcus; L. F. = lateral fissure; L. S. -- lunate sulcus: P. S. = principal sulcus; S. P. D. = superior precentral dimple; S. T. S. -- superior t e m p o r a l sulcus.
Brain Research, 15 (1969) 594-596
SHORT COMMUNICATIONS
595
mapped. In all cases some damage was found in the white matter immediately subjacent to the lesioned cortex. The lesions were placed as follows: (1) along the entire extent of the rostral bank of the central sulcus and extending into the caudal portion of the precentral gyrus (Fig. 1C), (2) in the upper third of this same strip, (3) in the lower third of the same strip, (4) along the entire rostral border of the precentral gyrus and (5) in the region surrounding the superior precentral dimple. A comparison of our findings with Woolsey's 'summary diagram' of sensory motor simiusculi (Fig. 1A) 11 indicated the existence of the following arrangement. The precentral areas which contain the hand and foot representation do not project to the opposite hemisphere. However, the face and the trunk areas do project to the opposite hemisphere. The projections from the latter areas are directed both to homotopic and non-homotopic areas. In regard to the non-homotopic projection, the face area projects non-homotopically to the neck area. The ventral portion of the trunk around the superior precentral dimple and in the rostral bank of the central sulcus projects non-homotopically to the dorsal portion of the trunk area in the rostral part of the precentral gyrus, and to the tail area (Fig. 1B, D). The dorsal portion of the trunk area in the rostral part of the precentral gyrus projects nonhomotopically to the caudal parts of the precentral gyrus, exclusive of the hand and the foot areas. A further comparison of our findings with Woolsey's 'summary diagram' indicates that the face and the ventral portion of the trunk areas additionally maintain projections to the corresponding portions of the supplementary motor cortex of the opposite hemisphere and a few projections to the corresponding portions of the opposite SI and SII areas (Fig. 1 B, D). The dorsal portion of the trunk sends only a few projections to the opposite supplementary motor cortex. It should be pointed out that the above mentioned conclusions are derived from consistent observations that the hand and foot areas do not receive any projections from the opposite precentral gyrus. Lesions limited to the hand and foot areas are needed to document the case that the hand and foot areas do not project to the opposite side. It seems, therefore, that the interhemispheric projections of the precentral gyrus do indeed follow a projection pattern similar to that of SI, i.e., the areas representing the hand and foot in the precentral motor cortex do not project to the opposite side at all, while the axial and limbgirdle regions project not only to the homotopic areas but also to the portions of the precentral motor cortex which represent adjacent portions of the body axis. These findings are in agreement with neuronographic studies 4. Our findings also show that the axial (the face and trunk areas) and limbgirdle regions of the precentral motor cortex are connected with the corresponding portions of the opposite supplementary motor area and to some degree to the axial representation in the opposite SI and SII. Recent studies of the callosal connections of the primary visual and primary somatosensory cortical areasZ,3,5,s, 10 have shown that the callosal connections of these regions are limited to areas representing the midline of the visual and somatosensory fields, respectively. The present finding of marked callosal connections of the axial and limbgirdle representations of the precentral motor cortex adds to the Brain Research, 15 (1969) 594-596
596
SHORT COMMUNICATIONS
evidence suggesting that one of the functions of the corpus c a l l o s u m is to c o n n e c t the cortical representations o f the midline fields. The m a r k e d interhemispheric c o n n e c t i o n s of the precentral m o t o r cortex to the s u p p l e m e n t a r y m o t o r area r u n parallel to the interhemispheric projections of SI to SII2,3, s. It is of interest also to note that the s u p p l e m e n t a r y m o t o r area is connected to the opposite s u p p l e m e n t a r y m o t o r area I j u s t as SII is c o n n e c t e d to the opposite SII a,s. This parallel p a t t e r n of c o n n e c t i o n s gains added interest from the comparative architectonic studies 9, according to which the p a r a l i m b i c s u p p l e m e n t a r y m o t o r area a n d the p a r a i n s u l a r SII area represent the a n c i e n t level of m o t o r a n d sensory control, respectively. This work was supported in part by G r a n t No. N B 06209 f r o m the N a t i o n a l Institute of Neurological Diseases a n d Blindness to the A p h a s i a Research Center, Boston University Medical School. We wish to t h a n k Miss L i n d a Greszko a n d Mr. V i n c e n t D a F o r n o for technical assistance. Neurological Unit, Boston City Hospital, Boston, Mass. 02118 (U.S.A.)
DEEPAK N. PANDYA DAVID GOLD THOMAS BERGER
1 DE VITO, J. L., AND SMITH, O. A., Projections from the mesial frontal cortex (supplementary motor area) of the cerebral hemispheres and brain stem of the Macaca mulatta, J. comp. Neurol., 111 (1959) 261-277. 2 JONES, E. G., Pattern of cortical and thalamic connections of somatic sensory cortex, Nature (Lond.), 216 (1967) 704-705. 3 JONES, E. G., AND POWELL,T. P. S., The commissural connexions of the somatic sensory cortex in cat, J. Anat. (Lond.), 103 (1968) 433455. 4 MCCULLOCH, W. S., AND GAROL, H. W., Cortical origin and distribution of corpus callosum and anterior commissure in the monkey, J. Neurophysiol., 4 (1941) 555-563. 5 MYERS,R. E., The neo-cortical commissures and interhemispheric transmission of information. In E. G. ETTLINGER(Ed.), Function of the Corpus Callosum, Little, Brown and Co., Boston, 1965, pp. 1-17. 6 NAUTA,W. J. H., Silver impregnation of degenerating axons. In W. F. WINDLE(Ed.), New Research Techniques of Neuroanatomy, Thomas, Springfield, Ill., 1957, pp. 17-26. 7 PANDYA,D. N., AND KUYPERS,H. G. J. M., Cortico-cortical connections in the rhesus monkey, Brain Research, 13 (1969) 13-36. 8 PANDYA, D. N., AND VIGNOLO, L. A., Interhemispheric neocortical projections of somatosensory areas I and II in the rhesus monkey, Brain Research, 7 (1968) 300-303. 9 SANIDES, F., Comparative architectonics of the neocortex of mammals and their evolutionary interpretation (in preparation). 10 WHITTERIDGE,D., Area 18 and the vertical meridian of the visual field. In E. G. ETTLINGER(Ed.), Functions of the Corpus Callosum, Little, Brown and Co., Boston, 1965, pp. 115-120. 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, Univ. of Wisconsin Press, Madison, 1958, pp. 63-82. (Accepted July 30th, 1969)
Brain Research, 15 (1969) 594-596
SHORT COMMUNICATIONS
Inlerhemispheric connections of the precentral motor cortex in the rhesus monkey Recent anatomical investigations have shown that in rhesus monkey the interhemispheric connections of the primary somatosensory area (SI) are limited to the areas representing the face, trunk and limbgirdles, whereas no callosal connections are found in the hand and foot representation2,5, 8. These studies 2,8 also demonstrated that SI is connected non-homotopicaUy to the opposite second somatosensory area (SII). Since the postcentral gyrus (SI) and the precentral m o t o r cortex are topographically interconnected ipsilaterally 7 it would be of interest to know whether the precentral motor cortex possesses a pattern of interhemispheric connection similar to that of SI. To investigate this, lesions were made in various parts of the precentral gyrus by the method of subpial suction in 5 rhesus monkeys. The resulting patterns of fiber degeneration in the opposite hemisphere were studied by means of the modified Nauta silver impregnation technique 6. The location and extent of each lesion were
CONTRA
o
l 'l 19
Fig. 1. A, D i a g r a m o f m o n k e y cortex showing t h e locations o f t h e s u p p l e m e n t a r y m o t o r (MID, the precentral m o t o r (MI), t h e postcentral p r i m a r y s o m a t o s e n s o r y (SI) a n d t h e second sensory (SII) areas as described by W o o l s e y 11. C a n d D , D i a g r a m m a t i c representation o f the lesion o f t h e rostral b a n k o f t h e central sulcus a n d adjacent part of t h e precentral g y r u s a n d resulting fiber degeneration (indicated by dots) in t h e lateral a n d medial surfaces o f the opposite hemisphere. In B, tracings o f representative sections t a k e n f r o m t h e levels (1-7) indicated in D are shown. Abbreviations: A. S. = arcuate sulcus; C. C. = c o r p u s c a l l o s u m ; C. S. = central sulcus; C I N G . S. -cingulate sulcus; I. O. S. -- inferior occipital sulcus; I. P. S. -- intraparietal sulcus; L. F. = lateral fissure; L. S. -- lunate sulcus: P. S. = principal sulcus; S. P. D. = superior precentral dimple; S. T. S. -- superior t e m p o r a l sulcus.
Brain Research, 15 (1969) 594-596
SHORT COMMUNICATIONS
595
mapped. In all cases some damage was found in the white matter immediately subjacent to the lesioned cortex. The lesions were placed as follows: (1) along the entire extent of the rostral bank of the central sulcus and extending into the caudal portion of the precentral gyrus (Fig. 1C), (2) in the upper third of this same strip, (3) in the lower third of the same strip, (4) along the entire rostral border of the precentral gyrus and (5) in the region surrounding the superior precentral dimple. A comparison of our findings with Woolsey's 'summary diagram' of sensory motor simiusculi (Fig. 1A) 11 indicated the existence of the following arrangement. The precentral areas which contain the hand and foot representation do not project to the opposite hemisphere. However, the face and the trunk areas do project to the opposite hemisphere. The projections from the latter areas are directed both to homotopic and non-homotopic areas. In regard to the non-homotopic projection, the face area projects non-homotopically to the neck area. The ventral portion of the trunk around the superior precentral dimple and in the rostral bank of the central sulcus projects non-homotopically to the dorsal portion of the trunk area in the rostral part of the precentral gyrus, and to the tail area (Fig. 1B, D). The dorsal portion of the trunk area in the rostral part of the precentral gyrus projects nonhomotopically to the caudal parts of the precentral gyrus, exclusive of the hand and the foot areas. A further comparison of our findings with Woolsey's 'summary diagram' indicates that the face and the ventral portion of the trunk areas additionally maintain projections to the corresponding portions of the supplementary motor cortex of the opposite hemisphere and a few projections to the corresponding portions of the opposite SI and SII areas (Fig. 1 B, D). The dorsal portion of the trunk sends only a few projections to the opposite supplementary motor cortex. It should be pointed out that the above mentioned conclusions are derived from consistent observations that the hand and foot areas do not receive any projections from the opposite precentral gyrus. Lesions limited to the hand and foot areas are needed to document the case that the hand and foot areas do not project to the opposite side. It seems, therefore, that the interhemispheric projections of the precentral gyrus do indeed follow a projection pattern similar to that of SI, i.e., the areas representing the hand and foot in the precentral motor cortex do not project to the opposite side at all, while the axial and limbgirdle regions project not only to the homotopic areas but also to the portions of the precentral motor cortex which represent adjacent portions of the body axis. These findings are in agreement with neuronographic studies 4. Our findings also show that the axial (the face and trunk areas) and limbgirdle regions of the precentral motor cortex are connected with the corresponding portions of the opposite supplementary motor area and to some degree to the axial representation in the opposite SI and SII. Recent studies of the callosal connections of the primary visual and primary somatosensory cortical areasZ,3,5,s, 10 have shown that the callosal connections of these regions are limited to areas representing the midline of the visual and somatosensory fields, respectively. The present finding of marked callosal connections of the axial and limbgirdle representations of the precentral motor cortex adds to the Brain Research, 15 (1969) 594-596
596
SHORT COMMUNICATIONS
evidence suggesting that one of the functions of the corpus c a l l o s u m is to c o n n e c t the cortical representations o f the midline fields. The m a r k e d interhemispheric c o n n e c t i o n s of the precentral m o t o r cortex to the s u p p l e m e n t a r y m o t o r area r u n parallel to the interhemispheric projections of SI to SII2,3, s. It is of interest also to note that the s u p p l e m e n t a r y m o t o r area is connected to the opposite s u p p l e m e n t a r y m o t o r area I j u s t as SII is c o n n e c t e d to the opposite SII a,s. This parallel p a t t e r n of c o n n e c t i o n s gains added interest from the comparative architectonic studies 9, according to which the p a r a l i m b i c s u p p l e m e n t a r y m o t o r area a n d the p a r a i n s u l a r SII area represent the a n c i e n t level of m o t o r a n d sensory control, respectively. This work was supported in part by G r a n t No. N B 06209 f r o m the N a t i o n a l Institute of Neurological Diseases a n d Blindness to the A p h a s i a Research Center, Boston University Medical School. We wish to t h a n k Miss L i n d a Greszko a n d Mr. V i n c e n t D a F o r n o for technical assistance. Neurological Unit, Boston City Hospital, Boston, Mass. 02118 (U.S.A.)
DEEPAK N. PANDYA DAVID GOLD THOMAS BERGER
1 DE VITO, J. L., AND SMITH, O. A., Projections from the mesial frontal cortex (supplementary motor area) of the cerebral hemispheres and brain stem of the Macaca mulatta, J. comp. Neurol., 111 (1959) 261-277. 2 JONES, E. G., Pattern of cortical and thalamic connections of somatic sensory cortex, Nature (Lond.), 216 (1967) 704-705. 3 JONES, E. G., AND POWELL,T. P. S., The commissural connexions of the somatic sensory cortex in cat, J. Anat. (Lond.), 103 (1968) 433455. 4 MCCULLOCH, W. S., AND GAROL, H. W., Cortical origin and distribution of corpus callosum and anterior commissure in the monkey, J. Neurophysiol., 4 (1941) 555-563. 5 MYERS,R. E., The neo-cortical commissures and interhemispheric transmission of information. In E. G. ETTLINGER(Ed.), Function of the Corpus Callosum, Little, Brown and Co., Boston, 1965, pp. 1-17. 6 NAUTA,W. J. H., Silver impregnation of degenerating axons. In W. F. WINDLE(Ed.), New Research Techniques of Neuroanatomy, Thomas, Springfield, Ill., 1957, pp. 17-26. 7 PANDYA,D. N., AND KUYPERS,H. G. J. M., Cortico-cortical connections in the rhesus monkey, Brain Research, 13 (1969) 13-36. 8 PANDYA, D. N., AND VIGNOLO, L. A., Interhemispheric neocortical projections of somatosensory areas I and II in the rhesus monkey, Brain Research, 7 (1968) 300-303. 9 SANIDES, F., Comparative architectonics of the neocortex of mammals and their evolutionary interpretation (in preparation). 10 WHITTERIDGE,D., Area 18 and the vertical meridian of the visual field. In E. G. ETTLINGER(Ed.), Functions of the Corpus Callosum, Little, Brown and Co., Boston, 1965, pp. 115-120. 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, Univ. of Wisconsin Press, Madison, 1958, pp. 63-82. (Accepted July 30th, 1969)
Brain Research, 15 (1969) 594-596