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Distribution of the anterior commissure to the amygdaloid complex in the monkey
Brain Research, 162 (1979) 331-337
331
((:) Elsevier/North-Holland Biomedical Press
Short Communications Distribution of the anterior commissure to the amygdaloid complex in the monkey
BLAIR H. TURNER,* MORTIMER MISHKIN and MARGARET E. KNAPP Department of Anatomy, Howard University Medical School, Washington, D.C. 20059 and Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Md. 20014 (U.S.A.)
(Accepted November 9th, 1978)
Although the anterior commissure is known to carry fibers to the amygdaloid complex in infraprimate species4,8,16, no evidence for such a projection has been reported in primates6, 9. As part of an investigation 13 15 into the connections of the amygdala in the rhesus monkey (Macaca mulatta), we examined this question of commissural amygdaloid projections using the method of anterograde degeneration v'. In one monkey, a control transection was made in that part of the body of the corpus callosum overlying the third ventricle through which the anterior commissure can be approached. In two experimental animals, the same part of the corpus callosum was cut, and the anterior commissure was visualized and sectioned. Details of the surgical procedures and the histological results of this type of commissural lesion have been reported previously 7 (see Fig. 2, Animal No. 56, for illustration). Following a survival period of 6 days, the monkeys were given a lethal dose of anesthetic and their brains prepared using the Fink-Heimer technique 5. In the control brain, no evidence of terminal degeneration was found either in the allocortex that covers the amygdala medially and anteriorly, or in the amygdala itself. In the experimental brains, however, degeneration was observed in both of these locations (see Figs. 2 and 3). In the allocortex, moderate degeneration was seen in the subdivision of entorhinal cortex that covers the anterior pole of the amygdala (Epol of Rose) ~I and also in the temporal prepiriform cortex (Prpy 3 of Rose tl) and the medial amygdaloid nucleus which cover the dorsomedial surface of the amygdala. In all 3 of these periamygdaloid allocortical areas, degeneration was heavier in layers IA and I B and progressively thinned out in layers II and III. Within the deep amygdaloid nuclei, moderately dense degeneration was seen in the lateral nucleus throughout its rostrocaudal and dorsoventral extent. In its mediolateral extent, degeneration was heavier in the lateral two-thirds than in the medial third. In addition, light degeneration was seen in the claustral area of the amygdala (as well as in the ventral part of * To whom correspondence should be sent at: Laboratory of Neuropsychology, National Institute of Mental Health, Building 9, 1NI07, Bethesda, Md 20014, U.S.A.
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333 the claustrum itself). N o other deep a m y g d a l o i d nucleus contained any evidence o f degeneration. The results indicate that b o t h the p e r i a m y g d a l o i d allocortex and the a m y g d a l a o f the p r i m a t e receive afferents by way o f the a n t e r i o r commissure. F u r t h e r m o r e , the d i s t r i b u t i o n o f these fibers in the rhesus m o n k e y is generally similar to that described in rodent species. Thus, afferents crossing in the a n t e r i o r commissure and projecting to p e r i a m y g d a l o i d allocortex have been r e p o r t e d in the rat 4,8, a l t h o u g h in this species the t e r m i n a t i o n a p p e a r s to be in the cortical s rather than the medial a m y g d a l o i d nucleus. Also, afferents crossing in the p o s t e r i o r limb o f the a n t e r i o r commissure and p r o j e c t i n g to the lateral a m y g d a l o i d nucleus have been reported in both rat 4,8 and r a b b i t t6. The sources o f the allocortical and a m y g d a l o i d afferents carried in the a n t e r i o r c o m m i s s u r e have not been established with certainty. However, it is likely that the c o m m i s s u r a l projections to p e r i a m y g d a l o i d allocortex originate in contralateral olfactory structures. Thus, after injection o f tritiated a m i n o acids into the olfactory bulb o f the monkey, a u t o r a d i o g r a p h i c a l l y labeled fibers were seen crossing in the a n t e r i o r c o m m i s s u r e a n d ending in layer IA o f the opposite t e m p o r a l prepiriform cortex 13. Also, projections to layers IB, II, and III of the contralateral prepiriform cortex have been observed in rat 1° and rabbit `) after injections o f radioactively labeled a m i n o acids in the prepiriform cortex or anterior olfactory nucleus. Afferents to the c o n t r a l a t e r a l medial a m y g d a l o i d nucleus and entorhinal cortex by way of the anterior c o m m i s s u r e have not been r e p o r t e d previously in any species, but it seems likely that those we have seen originate in the same structures on the projecting side. The l o c a t i o n o f the cells that project to the c o n t r a l a t e r a l lateral a m y g d a l o i d nucleus has also not been established. Two different p r o p o s a l s have been a d v a n c e d .
Fig. I. Normal and experimental coronal sections through the amygdala. A : a section at approximately 16 in the stereotaxic plane from an unoperated animal, stained for fibers by the VogOs method. The lateral nucleus, in which degeneration is evident in B, is separated medially from the basal nucleus by a vertical band offi bers, and dorsally from the claust ral area of the amygdala by a dorsomedially directed series of small fiber bundles. B: a section at approximately ÷ 15 from an experimental brain, stained by the Fink-Heimer '~ technique, bleached in 0.5 ~ potassium ferricyanide, and then counterstained with cresyl violet. This photograph was taken under dark-field conditions, where dense terminal and preterminal degeneration in gray matter appears light against a dark background. Arrow points to such an area of degeneration in the ventrolateral part of AL. Less dense degeneration, not apparent in the photograph, is observable microscopicallythroughout AL and in A M. A bbreviations for Figs. I 3 : a, amygdaloid sulcus (or sulcus semiannularis) ; AAA, anterior area of the amygdala ; AB, basal nucleus of the amygdala; ABI, basal nucleus of the amygdala, lateral part; ABm, basal nucleus of the amygdala, medial part; ABmd, basal nucleus of the amygdala, medial part (deep portion); A Bins, basal nucleus of the amygdala, medial part (superficial portion); ABA, basal accessory nucleus of the amygdala; ABAI, basal accessory nucleus of the amygdala, lateral part;ABAm, basal accessory nucleus of the amygdala, medial part; AC, cortical nucleus of the amygdala; ACA, claustral area of the amygdala; ACe, central nucleus of the amygdala; AL, lateral nucleus of the amygdala; AM, medial nucleus of the amygdala; C ant, anterior commissure; Cl, claustrum; C opt, optic chiasm; Ea, entorhinal cortex, anterior part; Ep, entorhinal cortex, posterior part; Epol, entorhinal cortex, polar part ; erh, endorhinal su[cus; H, fiippocampus; h, hippocampal sulcus; la, lateral sulcus ; Pe, perirhinal cortex ; Pr, prorhinal cortex; Prpy 3, prepiriform cortex, intermediate part; Put, putamen; rh, rhinal sulcus; SOL, lateral olfactory stria; TG, neocortex of the temporal pole; T Opt, optic tract: TA, transition area; V lat, lateral ventricle.
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Fig. 2. Drawings of cross sections through the rostral half of the amygdaloid complex, showing the cytoarchitectural divisions and sites of termination of fibers crossing in the anterior commissure. Approximate stereotaxic levels are shown in the upper left of each section. The classification of the entorhinal cortex is based on Rose 11, that of the amygdala on Crosby a n d Humphreya, that of the prorhinal and pedrhinal cortex on Van Hoesen 17, and that of neocortex on Bonin and ~ l e y ! . Cytoarchitectural areas are bounded by continuous lines, normal fiber bundles are shown by interrupted lines, and degeneration by dots. For abbreviations see Fig. 1.
335
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,,y Fig. 3. Drawings of cross sections through the caudal half of the amygdaloid complex, showing the cytoarchitectural divisions and sites of termination of fibers crossing in the anterior commissure. Conventions as in Fig. 2. Van Alphen 16 has suggested that in the rabbit both prepiriform cortex and temporal neocortex are the sources of the commissural projections to the amygdala. De Olmos 4, on the other hand, has reported that the origin of the crossed connection in the rat is the amygdala itself. Evidence from other studies in our laboratory bear out this issue 15. Unilateral lesions have been made in all of the cytoarchitectural divisions of the temporal neocortex of the rhesus monkey, and the projections from these sites traced. While several of the more anterior lesions resulted in degeneration in the ipsilateral amygdala, none sent projections to the contralateral amygdala. This eliminates the
336 neocortex as the source o f contralateral amygdaloid afferents and points instead to the a m y g d a l a as the possible origin of the interhemispheric pathway. It appears likely therefore that one part o f the anterior commissure interconnects b o t h the periamygdaloid allocortex on the two sides and the two lateral amygdaloid nuclei. In this it would resemble the neocortical part o f the anterior commissure in connecting mainly h o m o t y p i c areas of the two hemispheres. If this proposal is correct, then the amygdaloid-allocortical portion of the anterior commissure may resemble the neocortical p o r t i o n functionally also. A major c o m p o n e n t o f the anterior commissure interconnects the inferior temporal visual areas o f the two hemispheres 9, 19, and this connection is now k n o w n to provide inferior temporal neurons in each hemisphere with visual information that has been processed by the other 7. It is reasonable to suppose that the anterior commissure plays the same role for other sensory modalities (e.g. auditory) represented in anterior temporal neocortex. These same sensory representations in anterior temporal neocortex also send ipsilateral projections to the lateral amygdaloid nucleus, and the olfactory system sends one to the periamygdaloid allocortex. The likelihood that these subdivisions o f the amygdaloid complex are reciprocally connected across the anterior commissure suggests that the amygdaloid-allocortical part of this commissure, like the neocortical part, transmits sensory information between the hemispheres. This research was supported in part by N I M H G r a n t M H 25495. 1 Bonin, G. yon, and Bailey, P., The Neocortex of Maccaca Mulatta, University of Illinois Press, Urbana, I11., 1947, pp. 1-136. 2 Broadwell, R. D., Olfactory relationships of the telencephalon and diencephalon in the rabbit. 11. An autoradiographic and horseradish peroxidase study of the efferent connections of the anterior olfactory nucleus, J. comp. Neurol., 164 (1975) 389-410. 3 Crosby, E. and Humphrey, T., Studies of the vertebrate telencephalon: 1I. The nuclear pattern of the anterior olfactory nucleus, tuberculum olfactorium and the amygdaloid complex in adult man, J. comp. Neurol., 74 (1941) 309-352. 4 De Olmos, J. S. and Ingrain, W. R., Projection field of the stria terminalis in the rat brain: An experimental study, J. comp. Neurol., 146 (1972) 303-334. 5 Fink, R. and Heimer, L., Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system, Brain Research, 4 (1967) 369-374. 6 Fox, C. A., Fisher, R. R. and Desalva, S. J., The distribution of the anterior commissure in the monkey ( Macaca mulatta) , J. comp. Neurol., 89 (1948) 245-277. 7 Gross, C. G., Bender, D. B. and Mishkin, M., Contributions of the corpus callosum and the anterior commissure to visual activation of inferior temporal neurons, Brain Research, 131 (1977) 227-239. 8 Hotel, J. A., The i ntertemporat component of the anterior commissure of the rat, Anat. Rec., 190 (1978) 424-425. 9 Pandya, D. N., Karol, E. A. and Lele, P. P., The distribution of the anterior commissure in the squirrel monkey, Brain Research, 49 (1973) 177-180. 10 Price,J. L.,Anautoradiographicstudyofcomplementarylaminarpatternsofterminationofafferent fibers to the olfactory cortex, J. comp. Neurol., 150 (1973) 87-108. 11 Rose, M., Die sog. Reichrinde beim Menschen und beim Affen. 1I. Teil des Allocortex bei Tier und Mensch, J. Psychol. Neurol. ( Lpz.), 34 (1927) 261M01. 12 Turner, B. H., Afferents to the macaque amygdala by way of the anterior commissure, Neurosci. Abstr., 4 (1978) 228. 13 Turner, B. H. and Mishkin, M., A reassessment of the direct projections of the olfactory bulb, Brain Research, 151 (1978) 375-380. 14 Turner, B. H., Gupta, K. and Mishkin, M., The locus and cytoarchitecture of the projection areas of the olfactory bulb in Macaca mulatta, J. comp. Neurol., 177 (1978) 381-396.
337 15 Turner, B. H., Mishkin, M. and Knapp, M. E., Visual and other sensory inputs to the amygdala of the Rhesus monkey, Neurosci. Abstr., 2 (1976) 398. 16 Van Alphen, H. A. M., The anterior commissure of the rabbit, Acta anat. (Basel), 57 (1969) 1-112. 17 Van Hoesen, G. W. and Pandya, D. N., Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents, Brain Research, 95 (1975) 1-24. 18 Vogt, B., A reduced silver stain for normal axons in the central nervous system, Physiol. Behav., 13 (1974) 837-840. 19 Zeki, S. M., Comparison of the cortical degeneration in the visual regions of the temporal lobe of the monkey following section of the anterior commissure and the splenium, J. comp. Neurol., 148 (1973) 167 176.
331
((:) Elsevier/North-Holland Biomedical Press
Short Communications Distribution of the anterior commissure to the amygdaloid complex in the monkey
BLAIR H. TURNER,* MORTIMER MISHKIN and MARGARET E. KNAPP Department of Anatomy, Howard University Medical School, Washington, D.C. 20059 and Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Md. 20014 (U.S.A.)
(Accepted November 9th, 1978)
Although the anterior commissure is known to carry fibers to the amygdaloid complex in infraprimate species4,8,16, no evidence for such a projection has been reported in primates6, 9. As part of an investigation 13 15 into the connections of the amygdala in the rhesus monkey (Macaca mulatta), we examined this question of commissural amygdaloid projections using the method of anterograde degeneration v'. In one monkey, a control transection was made in that part of the body of the corpus callosum overlying the third ventricle through which the anterior commissure can be approached. In two experimental animals, the same part of the corpus callosum was cut, and the anterior commissure was visualized and sectioned. Details of the surgical procedures and the histological results of this type of commissural lesion have been reported previously 7 (see Fig. 2, Animal No. 56, for illustration). Following a survival period of 6 days, the monkeys were given a lethal dose of anesthetic and their brains prepared using the Fink-Heimer technique 5. In the control brain, no evidence of terminal degeneration was found either in the allocortex that covers the amygdala medially and anteriorly, or in the amygdala itself. In the experimental brains, however, degeneration was observed in both of these locations (see Figs. 2 and 3). In the allocortex, moderate degeneration was seen in the subdivision of entorhinal cortex that covers the anterior pole of the amygdala (Epol of Rose) ~I and also in the temporal prepiriform cortex (Prpy 3 of Rose tl) and the medial amygdaloid nucleus which cover the dorsomedial surface of the amygdala. In all 3 of these periamygdaloid allocortical areas, degeneration was heavier in layers IA and I B and progressively thinned out in layers II and III. Within the deep amygdaloid nuclei, moderately dense degeneration was seen in the lateral nucleus throughout its rostrocaudal and dorsoventral extent. In its mediolateral extent, degeneration was heavier in the lateral two-thirds than in the medial third. In addition, light degeneration was seen in the claustral area of the amygdala (as well as in the ventral part of * To whom correspondence should be sent at: Laboratory of Neuropsychology, National Institute of Mental Health, Building 9, 1NI07, Bethesda, Md 20014, U.S.A.
332
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333 the claustrum itself). N o other deep a m y g d a l o i d nucleus contained any evidence o f degeneration. The results indicate that b o t h the p e r i a m y g d a l o i d allocortex and the a m y g d a l a o f the p r i m a t e receive afferents by way o f the a n t e r i o r commissure. F u r t h e r m o r e , the d i s t r i b u t i o n o f these fibers in the rhesus m o n k e y is generally similar to that described in rodent species. Thus, afferents crossing in the a n t e r i o r commissure and projecting to p e r i a m y g d a l o i d allocortex have been r e p o r t e d in the rat 4,8, a l t h o u g h in this species the t e r m i n a t i o n a p p e a r s to be in the cortical s rather than the medial a m y g d a l o i d nucleus. Also, afferents crossing in the p o s t e r i o r limb o f the a n t e r i o r commissure and p r o j e c t i n g to the lateral a m y g d a l o i d nucleus have been reported in both rat 4,8 and r a b b i t t6. The sources o f the allocortical and a m y g d a l o i d afferents carried in the a n t e r i o r c o m m i s s u r e have not been established with certainty. However, it is likely that the c o m m i s s u r a l projections to p e r i a m y g d a l o i d allocortex originate in contralateral olfactory structures. Thus, after injection o f tritiated a m i n o acids into the olfactory bulb o f the monkey, a u t o r a d i o g r a p h i c a l l y labeled fibers were seen crossing in the a n t e r i o r c o m m i s s u r e a n d ending in layer IA o f the opposite t e m p o r a l prepiriform cortex 13. Also, projections to layers IB, II, and III of the contralateral prepiriform cortex have been observed in rat 1° and rabbit `) after injections o f radioactively labeled a m i n o acids in the prepiriform cortex or anterior olfactory nucleus. Afferents to the c o n t r a l a t e r a l medial a m y g d a l o i d nucleus and entorhinal cortex by way of the anterior c o m m i s s u r e have not been r e p o r t e d previously in any species, but it seems likely that those we have seen originate in the same structures on the projecting side. The l o c a t i o n o f the cells that project to the c o n t r a l a t e r a l lateral a m y g d a l o i d nucleus has also not been established. Two different p r o p o s a l s have been a d v a n c e d .
Fig. I. Normal and experimental coronal sections through the amygdala. A : a section at approximately 16 in the stereotaxic plane from an unoperated animal, stained for fibers by the VogOs method. The lateral nucleus, in which degeneration is evident in B, is separated medially from the basal nucleus by a vertical band offi bers, and dorsally from the claust ral area of the amygdala by a dorsomedially directed series of small fiber bundles. B: a section at approximately ÷ 15 from an experimental brain, stained by the Fink-Heimer '~ technique, bleached in 0.5 ~ potassium ferricyanide, and then counterstained with cresyl violet. This photograph was taken under dark-field conditions, where dense terminal and preterminal degeneration in gray matter appears light against a dark background. Arrow points to such an area of degeneration in the ventrolateral part of AL. Less dense degeneration, not apparent in the photograph, is observable microscopicallythroughout AL and in A M. A bbreviations for Figs. I 3 : a, amygdaloid sulcus (or sulcus semiannularis) ; AAA, anterior area of the amygdala ; AB, basal nucleus of the amygdala; ABI, basal nucleus of the amygdala, lateral part; ABm, basal nucleus of the amygdala, medial part; ABmd, basal nucleus of the amygdala, medial part (deep portion); A Bins, basal nucleus of the amygdala, medial part (superficial portion); ABA, basal accessory nucleus of the amygdala; ABAI, basal accessory nucleus of the amygdala, lateral part;ABAm, basal accessory nucleus of the amygdala, medial part; AC, cortical nucleus of the amygdala; ACA, claustral area of the amygdala; ACe, central nucleus of the amygdala; AL, lateral nucleus of the amygdala; AM, medial nucleus of the amygdala; C ant, anterior commissure; Cl, claustrum; C opt, optic chiasm; Ea, entorhinal cortex, anterior part; Ep, entorhinal cortex, posterior part; Epol, entorhinal cortex, polar part ; erh, endorhinal su[cus; H, fiippocampus; h, hippocampal sulcus; la, lateral sulcus ; Pe, perirhinal cortex ; Pr, prorhinal cortex; Prpy 3, prepiriform cortex, intermediate part; Put, putamen; rh, rhinal sulcus; SOL, lateral olfactory stria; TG, neocortex of the temporal pole; T Opt, optic tract: TA, transition area; V lat, lateral ventricle.
334
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Fig. 2. Drawings of cross sections through the rostral half of the amygdaloid complex, showing the cytoarchitectural divisions and sites of termination of fibers crossing in the anterior commissure. Approximate stereotaxic levels are shown in the upper left of each section. The classification of the entorhinal cortex is based on Rose 11, that of the amygdala on Crosby a n d Humphreya, that of the prorhinal and pedrhinal cortex on Van Hoesen 17, and that of neocortex on Bonin and ~ l e y ! . Cytoarchitectural areas are bounded by continuous lines, normal fiber bundles are shown by interrupted lines, and degeneration by dots. For abbreviations see Fig. 1.
335
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,,y Fig. 3. Drawings of cross sections through the caudal half of the amygdaloid complex, showing the cytoarchitectural divisions and sites of termination of fibers crossing in the anterior commissure. Conventions as in Fig. 2. Van Alphen 16 has suggested that in the rabbit both prepiriform cortex and temporal neocortex are the sources of the commissural projections to the amygdala. De Olmos 4, on the other hand, has reported that the origin of the crossed connection in the rat is the amygdala itself. Evidence from other studies in our laboratory bear out this issue 15. Unilateral lesions have been made in all of the cytoarchitectural divisions of the temporal neocortex of the rhesus monkey, and the projections from these sites traced. While several of the more anterior lesions resulted in degeneration in the ipsilateral amygdala, none sent projections to the contralateral amygdala. This eliminates the
336 neocortex as the source o f contralateral amygdaloid afferents and points instead to the a m y g d a l a as the possible origin of the interhemispheric pathway. It appears likely therefore that one part o f the anterior commissure interconnects b o t h the periamygdaloid allocortex on the two sides and the two lateral amygdaloid nuclei. In this it would resemble the neocortical part o f the anterior commissure in connecting mainly h o m o t y p i c areas of the two hemispheres. If this proposal is correct, then the amygdaloid-allocortical portion of the anterior commissure may resemble the neocortical p o r t i o n functionally also. A major c o m p o n e n t o f the anterior commissure interconnects the inferior temporal visual areas o f the two hemispheres 9, 19, and this connection is now k n o w n to provide inferior temporal neurons in each hemisphere with visual information that has been processed by the other 7. It is reasonable to suppose that the anterior commissure plays the same role for other sensory modalities (e.g. auditory) represented in anterior temporal neocortex. These same sensory representations in anterior temporal neocortex also send ipsilateral projections to the lateral amygdaloid nucleus, and the olfactory system sends one to the periamygdaloid allocortex. The likelihood that these subdivisions o f the amygdaloid complex are reciprocally connected across the anterior commissure suggests that the amygdaloid-allocortical part of this commissure, like the neocortical part, transmits sensory information between the hemispheres. This research was supported in part by N I M H G r a n t M H 25495. 1 Bonin, G. yon, and Bailey, P., The Neocortex of Maccaca Mulatta, University of Illinois Press, Urbana, I11., 1947, pp. 1-136. 2 Broadwell, R. D., Olfactory relationships of the telencephalon and diencephalon in the rabbit. 11. An autoradiographic and horseradish peroxidase study of the efferent connections of the anterior olfactory nucleus, J. comp. Neurol., 164 (1975) 389-410. 3 Crosby, E. and Humphrey, T., Studies of the vertebrate telencephalon: 1I. The nuclear pattern of the anterior olfactory nucleus, tuberculum olfactorium and the amygdaloid complex in adult man, J. comp. Neurol., 74 (1941) 309-352. 4 De Olmos, J. S. and Ingrain, W. R., Projection field of the stria terminalis in the rat brain: An experimental study, J. comp. Neurol., 146 (1972) 303-334. 5 Fink, R. and Heimer, L., Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system, Brain Research, 4 (1967) 369-374. 6 Fox, C. A., Fisher, R. R. and Desalva, S. J., The distribution of the anterior commissure in the monkey ( Macaca mulatta) , J. comp. Neurol., 89 (1948) 245-277. 7 Gross, C. G., Bender, D. B. and Mishkin, M., Contributions of the corpus callosum and the anterior commissure to visual activation of inferior temporal neurons, Brain Research, 131 (1977) 227-239. 8 Hotel, J. A., The i ntertemporat component of the anterior commissure of the rat, Anat. Rec., 190 (1978) 424-425. 9 Pandya, D. N., Karol, E. A. and Lele, P. P., The distribution of the anterior commissure in the squirrel monkey, Brain Research, 49 (1973) 177-180. 10 Price,J. L.,Anautoradiographicstudyofcomplementarylaminarpatternsofterminationofafferent fibers to the olfactory cortex, J. comp. Neurol., 150 (1973) 87-108. 11 Rose, M., Die sog. Reichrinde beim Menschen und beim Affen. 1I. Teil des Allocortex bei Tier und Mensch, J. Psychol. Neurol. ( Lpz.), 34 (1927) 261M01. 12 Turner, B. H., Afferents to the macaque amygdala by way of the anterior commissure, Neurosci. Abstr., 4 (1978) 228. 13 Turner, B. H. and Mishkin, M., A reassessment of the direct projections of the olfactory bulb, Brain Research, 151 (1978) 375-380. 14 Turner, B. H., Gupta, K. and Mishkin, M., The locus and cytoarchitecture of the projection areas of the olfactory bulb in Macaca mulatta, J. comp. Neurol., 177 (1978) 381-396.
337 15 Turner, B. H., Mishkin, M. and Knapp, M. E., Visual and other sensory inputs to the amygdala of the Rhesus monkey, Neurosci. Abstr., 2 (1976) 398. 16 Van Alphen, H. A. M., The anterior commissure of the rabbit, Acta anat. (Basel), 57 (1969) 1-112. 17 Van Hoesen, G. W. and Pandya, D. N., Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents, Brain Research, 95 (1975) 1-24. 18 Vogt, B., A reduced silver stain for normal axons in the central nervous system, Physiol. Behav., 13 (1974) 837-840. 19 Zeki, S. M., Comparison of the cortical degeneration in the visual regions of the temporal lobe of the monkey following section of the anterior commissure and the splenium, J. comp. Neurol., 148 (1973) 167 176.