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The organization of the connections between the cortex and the claustrum in the monkey
Brain Research, 234 (1982) 435-441 Elsevier Biomedical Press
435
The organization of the connections between, the cortex and the claustrum in the monkey
R. C. A. PEARSON, P. BRODAL, K. C. GATTER and T. P. S. POWELL Department of Human Anatomy, South Parks Road, Oxford, OX1 3QX ( U.K.)
(Accepted November 19th, 1981) Key words: claustrum - - cortex - - monkey
The distribution of labelled cells and of extracellular granules in the claustrum has been studied after injections of horseradish peroxidase in several areas of the neocortex. The frontal and parietal lobes are related to the anterior and posterior halves respectively of the claustrum, and the occipital and temporal cortex to the posterior and inferior margins. Parts of the claustrum related to areas of the cortex in the frontal lobe overlap considerably in the antero-posterior dimension with parts related to widely separated but interconnected areas of the parieto-temporal cortex. Areas of cortex within one lobe which are interconnected are related to parts of the claustrum which overlap in the dorsoventral dimension. The relationship of the basal ganglia with the cerebral cortex has been considerably elucidated in recent years. The entire cortex projects upon the striatum (caudate nucleus and putamen) in a well-organized manner2,S,lS, 19, and the termination of fibres from quite separate areas in the frontal and parieto-temporal lobes that are strongly interconnected by association fibres have been found to overlap 5,16,20. Like the striatum, the claustrum also receives fibres from the entire cortexZ, s,14, and in addition there is a reciprocal projection from the claustrum to the cortex~,9,11,18-15. The connections between the cortex and the claustrum are well-organized but it is not known whether, like the cortico-striate projection, there is overlap between the claustral connections with widely separated but interconnected areas of the cortex. I f there is such overlap it would be of interest to determine the manner and extent of it between the parts of the claustrum connected to those areas in the frontal and parietotemporal lobes that are sequentially linked in a series related to one or other of the major sensory systems 7. The distribution of labelled cells and of orthogradely transported enzyme in the claustrum has now been studied with reference to these questions after injections of horseradish peroxidase (HRP) into m a n y areas of the cortex. Nine brains from a large series of experiments will be described. Under pentobarbitone anaesthesia and with aseptic precautions single or multiple (3) injections of 20 % H R P totalling 0.2-0.5/~1 were made into different parts of the cortex on the lateral surface of the cerebral hemisphere. The animals were perfused 40-50 h 0006-8993/82/0000-0000/$02.75 © Elsevier Biomedical Press
436 after o p e r a t i o n with a mixture o f 2 o / p a r a f o r m a l d e h y d e a n d 1 ~!/,~glutaraldehyde. The b r a i n s were left for 24 h in the fixative at 4 °C, after which blocks o f the cortex a n d o f the rest o f the hemispheres were cut a n d placed in 30 ~ sucrose at 4 °C until they sank. Sections were cut at 40 # m on a freezing m i c r o t o m e , the cortex beiog cut in either the sagittal or c o r o n a l plane a n d the rest o f the hemispheres in the c o r o n a l p l a n e ; the sections were processed with the dianisidine a n d n i t r o p r u s s i d e m e t h o d 4. A 1:10 series o f sections was i n c u b a t e d a n d a l t e r n a t e sections were c o u n t e r s t a i n e d with neutral red. A r e c o n s t r u c t i o n o f the outline o f the c l a u s t r u m (Fig. 1) was m a d e f r o m the counterstained series.
®
[nterior~
Fig. 1. The sites of injection of HRP in 4 separate brains (A) and the distribution of the resulting labelling on a reconstruction of the claustrum (C). The sites of the labelling on a regular 1:40 series of coronal sections of the claustrum are shown in B and D. In B, the dotted region is that related to SI and the part in solid black to areas 8 and 9, and in D the dotted region is related to areas 17 and 18and the solid black to area 4. Med, medlal; Lat, lateral.
437 In all experiments the labelled cells in the claustrum were palely stained, were arranged in clusters amongst unlabelled cells and were concentrated in one part of the claustrum with progressively fewer as one moved away from the main focus. Accompanying and co-extensive with the cells were numerous fine extraceUu|ar granules, indicative of orthograde transport of enzyme and showing that the connections between the claustrum and the cortex are precisely reciprocal. In the 4 experiments shown in Fig. 1, areas of the cortex in front of and behind the central sulcus which are functionally related and interconnected were injected with HRP. Following an injection in the somatic sensory cortex in the postcentral gyrus limited to the cortex of areas 3, 1 and 2 and within the representation of the upper limb, labelled cells and extracellulat granules are found in the dorsal part of the elaustrum from just in front of the middle of its antero-posterior extent to near the caudal end. An injection of comparable size in area 4 in the precentral gyrus, involving the cortex on the lateral surface and anterior wall of the central sulcus, results in a band of labelled cells and granules in a closely similar part of the dorso-ventral extent of the claustrum but more anteriorly placed. The conside~able overlap of the bands of labelling in these two experiments in which adjoining areas were injected is not surprising, but that a similar degree of overlap may be found after injections of two widely separated but interconnected areas is shown in the other two experiments. A large injection in the posterior parts of areas 17 and 18 in the inferior wall of the calcarine sulcus and inferior surface of the hemisphere close to the occipital pole has resulted in labelling along the postero-inferior margin of the claustrum. In sections over this extent the labelling is quite clearly restricted to the medial half of the crosssectional area (Fig. 1). Overlap with this region of labelling is found after an injection in the frontal lobe affecting both banks of the posterior half of the principal sulcus and the anterior wall of the arcuate sulcus (aleas 8 and 9 of Brodman 1 or 8A, 45 and 46 of Walker17); the labelling in the claustrum extends over most of its antero-posterior extent, being greater anteriorly and forming a narrow band along the postero-inferior margin where, as in the previous experiment, it is in the medial half. This distribution, including the localization to the medial half of the claustrum, is in complete agreement with that described after injections of proline into area 810. The sites of injection in 5 further brains are shown in Fig. 2A. The injections into areas 5 and 7 of the parietal lobe are confined within the cortex of these areas, but the large injection into area 6 has involved the underlying white matter and the anterior margin of area 4. Of the labelled bands in the claustrum resulting from these injections (Fig. 2B) there is considerable overlap in the antero-posterior dimension between those related to areas 5 and 6, which are interconnected by association fibres, but not between areas 7 and 6 which are not. The bands of labelling related to areas 5 and 7 overlap in the vertical dimension, and that related to area 6 with some of those shown in Fig. 1 ; the significance of the vertical overlap will be considered later. The sites of injection in the frontal and temporal lobes in the other two experiments shown in Fig. 2A are in areas of the cortex that are known to be connected. The labelling in the claustrum (Fig. 2C and D) due to the injection in the middle of the superior temporal gyrus, area 22 and including the auditory cortex, is along the inferior margin and is
438 confined to the lateral part of the cross-sectional area with no overlap into the medial half where the labelling after injection into area 17 is found. The band of labelling following injection of the superior temporal gyrus does, however, overlap in both the medio-lateral and antero-posterior dimensions with that resulting from injections into the part of the frontal cortex with which it is connected, area 12 of Walker, just below the principal sulcus. These and other experiments show that the cortex of the frontal lobe is related to the anterior half of the claustrum and that of the parietal lobe to the posterior half, while the occipital and temporal cortex are related to the posterior and inferior
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Fig. 2. The sites of injection of HRP in 5 further experiments (A), and the distribution of the labelling on reconstructions of the ¢laustrum (B and C). In D is the site of the labelling following injections in areas 22 (dots) and 12 (solid black) on coronal sections at the level of the vertical line in C. Med, medial; Lat, lateral.
439
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n
,.
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O
Fig. 3. The pattern of overlap between the parts of the claustrum related to the areas of cortex in the frontal and parietal lobes connected with the somatic sensory system. In A, S1 of the parietal lobe is connected with area 4 of the frontal lobe (solid arrow heads) and the parts of the claustrum related to these areas overlap antero-posteriorly (horizontal hatching). Within the parietal lobe S1 is connected with area 5 (open arrow heads) and in the claustrum there is overlap in the vertical dimension (vertical hatching) between the related parts, and there is similar vertical overlap between the parts of the claustrum related to areas 4 and 6 within the frontal lobe which are interconnected. In turn area 5 is connected with area 6 (solid arrow heads) and there is again antero-posterior overlap between the related parts of the claustrum. The further steps in the progression on the somatic sensory pathway are shown in B. Within the parietal lobe area 5 projects to area 7 and within the frontal lobe areas 6 and 9 are interconnected; in the claustrum there is vertical overlap (vertical hatching) between the parts related to areas 5 and 7 and between those related to areas 6 and 9. Area 7 of the parietal lobe is interconnected with area 9 of the frontal lobe and there is overlap in the antero-posterior dimension (horizontal hatching) between the related parts of the claustrum. Arrows with solid heads denote connection between the frontal and parietal lobes, arrows with open heads connections within the frontal or parietal lobe.
m a r g i n s r e s p e c t i v e l y ; t h e p a r t s o f t h e c l a u s t r u m t h a t h a v e n o t b e e n l a b e l l e d in t h e s e e x p e r i m e n t s , t h e a n t e r i o r a n d d o r s a l m a r g i n s , a r e a l m o s t c e r t a i n l y r e l a t e d to t h e prefrontal and cingulate areas respectively. A common
feature of most of these
440 experiments with injections of H R P into individual areas of the cortex is that the resulting labelling in the claustrum has been in the form of bands which in general are disposed with their long axes in the antero-posterior dimension. As in the corticostriate projection 5,16,z0, the cortico-claustral connections from areas of the cortex in the frontal lobe terminate in bands which overlap considerably in the antero-posterior dimension with fibres from widely separated but interconnected areas in the parietotemporal lobe, and a similar overlap is present in the reciprocal claustro-cortlcal projection. Areas of cortex within one lobe which are interconnected are related to bands within the claustrum which overlap in the dorso-ventral dimension. No overlap is present between parts of the claustrum which are related to cortical areas that are not connected; even where the parts of the claustrum related to such cortical areas occupy the same antero-posterior and dorso-ventral positions, as in the experiments with injections in the visual and superior temporal cortex, the labelling is quite distinct in the medio-lateral dimension. The significance of the overlap may be found in the progression of cortical connections that has been shown to extend outwards from the main sensory areas into both the parieto-temporal and frontal lobes with an interlocking of each new parietotemporal and frontal step 7. The parts of the claustrum related to the areas in the sequence of connections within the somatic sensory system are shown in Fig. 3; the bands related to areas of the fiontal and parietal cortex which are interlocked overlap in the antero-posterior dimension. Thus, the parts of the claustrum related to S1 and 4, to 5 and 6, and to 7 and 9, all respectively overlap antero-posteriorly whereas there is dorso-ventral overlap between the parts related to areas within the parietal lobe which are connected, S1 with 5 and 5 with 7, and similarly between those related to areas within the frontal lobe that are connected, 4 with 6 and 6 with 9. These conclusions are confirmed by several other experiments which have not been described, and a similar overlapping relationship can be shown for the cortical areas comprising the visual and auditory pathways. It might be predicted that similar overlap would be found between those parts of the claustrum related to the cingulate and area 77,12. As a result of the overlap one cortical area may be able to influence another not only through the association cortical fibres passing between them but also through the claustrum, but whether adjoining clusters of cells project to individual areas remains to be determined. 1 Brodman, K., Vergleichende Lokalisationlehre der Grosshirnrinde in lnhren Prinzipien Dargestellt aufGrund des ZeUenbaues, Barth, Leipzig, 1909, 151. 2 Carman, J. B., Cowan, W. M. and Powell, T. P. S., The organization of the cortico-striate connexions in the rabbit, Brain, 86 (1963) 525-562. 3 Carman, J. B., Cowan, W. M. and Powell, T. P. S., The cortical projection upon the claustrum, J. Neurol. Neurosurg. Psychiat., 27 (1964) 46-51. 4 Colman, D. R., Scalia, F. 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. 5 Goldman, P. S. and Nauta, W. J. H., An intricately patterned prefronto-caudate projection in the rhesus monkey, J. comp. NeuroL, 171 (1977) 369-386. 6 Hughes, H. C., Efferent organization of the cat pulvinar complex, with a note on bilateral claustrocortical and reticulocortical connections, J. comp. Neurol., 193 (1980) 937-963.
441 7 Jones, E. G. and Poweli, T. P. S., An anatomical study of converging sensory pathways within the cerebral cortex of the monkey, Brain, 93 (1970) 793-820. 8 Kemp, J. M. and Powell, T. P. S., The cortico-striate projection in the monkey, Brain, 93 (1970) 525-546. 9 Kievit, J. and Kuypers, H. G. J. M., Subcortical afferents to the frontal lobe in the rhesus monkey studied by means of retrograde horseradish peroxidase transport, Brain Research, 85 (1975) 261-266. 10 Kiinzle, H. and Akert, K., Efferent connections of cortical area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique, J. comp. Neurol., 173 (1977) 147-164. 11 Macchi, G., Bentivoglio, M., Minciacchi, D. and Molinari, M., The organization of the claustroneocortical projections in the cat studied by means of the HRP retrograde axonal transport, J. comp. NeuroL, 195 (1981) 681-695. 12 Mesulam, M.-M., Van Hoesen, G. W., Pandya, D. N. and Geschwind, N., Limbic and sensory connections of the inferior parietal lobule (area PG) in the rhesus monkey: a study with a new method for horseradish peroxidase histochemistry, Brain Research, 136 (1977) 393-414. 13 Narkiewicz, O., Degenerations in the claustrum after regional neocortical ablations in the cat, J. comp. Neurol., 123 (1964) 335-356. 14 Olson, C. R. and Graybiel, A. M., Sensory maps in the claustrum of the cat, Nature (Lond.), 288 (1980) 479-481. 15 Riche, D. and Lanoir, J., Some claustro-cortical connections in the cat and baboon as studied by retrograde horseradish peroxidase transport, J. comp. Neurol., 177 (1978) 435--444. 16 Van Hoesen, G. W., Yeterian, E. H. and Lavizzo-Mourey, R., Widespread corticostriate projections from temporal cortex of the rhesus monkey, J. comp. NeuroL, 199 (1981) 205-219. 17 Walker, A. E., A cytoarchitectural study of the prefrontal area of the macaque monkey, J. comp. Neurol., 73 (1940) 59-86. 18 Webster, K. E., The cortico-striate interrelations in the albino rat, J. Anat. (Lond.), 95 (1961) 532-544. 19 Webster, K. E., The cortico-striatal projection in the cat, J. Anat. (Lond.), 99 (1965) 329-337. 20 Yeterian, E. H. and Van Hoesen, G. W., Cortico-striate projections in the rhesus monkey: the organization of certain cortico-caudate connections, Brain Research, 139 (1978) 43-63.
435
The organization of the connections between, the cortex and the claustrum in the monkey
R. C. A. PEARSON, P. BRODAL, K. C. GATTER and T. P. S. POWELL Department of Human Anatomy, South Parks Road, Oxford, OX1 3QX ( U.K.)
(Accepted November 19th, 1981) Key words: claustrum - - cortex - - monkey
The distribution of labelled cells and of extracellular granules in the claustrum has been studied after injections of horseradish peroxidase in several areas of the neocortex. The frontal and parietal lobes are related to the anterior and posterior halves respectively of the claustrum, and the occipital and temporal cortex to the posterior and inferior margins. Parts of the claustrum related to areas of the cortex in the frontal lobe overlap considerably in the antero-posterior dimension with parts related to widely separated but interconnected areas of the parieto-temporal cortex. Areas of cortex within one lobe which are interconnected are related to parts of the claustrum which overlap in the dorsoventral dimension. The relationship of the basal ganglia with the cerebral cortex has been considerably elucidated in recent years. The entire cortex projects upon the striatum (caudate nucleus and putamen) in a well-organized manner2,S,lS, 19, and the termination of fibres from quite separate areas in the frontal and parieto-temporal lobes that are strongly interconnected by association fibres have been found to overlap 5,16,20. Like the striatum, the claustrum also receives fibres from the entire cortexZ, s,14, and in addition there is a reciprocal projection from the claustrum to the cortex~,9,11,18-15. The connections between the cortex and the claustrum are well-organized but it is not known whether, like the cortico-striate projection, there is overlap between the claustral connections with widely separated but interconnected areas of the cortex. I f there is such overlap it would be of interest to determine the manner and extent of it between the parts of the claustrum connected to those areas in the frontal and parietotemporal lobes that are sequentially linked in a series related to one or other of the major sensory systems 7. The distribution of labelled cells and of orthogradely transported enzyme in the claustrum has now been studied with reference to these questions after injections of horseradish peroxidase (HRP) into m a n y areas of the cortex. Nine brains from a large series of experiments will be described. Under pentobarbitone anaesthesia and with aseptic precautions single or multiple (3) injections of 20 % H R P totalling 0.2-0.5/~1 were made into different parts of the cortex on the lateral surface of the cerebral hemisphere. The animals were perfused 40-50 h 0006-8993/82/0000-0000/$02.75 © Elsevier Biomedical Press
436 after o p e r a t i o n with a mixture o f 2 o / p a r a f o r m a l d e h y d e a n d 1 ~!/,~glutaraldehyde. The b r a i n s were left for 24 h in the fixative at 4 °C, after which blocks o f the cortex a n d o f the rest o f the hemispheres were cut a n d placed in 30 ~ sucrose at 4 °C until they sank. Sections were cut at 40 # m on a freezing m i c r o t o m e , the cortex beiog cut in either the sagittal or c o r o n a l plane a n d the rest o f the hemispheres in the c o r o n a l p l a n e ; the sections were processed with the dianisidine a n d n i t r o p r u s s i d e m e t h o d 4. A 1:10 series o f sections was i n c u b a t e d a n d a l t e r n a t e sections were c o u n t e r s t a i n e d with neutral red. A r e c o n s t r u c t i o n o f the outline o f the c l a u s t r u m (Fig. 1) was m a d e f r o m the counterstained series.
®
[nterior~
Fig. 1. The sites of injection of HRP in 4 separate brains (A) and the distribution of the resulting labelling on a reconstruction of the claustrum (C). The sites of the labelling on a regular 1:40 series of coronal sections of the claustrum are shown in B and D. In B, the dotted region is that related to SI and the part in solid black to areas 8 and 9, and in D the dotted region is related to areas 17 and 18and the solid black to area 4. Med, medlal; Lat, lateral.
437 In all experiments the labelled cells in the claustrum were palely stained, were arranged in clusters amongst unlabelled cells and were concentrated in one part of the claustrum with progressively fewer as one moved away from the main focus. Accompanying and co-extensive with the cells were numerous fine extraceUu|ar granules, indicative of orthograde transport of enzyme and showing that the connections between the claustrum and the cortex are precisely reciprocal. In the 4 experiments shown in Fig. 1, areas of the cortex in front of and behind the central sulcus which are functionally related and interconnected were injected with HRP. Following an injection in the somatic sensory cortex in the postcentral gyrus limited to the cortex of areas 3, 1 and 2 and within the representation of the upper limb, labelled cells and extracellulat granules are found in the dorsal part of the elaustrum from just in front of the middle of its antero-posterior extent to near the caudal end. An injection of comparable size in area 4 in the precentral gyrus, involving the cortex on the lateral surface and anterior wall of the central sulcus, results in a band of labelled cells and granules in a closely similar part of the dorso-ventral extent of the claustrum but more anteriorly placed. The conside~able overlap of the bands of labelling in these two experiments in which adjoining areas were injected is not surprising, but that a similar degree of overlap may be found after injections of two widely separated but interconnected areas is shown in the other two experiments. A large injection in the posterior parts of areas 17 and 18 in the inferior wall of the calcarine sulcus and inferior surface of the hemisphere close to the occipital pole has resulted in labelling along the postero-inferior margin of the claustrum. In sections over this extent the labelling is quite clearly restricted to the medial half of the crosssectional area (Fig. 1). Overlap with this region of labelling is found after an injection in the frontal lobe affecting both banks of the posterior half of the principal sulcus and the anterior wall of the arcuate sulcus (aleas 8 and 9 of Brodman 1 or 8A, 45 and 46 of Walker17); the labelling in the claustrum extends over most of its antero-posterior extent, being greater anteriorly and forming a narrow band along the postero-inferior margin where, as in the previous experiment, it is in the medial half. This distribution, including the localization to the medial half of the claustrum, is in complete agreement with that described after injections of proline into area 810. The sites of injection in 5 further brains are shown in Fig. 2A. The injections into areas 5 and 7 of the parietal lobe are confined within the cortex of these areas, but the large injection into area 6 has involved the underlying white matter and the anterior margin of area 4. Of the labelled bands in the claustrum resulting from these injections (Fig. 2B) there is considerable overlap in the antero-posterior dimension between those related to areas 5 and 6, which are interconnected by association fibres, but not between areas 7 and 6 which are not. The bands of labelling related to areas 5 and 7 overlap in the vertical dimension, and that related to area 6 with some of those shown in Fig. 1 ; the significance of the vertical overlap will be considered later. The sites of injection in the frontal and temporal lobes in the other two experiments shown in Fig. 2A are in areas of the cortex that are known to be connected. The labelling in the claustrum (Fig. 2C and D) due to the injection in the middle of the superior temporal gyrus, area 22 and including the auditory cortex, is along the inferior margin and is
438 confined to the lateral part of the cross-sectional area with no overlap into the medial half where the labelling after injection into area 17 is found. The band of labelling following injection of the superior temporal gyrus does, however, overlap in both the medio-lateral and antero-posterior dimensions with that resulting from injections into the part of the frontal cortex with which it is connected, area 12 of Walker, just below the principal sulcus. These and other experiments show that the cortex of the frontal lobe is related to the anterior half of the claustrum and that of the parietal lobe to the posterior half, while the occipital and temporal cortex are related to the posterior and inferior
®
©
Fig. 2. The sites of injection of HRP in 5 further experiments (A), and the distribution of the labelling on reconstructions of the ¢laustrum (B and C). In D is the site of the labelling following injections in areas 22 (dots) and 12 (solid black) on coronal sections at the level of the vertical line in C. Med, medial; Lat, lateral.
439
fd,t"
n
,.
lnferior~
O
Fig. 3. The pattern of overlap between the parts of the claustrum related to the areas of cortex in the frontal and parietal lobes connected with the somatic sensory system. In A, S1 of the parietal lobe is connected with area 4 of the frontal lobe (solid arrow heads) and the parts of the claustrum related to these areas overlap antero-posteriorly (horizontal hatching). Within the parietal lobe S1 is connected with area 5 (open arrow heads) and in the claustrum there is overlap in the vertical dimension (vertical hatching) between the related parts, and there is similar vertical overlap between the parts of the claustrum related to areas 4 and 6 within the frontal lobe which are interconnected. In turn area 5 is connected with area 6 (solid arrow heads) and there is again antero-posterior overlap between the related parts of the claustrum. The further steps in the progression on the somatic sensory pathway are shown in B. Within the parietal lobe area 5 projects to area 7 and within the frontal lobe areas 6 and 9 are interconnected; in the claustrum there is vertical overlap (vertical hatching) between the parts related to areas 5 and 7 and between those related to areas 6 and 9. Area 7 of the parietal lobe is interconnected with area 9 of the frontal lobe and there is overlap in the antero-posterior dimension (horizontal hatching) between the related parts of the claustrum. Arrows with solid heads denote connection between the frontal and parietal lobes, arrows with open heads connections within the frontal or parietal lobe.
m a r g i n s r e s p e c t i v e l y ; t h e p a r t s o f t h e c l a u s t r u m t h a t h a v e n o t b e e n l a b e l l e d in t h e s e e x p e r i m e n t s , t h e a n t e r i o r a n d d o r s a l m a r g i n s , a r e a l m o s t c e r t a i n l y r e l a t e d to t h e prefrontal and cingulate areas respectively. A common
feature of most of these
440 experiments with injections of H R P into individual areas of the cortex is that the resulting labelling in the claustrum has been in the form of bands which in general are disposed with their long axes in the antero-posterior dimension. As in the corticostriate projection 5,16,z0, the cortico-claustral connections from areas of the cortex in the frontal lobe terminate in bands which overlap considerably in the antero-posterior dimension with fibres from widely separated but interconnected areas in the parietotemporal lobe, and a similar overlap is present in the reciprocal claustro-cortlcal projection. Areas of cortex within one lobe which are interconnected are related to bands within the claustrum which overlap in the dorso-ventral dimension. No overlap is present between parts of the claustrum which are related to cortical areas that are not connected; even where the parts of the claustrum related to such cortical areas occupy the same antero-posterior and dorso-ventral positions, as in the experiments with injections in the visual and superior temporal cortex, the labelling is quite distinct in the medio-lateral dimension. The significance of the overlap may be found in the progression of cortical connections that has been shown to extend outwards from the main sensory areas into both the parieto-temporal and frontal lobes with an interlocking of each new parietotemporal and frontal step 7. The parts of the claustrum related to the areas in the sequence of connections within the somatic sensory system are shown in Fig. 3; the bands related to areas of the fiontal and parietal cortex which are interlocked overlap in the antero-posterior dimension. Thus, the parts of the claustrum related to S1 and 4, to 5 and 6, and to 7 and 9, all respectively overlap antero-posteriorly whereas there is dorso-ventral overlap between the parts related to areas within the parietal lobe which are connected, S1 with 5 and 5 with 7, and similarly between those related to areas within the frontal lobe that are connected, 4 with 6 and 6 with 9. These conclusions are confirmed by several other experiments which have not been described, and a similar overlapping relationship can be shown for the cortical areas comprising the visual and auditory pathways. It might be predicted that similar overlap would be found between those parts of the claustrum related to the cingulate and area 77,12. As a result of the overlap one cortical area may be able to influence another not only through the association cortical fibres passing between them but also through the claustrum, but whether adjoining clusters of cells project to individual areas remains to be determined. 1 Brodman, K., Vergleichende Lokalisationlehre der Grosshirnrinde in lnhren Prinzipien Dargestellt aufGrund des ZeUenbaues, Barth, Leipzig, 1909, 151. 2 Carman, J. B., Cowan, W. M. and Powell, T. P. S., The organization of the cortico-striate connexions in the rabbit, Brain, 86 (1963) 525-562. 3 Carman, J. B., Cowan, W. M. and Powell, T. P. S., The cortical projection upon the claustrum, J. Neurol. Neurosurg. Psychiat., 27 (1964) 46-51. 4 Colman, D. R., Scalia, F. 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. 5 Goldman, P. S. and Nauta, W. J. H., An intricately patterned prefronto-caudate projection in the rhesus monkey, J. comp. NeuroL, 171 (1977) 369-386. 6 Hughes, H. C., Efferent organization of the cat pulvinar complex, with a note on bilateral claustrocortical and reticulocortical connections, J. comp. Neurol., 193 (1980) 937-963.
441 7 Jones, E. G. and Poweli, T. P. S., An anatomical study of converging sensory pathways within the cerebral cortex of the monkey, Brain, 93 (1970) 793-820. 8 Kemp, J. M. and Powell, T. P. S., The cortico-striate projection in the monkey, Brain, 93 (1970) 525-546. 9 Kievit, J. and Kuypers, H. G. J. M., Subcortical afferents to the frontal lobe in the rhesus monkey studied by means of retrograde horseradish peroxidase transport, Brain Research, 85 (1975) 261-266. 10 Kiinzle, H. and Akert, K., Efferent connections of cortical area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique, J. comp. Neurol., 173 (1977) 147-164. 11 Macchi, G., Bentivoglio, M., Minciacchi, D. and Molinari, M., The organization of the claustroneocortical projections in the cat studied by means of the HRP retrograde axonal transport, J. comp. NeuroL, 195 (1981) 681-695. 12 Mesulam, M.-M., Van Hoesen, G. W., Pandya, D. N. and Geschwind, N., Limbic and sensory connections of the inferior parietal lobule (area PG) in the rhesus monkey: a study with a new method for horseradish peroxidase histochemistry, Brain Research, 136 (1977) 393-414. 13 Narkiewicz, O., Degenerations in the claustrum after regional neocortical ablations in the cat, J. comp. Neurol., 123 (1964) 335-356. 14 Olson, C. R. and Graybiel, A. M., Sensory maps in the claustrum of the cat, Nature (Lond.), 288 (1980) 479-481. 15 Riche, D. and Lanoir, J., Some claustro-cortical connections in the cat and baboon as studied by retrograde horseradish peroxidase transport, J. comp. Neurol., 177 (1978) 435--444. 16 Van Hoesen, G. W., Yeterian, E. H. and Lavizzo-Mourey, R., Widespread corticostriate projections from temporal cortex of the rhesus monkey, J. comp. NeuroL, 199 (1981) 205-219. 17 Walker, A. E., A cytoarchitectural study of the prefrontal area of the macaque monkey, J. comp. Neurol., 73 (1940) 59-86. 18 Webster, K. E., The cortico-striate interrelations in the albino rat, J. Anat. (Lond.), 95 (1961) 532-544. 19 Webster, K. E., The cortico-striatal projection in the cat, J. Anat. (Lond.), 99 (1965) 329-337. 20 Yeterian, E. H. and Van Hoesen, G. W., Cortico-striate projections in the rhesus monkey: the organization of certain cortico-caudate connections, Brain Research, 139 (1978) 43-63.