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An intrahemispheric columnar projection between two cortical multisensory convergence areas (inferior parietal lobule and prefrontal cortex): An anterograde study in macaque using HRP gel
Neuroscience Letters, 18 (1980) 119-124 © Elsevier/North-Holland Scientific Publishers Ltd.
119
AN INTRAHEMISPHERIC COLUMNAR PROJECTION BETWEEN TWO CORTICAL MULTISENSORY CONVERGENCE AREAS (INFERIOR PARIETAL LOBULE AND PREFRONTAL CORTEX): AN ANTEROGRADE STUDY IN MACAQUE USING HRP GEL
G.R. LE1CHNETZ
Department of Anatomy, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298 (U.S.A.) (Received March 24th, 1980) (Accepted March 28th, 1980)
SUMMARY
Horseradish peroxidase (HRP) gel and tetramethylbenzidine neurohistochemistry were used successfully in demonstrating the columnar organization of an intrahemispheric projection from the inferior parietal lobule to the prefrontal cortex in the macaque monkey. Following an HRP gel implant within the upper portion of the posterior (caudal) bank of the intraparietal sulcus, a prominent anterograde terminal projection field, consisting of alternate light and dark (300-500 ~m) columns, was observed using low-power dark-field microscopy in the caudal third of the sulcus principalis cortex (area 46). At higher magnification large numbers of small retrogradely-labeled pyramidal cells were present in layers III and V of the same cortex. The regionally-specific projection, coupled with its discrete anatomical organization, lends support to the reputed functional/behavioral subsectors within the prefrontal cortex and its apparent capacity for spatial representation.
The phenomenon of columnar organization with the mammalian cerebral cortex is now well established, and this unique anatomical feature is not restricted to primary sensory areas, but has been shown by Goldman and Nauta [4] to also occur in association, limbic and motor cortex. In the course of a comprehensive study of the connections of both prefrontal and inferior parietal cortex in macaque monkeys a dramatic demonstration of cortical 'columns' became apparent in the sulcus principalis cortex following an HRP gel implant (48 h survival) in the inferior parietal lobule, area PG of Von Bonin and Bailey [12]. The extensive and reciprocal inter-
120 connectivity between these two cortical regions has previously been established on the basis of both silver [1, 8, 11] and H R P studies [2, 7, 9]. The H R P polyacrylamide gel used in this study in combination with highly sensitive tetramethylbenzidine (TMB) neurohistochemistry (see ref. 10 for methods) and dark-field microscopy provided exquisite visualization of both anterogradelyand retrogradely-transported H R P . In the case illustrated (Fig. 1), two spear-like solid H R P gel fragments were introduced through a short slit in the pia on the lip of the upper caudal (posterior) bank of the intraparietal sulcus, and pushed into the sulcal cortex, parallel to the sulcus. The enzyme filled the middle to dorsal intraparietal sulcal cortex and spread caudally into approximately the rostrat half of the crown of the inferior parietal lobule, area PG. Low-power dark-field examination of TMB processed coronal sections revealed several ipsilateral cortical areas which demonstrated interconnections with the inferior parietal placement site as indicated by the presence of heavy anterogradely-labeled projection fields and large numbers of retrogradely-labeled neurons. The areas were, in order of magnitude, the prefrontal convexity cortex, the banks and fundus of the superior temporal sulcus, the medial bank of the occipitotemporal sulcus (area TF), and the cingulate gyrus. While these other cortical regions displayed an anterogradelylabeled projection ' b a n d ' in layer IV, only the caudal sulcus principalis cortex showed the prominent columnar field to be described in this report. The prefrontal projection field first becomes apparent at the level of the prearcuate area 8 'frontal eye field' cortex. The field is moderate in density and ' p a t c h y ' at this level, perhaps due to the tangential orientation of coronal sections through a sulcal cortex rather than being perpendicular to the surface, as the sections are at more rostral levels. In any case, as one moves rostral into the caudal sulcus principalis cortex, the columnar organization of the inferior p a r i e t a l -
Fig. 1. Illustration showing 3 serial coronal sections through the HRP gel implant site in the inferior parietal lobule (area PG) of a cynomolgus monkey (Macacafascicularis), which resulted in a columnar projection to the caudal sulcus principalis cortex. IPS, intraparietal sulcus; LS, lateral sulcus; P, pulvinar; STS, superior temporal sulcus.
121 prefrontal projection becomes heavier and more apparent (Fig. 2). The field ends abruptly at the level of the rostral tip of the superior ramus of the arcuate sulcus, i.e. it is present only in the caudal third of the sulcus principalis cortex, suggesting a definite specificity in the projection. The columnar field appears to be further restricted to area 46 of Walker [13], in that it begins dorsally at the superior ramus of the arcuate sulcus and continues over the crown of the 'subarcuate' cortex into the banks and fundus of the principal sulcus, and ends abruptly again at the lip of the ventral bank (Fig. 2A). The columns are very prominent in the sulcus principalis cortex. Alternate dark and light columns, perpendicular to the surface of the cortex, measure 300-500 #m in width and extend across all laminae of the cortex. At low magnification, a prominent line is observed, parallel to the cortical surface of the ventral bank, in layer IV (Fig. 2A, B). This appears to be lacking in the dorsal bank, and the ventral bank of the superior ramus of the arcuate sulcus demonstrates a negative image (dark line) in layer IV, suggesting the absence of such a terminal projection. When one examines the sulcus principalis cortex in higher power dark-field, the columnar projection becomes much less apparent. However, hundreds of small, retrogradely-labeled pyramids of both laminae III and V become visible (Fig. 3). While the dorsal sulcus principalis cortex also contained large numbers of labeled neurons, clearly the heaviest prefrontal-inferior parietal projection originates from
Fig. 2. A: low-power (3 × ) dark-field photomicrograph of a coronal section through the caudal sulcus principalis cortex showing the columnar projection field resulting from an HRP gel implant in the inferior parietal lobule. B: photographic enlargement illustrates the anterogradely-labeled projection 'line' in layer IV (arrows) of the ventral bank of the principal sulcus. PS, principal sulcus; SAS, superior ramus arcuate sulcus. Low magnification (whole section) dark-field required use of Sage Instruments Model 281 Stereo Light Source.
122
Fig. 3. Higherpower (145 x ) dark-field photomicrographand correspondingcresyl violet-stained section of the ventral bank of the principal sulcus (same section as Fig. 2A, B), demonstrating the presence of large numbers of retrogradely-labeled prefrontal-inferior parietal neurons in layers llI and V, the density of which appears to be uniform and thus unrelated to the columnar (parieto-prefrontal) projection field. layers III and V of the ventral bank of the principal sulcus. It should be noted, however, that another prominent terminal field, which did not demonstrate an obvious columnar organization, was seen in the caudal dorsal prefrontal convexity in area FC, dorsal to the rostral superior ramus of the arcuate sulcus (Fig. 2A). The findings described appear to be significant from a number of perspectives. First, the discretely-organized reciprocal interconnectivity between the inferior parietal and sulcus principalis cortices, two areas suggested by Jones and Powell [8] to represent multimodal sensory convergence areas within primate cerebral cortex, is noteworthy. One might be tempted to expect that as the intrahemispheric associational sequence is followed stepwise from primary sensory areas to these convergence areas that sensory specificity would be lost. But the distinct anatomical columnar organization observed in the interconnection of inferior parietal lobule and sulcus principalis regions leaves one with the strong impression that there persists at these cortical levels a substrate which might preserve specificity in much the same fashion as in the retinotopography of the striate cortex [6]. It would be interesting to know if the columns, shown by Goldman and Nauta [4] to exist in
123 interhemispheric homotypical sulcus principalis connections, are the same as, or alternate with, those resulting from inferior parietal projections. The presence or absence of the terminal 'line' or band observed in layer IV may also be of significance. Whereas this prominent anterogradely-labeled projection was clearly present in the ventral sulcus principalis cortex, and also the fundus and inferior bank of the superior temporal sulcus and medial bank of the occipitotemporal sulcus (area TF), it appeared to be lacking in the dorsal sulcus principalis cortex in response to the inferior parietal HRP implant. Hubel et al. [6] have shown, for example, that the visual orientation columns in striate cortex span all layers except IVc. The prominence of the 'line' in layer IV of the ventral bank of the principal sulcus could be a consequence of the fine dark lines above and below it (see Fig. 2A) which tend to highlight it. But it may be that later, more detailed investigation of the projection may reveal an absence of anterograde label in IVa and IVc (thus producing the dark lines), accentuating the prominent label in IVb. Unfortunately, higher power dark-field magnification of the ventral sulcus principalis cortex decreases the sharpness of the column and line borders and thus it may be difficult to determine if this in fact is the case. These distinctions in layer IV were not apparent in Goldman and Nauta's autoradiographic study of columns resulting from interhemispheric sulcus principalis projections. This study appears to be one of the first to demonstrate the usefulness of anterogradely-transported horseradish peroxidase for visualizing cortical orientation columns. It appears that using the HRP gel [5], in combination with the increased sensitivity of the TMB technique of Mesulam [10] and dark-field microscopy, is essential for such observations. Adjacent sections processed with the benzidine dihydrochloride (BDHC) technique failed to show any evidence of the anterograde projection field, and, in addition, labeled notably fewer retrogradely-filled prefronto-parietal neurons. The method used in this study seems to produce results which are at least equal to those obtained with autoradiography, and thus seems to support its efficacy in cortical investigations of this type. The HRP gel can be cut into fragments of any size or shape depending on its suitability for specific studies. In this study small 'spear-like' pieces (approximately 2 mm long, 0.5 mm wide), when solidified, could be introduced into the cortex lining the intraparietal sulcus, and the 'slow-release' properties of the polyacrylamide gel enhanced the prolonged and restricted uptake of the enzyme at the implant site. The point should also be made that the regional specificity of the inferior parietal-prefrontal projection to the caudal third of the sulcus principalis cortex and prearcuate FEF cortex lends further support to the many studies proposing the existence of functional and behavioral subsectors within the prefrontal cortex (for example, see ref. 3). Perhaps the columnar organization within subregions, such as sulcus principalis cortex, constitute in part the anatomical substrate of spatial capabilities associated with the classical delayed-response test. It is tempting to imagine that the prefrontal cortex may have cyto- and myelo-architectural means of
124
representing the external sensory milieu in much the same way that the 'barrels' of somatosensory cortex mirror vibrissal skin. Certainly the distinctive arrangement of the inputs to this sector of granular frontal cortex gives us a glimpse into the tremendous organization that exists within cortical association areas, which represent phylogenetically, and probably ontogenetically, the highest level of development in the neocortical mantle. ACKNOWLEDGEMENTS
The author wishes to express his appreciation to Mrs. JoAnne Botkin and Mrs. Doris Harris for their technical assistance. This study was supported by National Science Foundation Grant BNS 7822971. REFERENCES 1 2
3 4
5 6 7 8 9
10
11 12 13
Chavis, D.A. and Pandya, D.N., Further observations on corticofrontal connections in the rhesus monkeys, Brain Res., 117 (1976) 369-386. Divac, I., LaVail, J.H., Rakic, P. and Winston, K.R., Heterogeneous afferents to the inferior parietal lobe of the rhesus monkey revealed by the retrograde transport method, Brain Res., 123 (1977) 197-207. Goldman, P.S. and Rosvold, H.E., Localization of function within the dorsolateral prefrontal cortex of the rhesus monkey, Exp. Neurol., 27 (1970) 291-304. Goldman, P.S. and Nauta, W.J.H., Columnar distribution of cortico-cortical fibers in the frontal association, limbic, and motor cortex of the developing rhesus monkey, Brain Res., 122 (1977) 393-413. Griffin, G., Watkins, L. and Mayer D.J., HRP pellets and slow-release gels: two new techniques for greater localization and sensitivity, Brain Res., 168 (1979) 595-601. Hubel, D.H., Wiesel, T.N. and Stryker, M.P., Anatomical demonstration of orientation columns in macaque monkey, J. comp. Neurol., 177 (1978) 361-380. Jacobson, S. and Trojanowski, J.Q., Prefrontal granular cortex of the rhesus monkey. 1. Intrahemispheric cortical afferents, Brain Res., 132 (1977) 209-233. Jones, E.G. and Powell, T.P.S., An anatomical study of converging sensory pathways within the cerebral cortex of the monkey, Brain, 93 (1970) 793-820. Mesulam, M.-M., Van Hoesen, G.W., Pandya, D.N. and Geschwind, N., Limbic and sensory connections of the inferior parietal lobe (Area PG) in the rhesus monkey: a study with a new method for horseradish peroxidase histochemistry, Brain Res., 136 (1977) 393-414. Mesulam, M.-M., A tetramethylbenzidine method for the light microscopic tracing of neural connections with horseradish peroxidase (HRP) neurohistochemistry. In: Neuroanatomical Techniques, Short Course, Society for Neuroscience, 1978, pp. 65-71. Pandya, D.N. and Kuypers, H.G.J.M., Cortico-cortical connections in the rhesus monkey, Brain Res., 13 (1969) 13-36. Von Bonin, G. and Bailey, P., The Neocortex of Macaca mulatta, Univ. of Illinois Press, Urbana, 111., 1947, pp. 1-163. Walker, A.E., A cytoarchitectural study of the prefrontal area of the macaque monkey, J. comp. Neurol., 73 (1940) 59-86.
119
AN INTRAHEMISPHERIC COLUMNAR PROJECTION BETWEEN TWO CORTICAL MULTISENSORY CONVERGENCE AREAS (INFERIOR PARIETAL LOBULE AND PREFRONTAL CORTEX): AN ANTEROGRADE STUDY IN MACAQUE USING HRP GEL
G.R. LE1CHNETZ
Department of Anatomy, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298 (U.S.A.) (Received March 24th, 1980) (Accepted March 28th, 1980)
SUMMARY
Horseradish peroxidase (HRP) gel and tetramethylbenzidine neurohistochemistry were used successfully in demonstrating the columnar organization of an intrahemispheric projection from the inferior parietal lobule to the prefrontal cortex in the macaque monkey. Following an HRP gel implant within the upper portion of the posterior (caudal) bank of the intraparietal sulcus, a prominent anterograde terminal projection field, consisting of alternate light and dark (300-500 ~m) columns, was observed using low-power dark-field microscopy in the caudal third of the sulcus principalis cortex (area 46). At higher magnification large numbers of small retrogradely-labeled pyramidal cells were present in layers III and V of the same cortex. The regionally-specific projection, coupled with its discrete anatomical organization, lends support to the reputed functional/behavioral subsectors within the prefrontal cortex and its apparent capacity for spatial representation.
The phenomenon of columnar organization with the mammalian cerebral cortex is now well established, and this unique anatomical feature is not restricted to primary sensory areas, but has been shown by Goldman and Nauta [4] to also occur in association, limbic and motor cortex. In the course of a comprehensive study of the connections of both prefrontal and inferior parietal cortex in macaque monkeys a dramatic demonstration of cortical 'columns' became apparent in the sulcus principalis cortex following an HRP gel implant (48 h survival) in the inferior parietal lobule, area PG of Von Bonin and Bailey [12]. The extensive and reciprocal inter-
120 connectivity between these two cortical regions has previously been established on the basis of both silver [1, 8, 11] and H R P studies [2, 7, 9]. The H R P polyacrylamide gel used in this study in combination with highly sensitive tetramethylbenzidine (TMB) neurohistochemistry (see ref. 10 for methods) and dark-field microscopy provided exquisite visualization of both anterogradelyand retrogradely-transported H R P . In the case illustrated (Fig. 1), two spear-like solid H R P gel fragments were introduced through a short slit in the pia on the lip of the upper caudal (posterior) bank of the intraparietal sulcus, and pushed into the sulcal cortex, parallel to the sulcus. The enzyme filled the middle to dorsal intraparietal sulcal cortex and spread caudally into approximately the rostrat half of the crown of the inferior parietal lobule, area PG. Low-power dark-field examination of TMB processed coronal sections revealed several ipsilateral cortical areas which demonstrated interconnections with the inferior parietal placement site as indicated by the presence of heavy anterogradely-labeled projection fields and large numbers of retrogradely-labeled neurons. The areas were, in order of magnitude, the prefrontal convexity cortex, the banks and fundus of the superior temporal sulcus, the medial bank of the occipitotemporal sulcus (area TF), and the cingulate gyrus. While these other cortical regions displayed an anterogradelylabeled projection ' b a n d ' in layer IV, only the caudal sulcus principalis cortex showed the prominent columnar field to be described in this report. The prefrontal projection field first becomes apparent at the level of the prearcuate area 8 'frontal eye field' cortex. The field is moderate in density and ' p a t c h y ' at this level, perhaps due to the tangential orientation of coronal sections through a sulcal cortex rather than being perpendicular to the surface, as the sections are at more rostral levels. In any case, as one moves rostral into the caudal sulcus principalis cortex, the columnar organization of the inferior p a r i e t a l -
Fig. 1. Illustration showing 3 serial coronal sections through the HRP gel implant site in the inferior parietal lobule (area PG) of a cynomolgus monkey (Macacafascicularis), which resulted in a columnar projection to the caudal sulcus principalis cortex. IPS, intraparietal sulcus; LS, lateral sulcus; P, pulvinar; STS, superior temporal sulcus.
121 prefrontal projection becomes heavier and more apparent (Fig. 2). The field ends abruptly at the level of the rostral tip of the superior ramus of the arcuate sulcus, i.e. it is present only in the caudal third of the sulcus principalis cortex, suggesting a definite specificity in the projection. The columnar field appears to be further restricted to area 46 of Walker [13], in that it begins dorsally at the superior ramus of the arcuate sulcus and continues over the crown of the 'subarcuate' cortex into the banks and fundus of the principal sulcus, and ends abruptly again at the lip of the ventral bank (Fig. 2A). The columns are very prominent in the sulcus principalis cortex. Alternate dark and light columns, perpendicular to the surface of the cortex, measure 300-500 #m in width and extend across all laminae of the cortex. At low magnification, a prominent line is observed, parallel to the cortical surface of the ventral bank, in layer IV (Fig. 2A, B). This appears to be lacking in the dorsal bank, and the ventral bank of the superior ramus of the arcuate sulcus demonstrates a negative image (dark line) in layer IV, suggesting the absence of such a terminal projection. When one examines the sulcus principalis cortex in higher power dark-field, the columnar projection becomes much less apparent. However, hundreds of small, retrogradely-labeled pyramids of both laminae III and V become visible (Fig. 3). While the dorsal sulcus principalis cortex also contained large numbers of labeled neurons, clearly the heaviest prefrontal-inferior parietal projection originates from
Fig. 2. A: low-power (3 × ) dark-field photomicrograph of a coronal section through the caudal sulcus principalis cortex showing the columnar projection field resulting from an HRP gel implant in the inferior parietal lobule. B: photographic enlargement illustrates the anterogradely-labeled projection 'line' in layer IV (arrows) of the ventral bank of the principal sulcus. PS, principal sulcus; SAS, superior ramus arcuate sulcus. Low magnification (whole section) dark-field required use of Sage Instruments Model 281 Stereo Light Source.
122
Fig. 3. Higherpower (145 x ) dark-field photomicrographand correspondingcresyl violet-stained section of the ventral bank of the principal sulcus (same section as Fig. 2A, B), demonstrating the presence of large numbers of retrogradely-labeled prefrontal-inferior parietal neurons in layers llI and V, the density of which appears to be uniform and thus unrelated to the columnar (parieto-prefrontal) projection field. layers III and V of the ventral bank of the principal sulcus. It should be noted, however, that another prominent terminal field, which did not demonstrate an obvious columnar organization, was seen in the caudal dorsal prefrontal convexity in area FC, dorsal to the rostral superior ramus of the arcuate sulcus (Fig. 2A). The findings described appear to be significant from a number of perspectives. First, the discretely-organized reciprocal interconnectivity between the inferior parietal and sulcus principalis cortices, two areas suggested by Jones and Powell [8] to represent multimodal sensory convergence areas within primate cerebral cortex, is noteworthy. One might be tempted to expect that as the intrahemispheric associational sequence is followed stepwise from primary sensory areas to these convergence areas that sensory specificity would be lost. But the distinct anatomical columnar organization observed in the interconnection of inferior parietal lobule and sulcus principalis regions leaves one with the strong impression that there persists at these cortical levels a substrate which might preserve specificity in much the same fashion as in the retinotopography of the striate cortex [6]. It would be interesting to know if the columns, shown by Goldman and Nauta [4] to exist in
123 interhemispheric homotypical sulcus principalis connections, are the same as, or alternate with, those resulting from inferior parietal projections. The presence or absence of the terminal 'line' or band observed in layer IV may also be of significance. Whereas this prominent anterogradely-labeled projection was clearly present in the ventral sulcus principalis cortex, and also the fundus and inferior bank of the superior temporal sulcus and medial bank of the occipitotemporal sulcus (area TF), it appeared to be lacking in the dorsal sulcus principalis cortex in response to the inferior parietal HRP implant. Hubel et al. [6] have shown, for example, that the visual orientation columns in striate cortex span all layers except IVc. The prominence of the 'line' in layer IV of the ventral bank of the principal sulcus could be a consequence of the fine dark lines above and below it (see Fig. 2A) which tend to highlight it. But it may be that later, more detailed investigation of the projection may reveal an absence of anterograde label in IVa and IVc (thus producing the dark lines), accentuating the prominent label in IVb. Unfortunately, higher power dark-field magnification of the ventral sulcus principalis cortex decreases the sharpness of the column and line borders and thus it may be difficult to determine if this in fact is the case. These distinctions in layer IV were not apparent in Goldman and Nauta's autoradiographic study of columns resulting from interhemispheric sulcus principalis projections. This study appears to be one of the first to demonstrate the usefulness of anterogradely-transported horseradish peroxidase for visualizing cortical orientation columns. It appears that using the HRP gel [5], in combination with the increased sensitivity of the TMB technique of Mesulam [10] and dark-field microscopy, is essential for such observations. Adjacent sections processed with the benzidine dihydrochloride (BDHC) technique failed to show any evidence of the anterograde projection field, and, in addition, labeled notably fewer retrogradely-filled prefronto-parietal neurons. The method used in this study seems to produce results which are at least equal to those obtained with autoradiography, and thus seems to support its efficacy in cortical investigations of this type. The HRP gel can be cut into fragments of any size or shape depending on its suitability for specific studies. In this study small 'spear-like' pieces (approximately 2 mm long, 0.5 mm wide), when solidified, could be introduced into the cortex lining the intraparietal sulcus, and the 'slow-release' properties of the polyacrylamide gel enhanced the prolonged and restricted uptake of the enzyme at the implant site. The point should also be made that the regional specificity of the inferior parietal-prefrontal projection to the caudal third of the sulcus principalis cortex and prearcuate FEF cortex lends further support to the many studies proposing the existence of functional and behavioral subsectors within the prefrontal cortex (for example, see ref. 3). Perhaps the columnar organization within subregions, such as sulcus principalis cortex, constitute in part the anatomical substrate of spatial capabilities associated with the classical delayed-response test. It is tempting to imagine that the prefrontal cortex may have cyto- and myelo-architectural means of
124
representing the external sensory milieu in much the same way that the 'barrels' of somatosensory cortex mirror vibrissal skin. Certainly the distinctive arrangement of the inputs to this sector of granular frontal cortex gives us a glimpse into the tremendous organization that exists within cortical association areas, which represent phylogenetically, and probably ontogenetically, the highest level of development in the neocortical mantle. ACKNOWLEDGEMENTS
The author wishes to express his appreciation to Mrs. JoAnne Botkin and Mrs. Doris Harris for their technical assistance. This study was supported by National Science Foundation Grant BNS 7822971. REFERENCES 1 2
3 4
5 6 7 8 9
10
11 12 13
Chavis, D.A. and Pandya, D.N., Further observations on corticofrontal connections in the rhesus monkeys, Brain Res., 117 (1976) 369-386. Divac, I., LaVail, J.H., Rakic, P. and Winston, K.R., Heterogeneous afferents to the inferior parietal lobe of the rhesus monkey revealed by the retrograde transport method, Brain Res., 123 (1977) 197-207. Goldman, P.S. and Rosvold, H.E., Localization of function within the dorsolateral prefrontal cortex of the rhesus monkey, Exp. Neurol., 27 (1970) 291-304. Goldman, P.S. and Nauta, W.J.H., Columnar distribution of cortico-cortical fibers in the frontal association, limbic, and motor cortex of the developing rhesus monkey, Brain Res., 122 (1977) 393-413. Griffin, G., Watkins, L. and Mayer D.J., HRP pellets and slow-release gels: two new techniques for greater localization and sensitivity, Brain Res., 168 (1979) 595-601. Hubel, D.H., Wiesel, T.N. and Stryker, M.P., Anatomical demonstration of orientation columns in macaque monkey, J. comp. Neurol., 177 (1978) 361-380. Jacobson, S. and Trojanowski, J.Q., Prefrontal granular cortex of the rhesus monkey. 1. Intrahemispheric cortical afferents, Brain Res., 132 (1977) 209-233. Jones, E.G. and Powell, T.P.S., An anatomical study of converging sensory pathways within the cerebral cortex of the monkey, Brain, 93 (1970) 793-820. Mesulam, M.-M., Van Hoesen, G.W., Pandya, D.N. and Geschwind, N., Limbic and sensory connections of the inferior parietal lobe (Area PG) in the rhesus monkey: a study with a new method for horseradish peroxidase histochemistry, Brain Res., 136 (1977) 393-414. Mesulam, M.-M., A tetramethylbenzidine method for the light microscopic tracing of neural connections with horseradish peroxidase (HRP) neurohistochemistry. In: Neuroanatomical Techniques, Short Course, Society for Neuroscience, 1978, pp. 65-71. Pandya, D.N. and Kuypers, H.G.J.M., Cortico-cortical connections in the rhesus monkey, Brain Res., 13 (1969) 13-36. Von Bonin, G. and Bailey, P., The Neocortex of Macaca mulatta, Univ. of Illinois Press, Urbana, 111., 1947, pp. 1-163. Walker, A.E., A cytoarchitectural study of the prefrontal area of the macaque monkey, J. comp. Neurol., 73 (1940) 59-86.