166
Brain Research, 98 (1975) 166-171 ~ Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Short Communications
The commissural fibre connections of the primary somatic sensory cortex
M. F. SHANKS, A. J. ROCKEL AND T. P. S. POWELL Department of Human Anatomy, Oxford University, OxJbrd OXI 3QX (Great Britain)
(Accepted July 7th, 1975)
Previous studies of the commissural connections of the primary somatic sensory area in more than one species have shown that the areas of cortex containing the representation of the distal parts of the limbs neither send nor receive such fibres 8-1z. The areas of cortex which lack such commissural connections are, however, bounded posteriorly by narrow strips of cortex which are connected across the midline. Recent studies on the topographic representation in the somatic sensory area of the monkey have suggested that the representations of the hand and foot are bounded both in front and behind by strips of cortex related to the pre- and post-axial parts of the limbs16,17. It seemed possible, therefore, that there might be a commissurally connected band of cortex anterior as well as posterior to the bare area, and this possibility is of interest because such an anterior strip would be in area 3a, which has been shown to be in receipt of afferent impulses from receptors in musclO 3. In addition, there is electrophysiological evidence that the cortex of the distal limb representations may in fact be commissurally connected6,L For these reasons the commissural connections of the primary somatic sensory area have been reinvestigated. Eight monkeys and 3 cats were used and lesions of varying size were placed in the primary somatic sensory area of one side. In 3 monkeys most of the cortex of the post-central gyrus was removed by suction and in the other monkeys smaller lesions were made which involved a restricted part of the mediolateral extent of the gyrus and which extended to the depth of the central sulcus, or were confined to areas 1 and 2 on the exposed surface of the hemisphere. In the 3 cats, all of the cortex on the medial and lateral surfaces of the anterior one-third of the hemisphere was removed by suction. After survival periods of 4 or 5 days the animals were perfused with saline and 10 ~ formalin, the brains were removed and immersed for a few weeks in the fixative. Blocks of the pre- and post-central gyri of both hemispheres of the monkey brains and of the anterior thirds of the hemispheres of the cat brains were cut sagittally at 25 #m on a freezing microtome and a 1 in 10 series stained with the Fink-Heimer method 3 and an alternate series with thionine. The total pattern of degeneration of commissural fibres in the monkey was
167 studied in an experiment in which the whole of the somatic sensory cortex was removed together with adjoining parts of areas 5 and 7 (Fig. 1). The lesion extended sufficiently deep either to undercut or damage area 3a at the bottom of the central sulcus. In the sagittal sections of the opposite hemisphere the intensity and the extent of the degeneration in the post-central gyrus differed along its mediolateral extent. In the regions of the representation of the trunk and face, at the levels of the post-central dimple and below the intraparietal sulcus respectively, degeneration is found throughout the anteroposterior extent of the gyrus from the bottom of the central sulcus anteriorly and into the anterior parts of areas 5 and 7 posteriorly. The intensity of the degeneration, however, varies and is clearly heaviest in 3 narrow strips. The most anterior of these occupies area 3a at the bottom of the central sulcus, the intermediate one is at the boundary of areas 3 and 1 close to the posterior bank of the central sulcus and the most intense degeneration is seen posteriorly at the boundary of areas 2 and 5. As the degeneration is traced towards the distal limb representations the density of the degeneration gradually diminishes, particularly in area 3 in the posterior wall of the sulcus and throughout most of areas 1 and 2 on the lateral surface, but definite bands of degeneration persist and these are all situated at the boundaries of the various architectonic and functional subdivisions of the somatic sensory cortex. With the decrease in degeneration in the central parts of the subdivisions, the degeneration at the margins of the areas stands out more prominently and is found at the anterior and posterior margins of area 3a, at the junction of areas 3 and 1, between areas I and 2 and at the boundary of area 2 with either 5 or 7. As one proceeds even further from the trunk and face representations into the central parts of the hand and foot representations, there is very little degeneration throughout most of the anteroposterior extent of the post-central gyrus; however, two narrow zones of degeneration remain: at the anterior margins of area 3a and at the posterior limit of area 2. This persistent degeneration is much lighter than that found in these situations in the trunk, face or proximal limb areas, but the anterior part of area 3a and the posterior part of area 2 are commissurally connected throughout their entire mediolateral extent. The mediolateral extent of the cortex in which there is no degeneration is smaller than was found in earlier studies, as the bands of degeneration between areas 3, 1 and 2 are present in what were formerly described as 'bare areas'. The differences in the findings are almost certainly due to the use of the Fink-Heimer technique as compared to the N a u t a Gygax and because of the use of sagittal rather than coronal sections. The distribution of the degeneration in areas 5 and 7 will not be considered in detail but it may be noted that the degeneration again tends to be arranged in bands, and in certain regions of area 7 these are quite narrow, about 500/~m wide, and alternate regularly with bands of equal width in which the degeneration is much lighter. In experiments with smaller lesions in which the damage is restricted to areas 1 and 2 on the exposed surface of the hemisphere and involving a varying amount of the mediolateral extent of the postcentral gyrus, the degeneration in the opposite hemisphere has been found in all of the bands described above after a large lesion. For example, when the region of the trunk representation (Fig. 1) has been damaged with such a lesion, the degeneration in the opposite hemisphere occupies most of areas 3a, 3, 1 and 2, but is accentuated as before
168
:
"
~
)~-\
../
\
~l
J,
\
\:,\
D
1
4 3b
0
Fig. 1. Shows the distribution of the fibre and terminal degeneration in sagittal sections of the somatic sensory cortex of the contralateral hemisphere after a large (top) and small (bottom) lesion of the somatic sensory area of the monkey, and in the cat (middle). The extents of the lesions are shown by hatching, the levels of the sagittal sections by the lines (A, B, C and D) and the boundaries of the architectonic subdivisions by arrows. A and A' (in bottom figure) are at corresponding levels in the two hemispheres.
at the b o u n d a r i e s o f these subdivisions; because the density o f degeneration in the architectonic subdivisions is less than after a c o m p l e t e removal o f the somatic sensory area the b a n d s at their b o u n d a r i e s stand out more prominently. In the sagittal sections o f the u n o p e r a t e d hemisphere o f the cat, degeneration is again found to be p r e d o m i n a n t l y at architectonic b o u n d a r i e s 5 (Fig. 1). A l t h o u g h in the representations o f the t r u n k a n d face there is degeneration t h r o u g h o u t the anteroposterior extent o f the somatic sensory area, the a c c e n t u a t i o n at the b o u n d a r i e s o f areas 3a, 3, 1, 2 a n d 5 is even m o r e m a r k e d than in the monkey. In the regions o f transition into the hand a n d foot regions, the degeneration in the central p a r t s o f the architectonic subdivisions disappears and the persistent degeneration at the b o u n d a r y
Figs. 2 and 3. The differences in cytoarchitecture of the cortex at the boundary of areas 3 and 1, close to the posterior bank of the central sulcus, between the trunk region which is commissurally connected (Fig. 3) and the hand region which is not (Fig. 2). The lateral surface of the cortex is to the left and the central sulcus above. The photographs are of two sections of the same brain, 8 mm apart, x 50.
170 zones, though clearly visible in the sagittal sections, is very narrow and would be missed in coronal sections. As in the monkey, however, there is a restricted central region of the hand and foot representations where degeneration is present only at the anterior and posterior extremes of the somatic sensory cortex. The differences in distribution of the commissural fibres between the distal limb representations on the one hand and the trunk and face on the other, are paralleled by differences in cytoarchitecture (Figs. 2 and 3). In the representation of the hand, layers I1, III and IV of area 3 are composed of small cells and it is difficult to demarcate them from each other 14. Towards the trunk or face representation large or medium sized pyramidal cells appear in layer III, particularly near the posterior bank of the central sulcus and deeply at the junction with area 3a. In addition, in these regions there is an increasing columnar arrangement of the cells and the distribution of these cellular changes corresponds exactly with the distribution of the commissural fibre degeneration. In areas 1 and 2 there are similar but not such marked changes, so that in the regions which are commissurally connected the pyramidal cells are larger and the neurones are arranged more clearly in vertical columns. The present findings confirm and extend previous studies on the commissural connections of the primary somatic sensory area. In particular they show that the boundary regions between the main subdivisions are the most strongly connected, that these bands of degeneration between architectonic areas extend for some way into the distal limb representations, and that area 3a is connected throughout its whole mediolateral extent. The pattern of the commissural connections resembles closely the topographic representation in the somatic sensory area 16,17 in that the hand and foot regions form bare areas which are bounded anteriorly and posteriorly by narrow strips. It would appear that the commissural connections are heterotopical, at least within the somatic sensory area itself, in that restricted superficial lesions of the postcentral gyrus produce degeneration both anterior and posterior to the homotopical region of the opposite hemisphere. The differences in cytoarchitecture between the trunk and face regions on the one hand, which send and receive commissural fibres, and the distal limb representations on the other, which are largely devoid of such connections, strongly suggest that the commissural fibres arise predominantly at least from pyramidal cells in the deep half of layer Ill. Furthermore, the clearer arrangement of the cells into columns in these regions indicates that this feature of cytoarchitecture is related, in part at least, to the commissural pathways. It is probable that association cortical fibres also contribute to the columnar arrangement, as it has been found (unpublished observations) that the association fibres from the motor cortex into the somatic sensory area and the intrinsic association connections from areas 1 and 2 end predominantly in the same regions as the commissural fibres. In this respect the organization of the commissural connections of the somatic and visual sensory areas is quite similar, as in both areas the degeneration is in bands at the boundary regions of the cytoarchitectonic subdivisions, and in the callosally connected regions there is an increased number of pyramidal cells in layer III and a more marked columnar arrangement of the cells4,15. The correlation of a pyramidal and columnar arrangement of the cells with the presence of association and commissural fibres in these two
171 sensory areas is also in accordance with the fact that in the auditory cortex there is a well developed columnar arrangement together with strong association and commissural fibres1, 2 throughout most of these areas, while the converse is true o f the two most 'granular' areas o f the neocortex, areas 17 and 3, in which there are virtually no commissural fibres terminating. This work was supported by grants from the Medical and Science Research Councils.
1 DIAMOND, I. T., JONES, E. G., AND POWELL, T. P. S., Interhemispheric fibre connections of the auditory cortex of the cat, Brain Research, II (1968) 177-193. 2 DIAMOND, I. T., JONES, E. G., AND POWELL, T. P. S., The association connections of the auditory cortex of the cat, Brain Research, 11 (1968) 560-579. 3 FINK, R. P., AND HEIMER, L., TWO methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system, Brain Research, 4 (1967) 369-374. 4 GLICKSTEIN, M., AND WHI'I~ERIDGE, D., Degeneration of layer III pyramidal cells in area 18 following destruction of callosal input, Anat. Rec., 178 (1974) 362-363. 5 HASSLER, R., UND MUHS-CLEMENT, K., Architektonischer Aufbau des sensomotorischen und parietalen Cortex der Katze, J. Hirnforsch., 6 (1964) 377-420. 6 INNOCENTI, G. M., MANZONI, T., AND SPIDALIERI, G°, Cutaneous receptive fields of single fibres of the corpus callosum, Brain Research, 40 (1972) 507-512. 7 INNOCENTI, G. M., MANZONI, T., AND SPIDALIERI, G., Patterns of the somesthetic messages transferred through the corpus callosum, Exp. Brain Res., 19 (1974) 447-466. 8 JONES, E. G., AND POWELL, T. P. S., The commissural connections of the somatic sensory cortex in the cat, J. Anat. (Lond.), 103 (1968) 433-455. 9 JONES, E. G., AND POWELL, T. P. S., Connections of the somatic sensory cortex of the rhesus monkey, Brain, 92 (1969) 717-730. 10 JONES, E. G., AND POWELL, T. P. S., Anatomical organization of the somatosensory cortex. In A. IGGO (Ed.), Handbook of Sensory Physiology, Vol. lI, Springer, Berlin, 1973, pp. 579-620. 11 KAROL, E. A., AND PANDYA, D. N., The distribution of the corpus callosum in the rhesus monkey, Brain, 94 (1971) 471-486. 12 PANDYA, O. N., AND VIGNOLO, L. A., Interhemispheric projections of the parietal lobe in the rhesus monkey, Brain Research, 15 (1969) 49-65. 13 PHILLIPS, C. G., POWELL, T. P. S., AND WIESENDANGER, M., Projection from low-threshold muscle afferents of hand and forearm to area 3a of baboon's cortex, J. Physiol. (Lond.), 217 (1971) 419-446. 14 POWELL, T. P. S., AND MOUNTCASTLE, V. B., The cytoarchitecture of the postcentral gyrus of Macaca mulatta, Bull. Johns Hopk. Hosp., 105 (1959) 108-131. 15 SHOUMURA, K., An attempt to relate the origin and distribution of commissural fibres to the presence of large and medium pyramids in layer IlI in the cat's visual cortex, Brain Research, 67 (1974) 13-25. 16 WERNER, G., AND WHITSEL, B. L., Topology of the body representation in somatosensory area 1 of primates, J. Neurophysiol., 31 (1968) 856-869. 17 WHITSEL, B. L., DREYER, O. A., AND ROPPOLO, J. R., Determinants of the body representation in the postcentral gyrus of macaques, J. Neurophysiol., 34 (1971) 1018-1034.
Brain Research, 98 (1975) 166-171 ~ Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Short Communications
The commissural fibre connections of the primary somatic sensory cortex
M. F. SHANKS, A. J. ROCKEL AND T. P. S. POWELL Department of Human Anatomy, Oxford University, OxJbrd OXI 3QX (Great Britain)
(Accepted July 7th, 1975)
Previous studies of the commissural connections of the primary somatic sensory area in more than one species have shown that the areas of cortex containing the representation of the distal parts of the limbs neither send nor receive such fibres 8-1z. The areas of cortex which lack such commissural connections are, however, bounded posteriorly by narrow strips of cortex which are connected across the midline. Recent studies on the topographic representation in the somatic sensory area of the monkey have suggested that the representations of the hand and foot are bounded both in front and behind by strips of cortex related to the pre- and post-axial parts of the limbs16,17. It seemed possible, therefore, that there might be a commissurally connected band of cortex anterior as well as posterior to the bare area, and this possibility is of interest because such an anterior strip would be in area 3a, which has been shown to be in receipt of afferent impulses from receptors in musclO 3. In addition, there is electrophysiological evidence that the cortex of the distal limb representations may in fact be commissurally connected6,L For these reasons the commissural connections of the primary somatic sensory area have been reinvestigated. Eight monkeys and 3 cats were used and lesions of varying size were placed in the primary somatic sensory area of one side. In 3 monkeys most of the cortex of the post-central gyrus was removed by suction and in the other monkeys smaller lesions were made which involved a restricted part of the mediolateral extent of the gyrus and which extended to the depth of the central sulcus, or were confined to areas 1 and 2 on the exposed surface of the hemisphere. In the 3 cats, all of the cortex on the medial and lateral surfaces of the anterior one-third of the hemisphere was removed by suction. After survival periods of 4 or 5 days the animals were perfused with saline and 10 ~ formalin, the brains were removed and immersed for a few weeks in the fixative. Blocks of the pre- and post-central gyri of both hemispheres of the monkey brains and of the anterior thirds of the hemispheres of the cat brains were cut sagittally at 25 #m on a freezing microtome and a 1 in 10 series stained with the Fink-Heimer method 3 and an alternate series with thionine. The total pattern of degeneration of commissural fibres in the monkey was
167 studied in an experiment in which the whole of the somatic sensory cortex was removed together with adjoining parts of areas 5 and 7 (Fig. 1). The lesion extended sufficiently deep either to undercut or damage area 3a at the bottom of the central sulcus. In the sagittal sections of the opposite hemisphere the intensity and the extent of the degeneration in the post-central gyrus differed along its mediolateral extent. In the regions of the representation of the trunk and face, at the levels of the post-central dimple and below the intraparietal sulcus respectively, degeneration is found throughout the anteroposterior extent of the gyrus from the bottom of the central sulcus anteriorly and into the anterior parts of areas 5 and 7 posteriorly. The intensity of the degeneration, however, varies and is clearly heaviest in 3 narrow strips. The most anterior of these occupies area 3a at the bottom of the central sulcus, the intermediate one is at the boundary of areas 3 and 1 close to the posterior bank of the central sulcus and the most intense degeneration is seen posteriorly at the boundary of areas 2 and 5. As the degeneration is traced towards the distal limb representations the density of the degeneration gradually diminishes, particularly in area 3 in the posterior wall of the sulcus and throughout most of areas 1 and 2 on the lateral surface, but definite bands of degeneration persist and these are all situated at the boundaries of the various architectonic and functional subdivisions of the somatic sensory cortex. With the decrease in degeneration in the central parts of the subdivisions, the degeneration at the margins of the areas stands out more prominently and is found at the anterior and posterior margins of area 3a, at the junction of areas 3 and 1, between areas I and 2 and at the boundary of area 2 with either 5 or 7. As one proceeds even further from the trunk and face representations into the central parts of the hand and foot representations, there is very little degeneration throughout most of the anteroposterior extent of the post-central gyrus; however, two narrow zones of degeneration remain: at the anterior margins of area 3a and at the posterior limit of area 2. This persistent degeneration is much lighter than that found in these situations in the trunk, face or proximal limb areas, but the anterior part of area 3a and the posterior part of area 2 are commissurally connected throughout their entire mediolateral extent. The mediolateral extent of the cortex in which there is no degeneration is smaller than was found in earlier studies, as the bands of degeneration between areas 3, 1 and 2 are present in what were formerly described as 'bare areas'. The differences in the findings are almost certainly due to the use of the Fink-Heimer technique as compared to the N a u t a Gygax and because of the use of sagittal rather than coronal sections. The distribution of the degeneration in areas 5 and 7 will not be considered in detail but it may be noted that the degeneration again tends to be arranged in bands, and in certain regions of area 7 these are quite narrow, about 500/~m wide, and alternate regularly with bands of equal width in which the degeneration is much lighter. In experiments with smaller lesions in which the damage is restricted to areas 1 and 2 on the exposed surface of the hemisphere and involving a varying amount of the mediolateral extent of the postcentral gyrus, the degeneration in the opposite hemisphere has been found in all of the bands described above after a large lesion. For example, when the region of the trunk representation (Fig. 1) has been damaged with such a lesion, the degeneration in the opposite hemisphere occupies most of areas 3a, 3, 1 and 2, but is accentuated as before
168
:
"
~
)~-\
../
\
~l
J,
\
\:,\
D
1
4 3b
0
Fig. 1. Shows the distribution of the fibre and terminal degeneration in sagittal sections of the somatic sensory cortex of the contralateral hemisphere after a large (top) and small (bottom) lesion of the somatic sensory area of the monkey, and in the cat (middle). The extents of the lesions are shown by hatching, the levels of the sagittal sections by the lines (A, B, C and D) and the boundaries of the architectonic subdivisions by arrows. A and A' (in bottom figure) are at corresponding levels in the two hemispheres.
at the b o u n d a r i e s o f these subdivisions; because the density o f degeneration in the architectonic subdivisions is less than after a c o m p l e t e removal o f the somatic sensory area the b a n d s at their b o u n d a r i e s stand out more prominently. In the sagittal sections o f the u n o p e r a t e d hemisphere o f the cat, degeneration is again found to be p r e d o m i n a n t l y at architectonic b o u n d a r i e s 5 (Fig. 1). A l t h o u g h in the representations o f the t r u n k a n d face there is degeneration t h r o u g h o u t the anteroposterior extent o f the somatic sensory area, the a c c e n t u a t i o n at the b o u n d a r i e s o f areas 3a, 3, 1, 2 a n d 5 is even m o r e m a r k e d than in the monkey. In the regions o f transition into the hand a n d foot regions, the degeneration in the central p a r t s o f the architectonic subdivisions disappears and the persistent degeneration at the b o u n d a r y
Figs. 2 and 3. The differences in cytoarchitecture of the cortex at the boundary of areas 3 and 1, close to the posterior bank of the central sulcus, between the trunk region which is commissurally connected (Fig. 3) and the hand region which is not (Fig. 2). The lateral surface of the cortex is to the left and the central sulcus above. The photographs are of two sections of the same brain, 8 mm apart, x 50.
170 zones, though clearly visible in the sagittal sections, is very narrow and would be missed in coronal sections. As in the monkey, however, there is a restricted central region of the hand and foot representations where degeneration is present only at the anterior and posterior extremes of the somatic sensory cortex. The differences in distribution of the commissural fibres between the distal limb representations on the one hand and the trunk and face on the other, are paralleled by differences in cytoarchitecture (Figs. 2 and 3). In the representation of the hand, layers I1, III and IV of area 3 are composed of small cells and it is difficult to demarcate them from each other 14. Towards the trunk or face representation large or medium sized pyramidal cells appear in layer III, particularly near the posterior bank of the central sulcus and deeply at the junction with area 3a. In addition, in these regions there is an increasing columnar arrangement of the cells and the distribution of these cellular changes corresponds exactly with the distribution of the commissural fibre degeneration. In areas 1 and 2 there are similar but not such marked changes, so that in the regions which are commissurally connected the pyramidal cells are larger and the neurones are arranged more clearly in vertical columns. The present findings confirm and extend previous studies on the commissural connections of the primary somatic sensory area. In particular they show that the boundary regions between the main subdivisions are the most strongly connected, that these bands of degeneration between architectonic areas extend for some way into the distal limb representations, and that area 3a is connected throughout its whole mediolateral extent. The pattern of the commissural connections resembles closely the topographic representation in the somatic sensory area 16,17 in that the hand and foot regions form bare areas which are bounded anteriorly and posteriorly by narrow strips. It would appear that the commissural connections are heterotopical, at least within the somatic sensory area itself, in that restricted superficial lesions of the postcentral gyrus produce degeneration both anterior and posterior to the homotopical region of the opposite hemisphere. The differences in cytoarchitecture between the trunk and face regions on the one hand, which send and receive commissural fibres, and the distal limb representations on the other, which are largely devoid of such connections, strongly suggest that the commissural fibres arise predominantly at least from pyramidal cells in the deep half of layer Ill. Furthermore, the clearer arrangement of the cells into columns in these regions indicates that this feature of cytoarchitecture is related, in part at least, to the commissural pathways. It is probable that association cortical fibres also contribute to the columnar arrangement, as it has been found (unpublished observations) that the association fibres from the motor cortex into the somatic sensory area and the intrinsic association connections from areas 1 and 2 end predominantly in the same regions as the commissural fibres. In this respect the organization of the commissural connections of the somatic and visual sensory areas is quite similar, as in both areas the degeneration is in bands at the boundary regions of the cytoarchitectonic subdivisions, and in the callosally connected regions there is an increased number of pyramidal cells in layer III and a more marked columnar arrangement of the cells4,15. The correlation of a pyramidal and columnar arrangement of the cells with the presence of association and commissural fibres in these two
171 sensory areas is also in accordance with the fact that in the auditory cortex there is a well developed columnar arrangement together with strong association and commissural fibres1, 2 throughout most of these areas, while the converse is true o f the two most 'granular' areas o f the neocortex, areas 17 and 3, in which there are virtually no commissural fibres terminating. This work was supported by grants from the Medical and Science Research Councils.
1 DIAMOND, I. T., JONES, E. G., AND POWELL, T. P. S., Interhemispheric fibre connections of the auditory cortex of the cat, Brain Research, II (1968) 177-193. 2 DIAMOND, I. T., JONES, E. G., AND POWELL, T. P. S., The association connections of the auditory cortex of the cat, Brain Research, 11 (1968) 560-579. 3 FINK, R. P., AND HEIMER, L., TWO methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system, Brain Research, 4 (1967) 369-374. 4 GLICKSTEIN, M., AND WHI'I~ERIDGE, D., Degeneration of layer III pyramidal cells in area 18 following destruction of callosal input, Anat. Rec., 178 (1974) 362-363. 5 HASSLER, R., UND MUHS-CLEMENT, K., Architektonischer Aufbau des sensomotorischen und parietalen Cortex der Katze, J. Hirnforsch., 6 (1964) 377-420. 6 INNOCENTI, G. M., MANZONI, T., AND SPIDALIERI, G°, Cutaneous receptive fields of single fibres of the corpus callosum, Brain Research, 40 (1972) 507-512. 7 INNOCENTI, G. M., MANZONI, T., AND SPIDALIERI, G., Patterns of the somesthetic messages transferred through the corpus callosum, Exp. Brain Res., 19 (1974) 447-466. 8 JONES, E. G., AND POWELL, T. P. S., The commissural connections of the somatic sensory cortex in the cat, J. Anat. (Lond.), 103 (1968) 433-455. 9 JONES, E. G., AND POWELL, T. P. S., Connections of the somatic sensory cortex of the rhesus monkey, Brain, 92 (1969) 717-730. 10 JONES, E. G., AND POWELL, T. P. S., Anatomical organization of the somatosensory cortex. In A. IGGO (Ed.), Handbook of Sensory Physiology, Vol. lI, Springer, Berlin, 1973, pp. 579-620. 11 KAROL, E. A., AND PANDYA, D. N., The distribution of the corpus callosum in the rhesus monkey, Brain, 94 (1971) 471-486. 12 PANDYA, O. N., AND VIGNOLO, L. A., Interhemispheric projections of the parietal lobe in the rhesus monkey, Brain Research, 15 (1969) 49-65. 13 PHILLIPS, C. G., POWELL, T. P. S., AND WIESENDANGER, M., Projection from low-threshold muscle afferents of hand and forearm to area 3a of baboon's cortex, J. Physiol. (Lond.), 217 (1971) 419-446. 14 POWELL, T. P. S., AND MOUNTCASTLE, V. B., The cytoarchitecture of the postcentral gyrus of Macaca mulatta, Bull. Johns Hopk. Hosp., 105 (1959) 108-131. 15 SHOUMURA, K., An attempt to relate the origin and distribution of commissural fibres to the presence of large and medium pyramids in layer IlI in the cat's visual cortex, Brain Research, 67 (1974) 13-25. 16 WERNER, G., AND WHITSEL, B. L., Topology of the body representation in somatosensory area 1 of primates, J. Neurophysiol., 31 (1968) 856-869. 17 WHITSEL, B. L., DREYER, O. A., AND ROPPOLO, J. R., Determinants of the body representation in the postcentral gyrus of macaques, J. Neurophysiol., 34 (1971) 1018-1034.
