Brain Research, 514 (1990) 159-162 Elsevier
159
BRES 24045
The callosal connections of area 7b, PF in the monkey J.W. Neal Department of Human Anatomy, Oxford (U. K.) (Accepted 26 December 1989)
Key words: Cortex; CaUosal connection; Area 7b (PF); Monkey
The callosal connections of area 7b, PF, in the monkey have been studied after injections of HRP into this area in one hemisphere. On the opposite side labelled cells were present in area 7b and in certain areas that are connected with it, area 5, SII and the insular granular area. In these areas the cells are in the representations of all parts of the body except that of the distal forelimb.
The callosal connections of area 7 in the monkey have previously been studied, but mainly in relation to the medial part, area 7a or PG, and this part of area 7 is connected with most of area 7a on the opposite side of the brain, together with parts of the cortex known to send association fibres to area 7a (refs. 1, 6, 13, 17). In contrast, little information is available for area 7b or PF which is related to the somatic sensory system; following callosal section 7 and lesions of the parietal lobe 13 terminal degeneration was found throughout the surface of the lateral part of the inferior parietal lobule but there was a part of area PF on the posterior wall of the intraparietal sulcus that was free of degeneration. From earlier studies the arrangement of the callosal fibres in other somatosensory cortical areas was considered to have been established, the primary (SI) and secondary (SII) somatic sensory areas and area 5 having widespread callosal fibre connections, but in each area the cortex related to the distal parts of the limb was relatively free of callosal connections (for review see ref. 8). However, more recent investigations have shown that there are callosal connections between the cortex containing the representation of the hand in SI and SII 9. The representation of the body in area 7b is now known 16 so it has been of interest to determine the organisation of the callosal fibres between this area on opposite sides of the brain. The material used is similar to that used previously ~1'12 and need not be described in detail. Injections of various amounts of 15% H R P or W G A - H R P were made into the cortex of area 7b in 6 macaque monkeys. After survival periods of 24-72 h the brains were fixed by perfusion of a mixture of paraformaldehyde and glutaraldehyde. Frozen sections were cut at 40/zm in the coronal plane in
5 monkeys and in the sagittal plane in one animal, and a 1:20 series was processed with the dianisidine and nitroprusside (DAS) method 3 and with the tetramethylbenzidine (TMB) method t°. The sites of the injections and the distribution of the labelled cells were transferred onto a planar reconstruction of the extent of the cortex shown in Fig. 1. After a large injection of H R P that involved area 7b on the surface of the hemisphere and also extended for a short distance into the posterior wall of the intraparietal sulcus and superior wall of the lateral sulcus labelled cells were found in the contralateral parietal lobe (Fig. 2). This injection was considered to involve all parts of the representation of the body except the cortex related to the face 16. The labelled cells were found in the cortex of area 7b in the inferior parietal lobule, on the surface and also extending as a band into the posterior wall of the intraparietal sulcus close to the boundary with area 7a; no cell labelling was found in the cortex of area 7b in the lowermost part of the posterior wall of the intraparietal sulcus where there is a representation of the forepaw 16. Outside the intraparietal sulcus, labelled cells were present in the superior parietal lobule, in the part of area 5 considered to contain the representation of the leg and trunk 14. Labelled cells were also seen in the wall of the lateral sulcus in what is considered to be area SII and in the granular insular area 4'5"15'16. The cells in areas SII and the granular insular area were interpreted as being in the representations of the leg and trunk in each of these
areas4,5, is,16. In two experiments in which small injections were made into the cortex containing the representation of the face in area 7b, labelled cells were found throughout the
Correspondence: J.W. Neal, Department of Human Anatomy, South Parks Road, Oxford OX1 3QX, U.K. 0006-8993/90/$03.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)
160
",,..
A;) CG
/
~
TS
$q
/
CG
STS
R
Fig. 1. A planar reconstruction of the extent of the cortex of the
right hemisphere as shown within the interrupted lines (above). Both the outline of the surface of hemisphere and the planar reconstruction have been transposed from those shown in an earlier publication for the left hemisphere,
Fig. 2. The site of a large injection (stippled) on a planar reconstruction of the left hemisphere (above) and the distribution of the resulting cell labelling (dots) on a similar reconstruction of the right hemisphere (below).
corresponding area on the contralateral side of the brain (Fig. 3). Further labelled cells were also found around the lateral tip of the intraparietal sulcus in what is considered to be the representation of the face in area 5 (ref. 14). No labelled cells were found in areas outside area 5 and area 7b on the contralateral side of this brain. Orthograde labelling was also found in area 7b on the contralateral side following one injection in the face area of 7b. In another two experiments similar-sized injections were placed in the representation of the arm in area 7b (Fig. 4). One of these injections extended from the surface into the posterior wall of the intraparietal sulcus, whereas the other was situated on the surface and anterior wall of the lateral sulcus. Each experiment resulted in labelled cells in the representation of the arm
in the part of area 7b on the surface of the contralateral hemisphere, but neither resulted in labelling in the posterior wall of the intraparietal sulcus. After both injections a patch of cells was found the anterolateral part of the granular insular area (Ig) on the opposite side of the brain. Following injections in the leg, trunk and face representations of area 7b labelled cells were found in corresponding parts of the representation in area 5. In area Ig the cortex containing the representations of the face, arm, leg and trunk receives heterotopic callosal fibres from area 7b, while SII appears to receive heterotopic callosal connections only from the cortex of area 7b containing the representation of the leg. In contrast to the numbers of cells in homotypically con-
161 nected areas, those in the heterotopic areas were few. The labelled cells in these callosally connected areas were distributed mainly in layer III and a few in V, and the accompanying fine granularity was in layers III and IV and both were arranged in small clusters. Over several sections these clusters could be identified in comparable positions so it is probable that they formed bands orientated parallel to the fundus of the intraparietal sulcus. A r e a 7b is similar to other somatosensory areas in the parietal lobe, a large part of its extent being connected by callosal fibres to the contralateral side of the brain. In most studies on areas SI, SII and 5, the cortex related to the distal limb has been found to be relatively free of callosal fibres and this is also the case for area 7b. After
CG
injections of H R P into the cortex of area PF related to the face, trunk and leg, labelled cells of origin of callosal fibres were distributed throughout the corresponding representation in area 7b on the opposite side of the brain. A n injection placed in the cortex of 7b within the part of the representation of the fore-limb on the surface of the hemisphere, produced labelling in the contralateral area 7b, but when an injection extended into the posterior wall of the intraparietal sulcus, into the distal part of the fore-limb representation 16, no labelled cells were found in the corresponding part of the contralateral area. This is in agreement with the findings after the callosum was cut as that part of 7b in the posterior wall of the intraparietal sulcus was relatively free of terminal degeneration 7.
~~
IPS
L
CG
8TS
STS
R
R
Fig. 3. The sites of two small injections (solid black and stippled) in the cortex containing the representation of the face on a planar reconstruction of the left hemisphere (above). The distribution of the cell labelling in the right hemisphere (filled and open circles) after these two injections is shown (below).
Fig. 4. The sites of two separate injections (one solid black, the other stippled) in the cortex of area.7b containing the representation of the arm (above) and the distribution of the resulting cell labelling in the right hemisphere after each of these injections is indicated by open and filled triangles on a planar reconstruction.
162 These results on the organization of the callosal connection in 7b are of interest in view of the observations m a d e in an electrophysiological study; more than half the receptive fields that were restricted to the hands or digits were only activated by contralateral stimuli, whereas neurones that had receptive fields that included the proximal and distal parts of a limb 16, were generally activated by both contra- and ipsilateral inputs. L a b e l l e d cells were also found on the contralateral side in areas other than 7b, in areas 5, SII and the insular granular area Ig, which are all interconnected with area P F by ipsilateral cortico-cortical connections 11. No cells were found in the representation of the arm in areas 5 or SII, after an injection in the part of 7b corresponding to the arm representation. H o w e v e r , following an injection in cortex containing the representation of the face, leg and trunk in area 7b labelled cells were found in the corresponding parts of the representation on the contralateral side in area 5. It is possible that the failure to find labelled cells in each of these areas after injections in the
cortex of area 7b involving all parts of the representation of the body m a y have been due to such technical factors as the small size of some of the injections and the limited extent of area SII. Surprisingly, no cells were found in the contralateral cingulate cortex nor in the walls of the superior temporal sulcus after injections in area 7b, as after involvement of area P G 6, but these findings are, however, in agreement with those of P a n d y a and Vignolo following lesions in the lateral part of area 7 (ref. 13). These authors also showed that lesions placed in the parts of the cortex of area 7b which are now known to be related to the representation of the face and trunk p r o d u c e d degeneration in the corresponding parts of the representation in areas 5, SII and the insular granular Ig on the opposite side of the brain. The present results are also in agreement with the findings of Caminiti and Soricolli2; following large injections of H R P in the cortex of area 5 only the parts of area 7b on the opposite side of the brain related to the r e p r e s e n t a t i o n of the trunk and leg were found to contain labelled cells.
1 Andersen, R.A., Asanuma, C. and Cowan, W.M., Callosal and prefrontal associational projecting cell populations in Area 7a of the macaque monkey: a study using retrograde transported fluorescent dyes, J. Comp. NeuroL, 232 (1985) 443-455. 2 Caminiti, R. and Soriccoli, A., The callosal system of the superior parietal lobule in the monkey, J. Comp. Neurol., 237 (1985) 85-99. 3 Colman, D.R., Scalia, E and Cabrales, E., Light and electron microscopic observations on the antegrade transport of horseradish peroxidase in the optic pathway in the mouse and rat, Brain Research, 102 (1976) 156-163. 4 Friedman, D.P., Jones, E.G. and Burton, H., Representation pattern in the second somatic sensory area of the monkey cerebral cortex, J. Comp. Neurol., 192 (1980) 21-42. 5 Friedman, D.P., Murray, E.A., O'Neill, J.B. and Mishkin, M., Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch, J. Comp. Neurol., 252 (1986) 323-347. 6 Hedreen, J.G. and Yin, T.G.T., Homotopic and heterotopic callosal afferents of caudal inferior parietal lobule in Macaca mulatta, J. Comp. Neurol., 197 (1981) 605-621. 7 Karol, E.A. and Pandya, D.N., The distribution of the corpus callosum in the rhesus monkey, Brain, 94 (1971) 471-486. 8 Manzoni, T., Barbaresi, P., Conti, E and Fabri, M., The callosal connections of the primary somatosensory cortex and the neural bases of midline fusion, Exp. Brain Res., 76 (1989) 251-266. 9 Manzoni, T., Conti, E and Fabri, M., Callosal projections from area SII to SI in monkeys: anatomical organization and comparison with associations projections, J. Comp. Neurol., 252
(1986) 245-263. 10 Mesulam, M.M., Tetramethylbenzidine for horseradish peroxidase immunohistochemistry: a non-carcinogenic blue reaction product for visualizing neural afferents and efferents, J. Histochem. Cytochem., 26 (1978) 106-117. 11 Neal, J.W., Pearson, R.C.A. and Powell, T.P.S., The corticocortical connections of area 7b, PF, in the parietal lobe of the monkey, Brain Research, 419 (1987) 341-346. 12 Neal, J.W., Pearson, R.C.A. and Powell, T.P.S., The corticocortical connections within the parietotemporal lobe of area PG, 7a, in the monkey, Brain Research, 438 (1988) 343-350. 13 Pandya, D.N. and Vignolo, L.A., Interhemispheric projections of the parietal lobe in the rhesus monkey, Brain Research, 15 (1969) 49-65. 14 Pearson, R.C.A. and Powell, T.P.S., The projection of the primary somatic sensory cortex upon area 5 in the monkey, Brain Res. Rev., 9 (1985) 89-107. 15 Robinson, C.J. and Burton, H., Somatotopographic organization in the second somatosensory area of M. fascicularis, J. Comp. Neurol., 192 (1980) 43-67. 16 Robinson, C.J. and Burton, H., Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insular of M. fascicularis, J. Comp. Neurol., 192 (1980) 69-92. 17 Van Essen, D.C., Newsome, W.T. and Bixby, J.H., The pattern of interhemisphere connections and its relationship to extrastriate visual areas in the macaque monkey, J. Neurosci., 2 (1982) 265-283.
159
BRES 24045
The callosal connections of area 7b, PF in the monkey J.W. Neal Department of Human Anatomy, Oxford (U. K.) (Accepted 26 December 1989)
Key words: Cortex; CaUosal connection; Area 7b (PF); Monkey
The callosal connections of area 7b, PF, in the monkey have been studied after injections of HRP into this area in one hemisphere. On the opposite side labelled cells were present in area 7b and in certain areas that are connected with it, area 5, SII and the insular granular area. In these areas the cells are in the representations of all parts of the body except that of the distal forelimb.
The callosal connections of area 7 in the monkey have previously been studied, but mainly in relation to the medial part, area 7a or PG, and this part of area 7 is connected with most of area 7a on the opposite side of the brain, together with parts of the cortex known to send association fibres to area 7a (refs. 1, 6, 13, 17). In contrast, little information is available for area 7b or PF which is related to the somatic sensory system; following callosal section 7 and lesions of the parietal lobe 13 terminal degeneration was found throughout the surface of the lateral part of the inferior parietal lobule but there was a part of area PF on the posterior wall of the intraparietal sulcus that was free of degeneration. From earlier studies the arrangement of the callosal fibres in other somatosensory cortical areas was considered to have been established, the primary (SI) and secondary (SII) somatic sensory areas and area 5 having widespread callosal fibre connections, but in each area the cortex related to the distal parts of the limb was relatively free of callosal connections (for review see ref. 8). However, more recent investigations have shown that there are callosal connections between the cortex containing the representation of the hand in SI and SII 9. The representation of the body in area 7b is now known 16 so it has been of interest to determine the organisation of the callosal fibres between this area on opposite sides of the brain. The material used is similar to that used previously ~1'12 and need not be described in detail. Injections of various amounts of 15% H R P or W G A - H R P were made into the cortex of area 7b in 6 macaque monkeys. After survival periods of 24-72 h the brains were fixed by perfusion of a mixture of paraformaldehyde and glutaraldehyde. Frozen sections were cut at 40/zm in the coronal plane in
5 monkeys and in the sagittal plane in one animal, and a 1:20 series was processed with the dianisidine and nitroprusside (DAS) method 3 and with the tetramethylbenzidine (TMB) method t°. The sites of the injections and the distribution of the labelled cells were transferred onto a planar reconstruction of the extent of the cortex shown in Fig. 1. After a large injection of H R P that involved area 7b on the surface of the hemisphere and also extended for a short distance into the posterior wall of the intraparietal sulcus and superior wall of the lateral sulcus labelled cells were found in the contralateral parietal lobe (Fig. 2). This injection was considered to involve all parts of the representation of the body except the cortex related to the face 16. The labelled cells were found in the cortex of area 7b in the inferior parietal lobule, on the surface and also extending as a band into the posterior wall of the intraparietal sulcus close to the boundary with area 7a; no cell labelling was found in the cortex of area 7b in the lowermost part of the posterior wall of the intraparietal sulcus where there is a representation of the forepaw 16. Outside the intraparietal sulcus, labelled cells were present in the superior parietal lobule, in the part of area 5 considered to contain the representation of the leg and trunk 14. Labelled cells were also seen in the wall of the lateral sulcus in what is considered to be area SII and in the granular insular area 4'5"15'16. The cells in areas SII and the granular insular area were interpreted as being in the representations of the leg and trunk in each of these
areas4,5, is,16. In two experiments in which small injections were made into the cortex containing the representation of the face in area 7b, labelled cells were found throughout the
Correspondence: J.W. Neal, Department of Human Anatomy, South Parks Road, Oxford OX1 3QX, U.K. 0006-8993/90/$03.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)
160
",,..
A;) CG
/
~
TS
$q
/
CG
STS
R
Fig. 1. A planar reconstruction of the extent of the cortex of the
right hemisphere as shown within the interrupted lines (above). Both the outline of the surface of hemisphere and the planar reconstruction have been transposed from those shown in an earlier publication for the left hemisphere,
Fig. 2. The site of a large injection (stippled) on a planar reconstruction of the left hemisphere (above) and the distribution of the resulting cell labelling (dots) on a similar reconstruction of the right hemisphere (below).
corresponding area on the contralateral side of the brain (Fig. 3). Further labelled cells were also found around the lateral tip of the intraparietal sulcus in what is considered to be the representation of the face in area 5 (ref. 14). No labelled cells were found in areas outside area 5 and area 7b on the contralateral side of this brain. Orthograde labelling was also found in area 7b on the contralateral side following one injection in the face area of 7b. In another two experiments similar-sized injections were placed in the representation of the arm in area 7b (Fig. 4). One of these injections extended from the surface into the posterior wall of the intraparietal sulcus, whereas the other was situated on the surface and anterior wall of the lateral sulcus. Each experiment resulted in labelled cells in the representation of the arm
in the part of area 7b on the surface of the contralateral hemisphere, but neither resulted in labelling in the posterior wall of the intraparietal sulcus. After both injections a patch of cells was found the anterolateral part of the granular insular area (Ig) on the opposite side of the brain. Following injections in the leg, trunk and face representations of area 7b labelled cells were found in corresponding parts of the representation in area 5. In area Ig the cortex containing the representations of the face, arm, leg and trunk receives heterotopic callosal fibres from area 7b, while SII appears to receive heterotopic callosal connections only from the cortex of area 7b containing the representation of the leg. In contrast to the numbers of cells in homotypically con-
161 nected areas, those in the heterotopic areas were few. The labelled cells in these callosally connected areas were distributed mainly in layer III and a few in V, and the accompanying fine granularity was in layers III and IV and both were arranged in small clusters. Over several sections these clusters could be identified in comparable positions so it is probable that they formed bands orientated parallel to the fundus of the intraparietal sulcus. A r e a 7b is similar to other somatosensory areas in the parietal lobe, a large part of its extent being connected by callosal fibres to the contralateral side of the brain. In most studies on areas SI, SII and 5, the cortex related to the distal limb has been found to be relatively free of callosal fibres and this is also the case for area 7b. After
CG
injections of H R P into the cortex of area PF related to the face, trunk and leg, labelled cells of origin of callosal fibres were distributed throughout the corresponding representation in area 7b on the opposite side of the brain. A n injection placed in the cortex of 7b within the part of the representation of the fore-limb on the surface of the hemisphere, produced labelling in the contralateral area 7b, but when an injection extended into the posterior wall of the intraparietal sulcus, into the distal part of the fore-limb representation 16, no labelled cells were found in the corresponding part of the contralateral area. This is in agreement with the findings after the callosum was cut as that part of 7b in the posterior wall of the intraparietal sulcus was relatively free of terminal degeneration 7.
~~
IPS
L
CG
8TS
STS
R
R
Fig. 3. The sites of two small injections (solid black and stippled) in the cortex containing the representation of the face on a planar reconstruction of the left hemisphere (above). The distribution of the cell labelling in the right hemisphere (filled and open circles) after these two injections is shown (below).
Fig. 4. The sites of two separate injections (one solid black, the other stippled) in the cortex of area.7b containing the representation of the arm (above) and the distribution of the resulting cell labelling in the right hemisphere after each of these injections is indicated by open and filled triangles on a planar reconstruction.
162 These results on the organization of the callosal connection in 7b are of interest in view of the observations m a d e in an electrophysiological study; more than half the receptive fields that were restricted to the hands or digits were only activated by contralateral stimuli, whereas neurones that had receptive fields that included the proximal and distal parts of a limb 16, were generally activated by both contra- and ipsilateral inputs. L a b e l l e d cells were also found on the contralateral side in areas other than 7b, in areas 5, SII and the insular granular area Ig, which are all interconnected with area P F by ipsilateral cortico-cortical connections 11. No cells were found in the representation of the arm in areas 5 or SII, after an injection in the part of 7b corresponding to the arm representation. H o w e v e r , following an injection in cortex containing the representation of the face, leg and trunk in area 7b labelled cells were found in the corresponding parts of the representation on the contralateral side in area 5. It is possible that the failure to find labelled cells in each of these areas after injections in the
cortex of area 7b involving all parts of the representation of the body m a y have been due to such technical factors as the small size of some of the injections and the limited extent of area SII. Surprisingly, no cells were found in the contralateral cingulate cortex nor in the walls of the superior temporal sulcus after injections in area 7b, as after involvement of area P G 6, but these findings are, however, in agreement with those of P a n d y a and Vignolo following lesions in the lateral part of area 7 (ref. 13). These authors also showed that lesions placed in the parts of the cortex of area 7b which are now known to be related to the representation of the face and trunk p r o d u c e d degeneration in the corresponding parts of the representation in areas 5, SII and the insular granular Ig on the opposite side of the brain. The present results are also in agreement with the findings of Caminiti and Soricolli2; following large injections of H R P in the cortex of area 5 only the parts of area 7b on the opposite side of the brain related to the r e p r e s e n t a t i o n of the trunk and leg were found to contain labelled cells.
1 Andersen, R.A., Asanuma, C. and Cowan, W.M., Callosal and prefrontal associational projecting cell populations in Area 7a of the macaque monkey: a study using retrograde transported fluorescent dyes, J. Comp. NeuroL, 232 (1985) 443-455. 2 Caminiti, R. and Soriccoli, A., The callosal system of the superior parietal lobule in the monkey, J. Comp. Neurol., 237 (1985) 85-99. 3 Colman, D.R., Scalia, E and Cabrales, E., Light and electron microscopic observations on the antegrade transport of horseradish peroxidase in the optic pathway in the mouse and rat, Brain Research, 102 (1976) 156-163. 4 Friedman, D.P., Jones, E.G. and Burton, H., Representation pattern in the second somatic sensory area of the monkey cerebral cortex, J. Comp. Neurol., 192 (1980) 21-42. 5 Friedman, D.P., Murray, E.A., O'Neill, J.B. and Mishkin, M., Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch, J. Comp. Neurol., 252 (1986) 323-347. 6 Hedreen, J.G. and Yin, T.G.T., Homotopic and heterotopic callosal afferents of caudal inferior parietal lobule in Macaca mulatta, J. Comp. Neurol., 197 (1981) 605-621. 7 Karol, E.A. and Pandya, D.N., The distribution of the corpus callosum in the rhesus monkey, Brain, 94 (1971) 471-486. 8 Manzoni, T., Barbaresi, P., Conti, E and Fabri, M., The callosal connections of the primary somatosensory cortex and the neural bases of midline fusion, Exp. Brain Res., 76 (1989) 251-266. 9 Manzoni, T., Conti, E and Fabri, M., Callosal projections from area SII to SI in monkeys: anatomical organization and comparison with associations projections, J. Comp. Neurol., 252
(1986) 245-263. 10 Mesulam, M.M., Tetramethylbenzidine for horseradish peroxidase immunohistochemistry: a non-carcinogenic blue reaction product for visualizing neural afferents and efferents, J. Histochem. Cytochem., 26 (1978) 106-117. 11 Neal, J.W., Pearson, R.C.A. and Powell, T.P.S., The corticocortical connections of area 7b, PF, in the parietal lobe of the monkey, Brain Research, 419 (1987) 341-346. 12 Neal, J.W., Pearson, R.C.A. and Powell, T.P.S., The corticocortical connections within the parietotemporal lobe of area PG, 7a, in the monkey, Brain Research, 438 (1988) 343-350. 13 Pandya, D.N. and Vignolo, L.A., Interhemispheric projections of the parietal lobe in the rhesus monkey, Brain Research, 15 (1969) 49-65. 14 Pearson, R.C.A. and Powell, T.P.S., The projection of the primary somatic sensory cortex upon area 5 in the monkey, Brain Res. Rev., 9 (1985) 89-107. 15 Robinson, C.J. and Burton, H., Somatotopographic organization in the second somatosensory area of M. fascicularis, J. Comp. Neurol., 192 (1980) 43-67. 16 Robinson, C.J. and Burton, H., Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insular of M. fascicularis, J. Comp. Neurol., 192 (1980) 69-92. 17 Van Essen, D.C., Newsome, W.T. and Bixby, J.H., The pattern of interhemisphere connections and its relationship to extrastriate visual areas in the macaque monkey, J. Neurosci., 2 (1982) 265-283.
