Brain Research, 159 (1978) 371-378 © Elsevier/North-Holland Biomedical Press
371
Short Communications Some observations on the patterns of segregated geniculate inputs to the visual cortex in New World primates: an autoradiographic study MICHAEL H. ROWE*, L. A. BENEVENTO** and MICHAEL REZAK
Department of Anatomy, College of Medicine, University of Illinois Medical Center, Chicago, IlL 60680
(U.S.A.) (Accepted August 31 st, 1978)
Both the internal structure and the pattern of primary afferent connections of striate cortex (area 17) appear to vary considerably among primates. For example, the striate cortex of the Old World macaque monkey is usually described as having an expanded layer IV, comprised of 3 sublayers, IVA, IVB and IVC. Some investigators14 regard layer IVC as consisting of two parts, an upper IVCa and a lower IVCfl. Layers IVA and IVCfl are the sites of termination of axons arising from the parvocellular layers of the dorsal lateral geniculate nucleus (LGN) 4,7,16. Layer IVCa receives input from the magnocellular layers, while layer IVB apparently gets little or no LGN input 7. In all geniculo-recepient layers of macaque monkey striate cortex, there is a horizontal segregation of geniculate terminals relaying ipsilateral and contralateral retinal input into discrete non-overlapping patches4.7,1n,2a which correspond to the physiologically described ocular dominance columns6. In contrast, the striate cortex of the New World owl monkey (Aotus trivirgatus) is generally described as having an expanded layer III and a relatively undifferentiated layer IV 11. LGN afferents terminate in a single horizontal band which includes layer IV and extends into layer II111. Furthermore, there does not appear to be any segregation of LGN terminals relaying ipsilateral and contralateral retinal input as there is in the macaque. These differences may represent characteristic differences between the Old and New World monkeys, but since the macaque monkey is diurnal and largely terrestrial and the owl monkey is nocturnal and arboreal, it seems equally possible that ecological factors may be responsible. Thus the retina of the macaque monkey contains both rods and cones and has a well-developed fovea, while the retina of the owl monkey contains few or no cones 3,9 and typically has an area centralis rather than a fovea9,22. The pattern of segregation of ipsilateral from contralateral retinal input to the LGN also differs considerably1°. It seems reasonable to expect that the organization of striate cortex would reflect the organization of lower levels of the visual pathway more than the * Present Address: Department of Psychology, University of California, Riverside, Calif. 92521
(U.S.A.) ** To whom correspondence and reprint requests should de addressed.
372 taxonomic status of the animals. In this regard the squirrel monkey (Saimiri sciureus) is of particular interest. Although the squirrel monkey is a New World monkey like Aotus, it is diurnal like the macaque, and more closely resembles the macaque in the organization of the retina and L G N 2°. We have examined the pattern of L G N projections in the squirrel monkey and the owl monkey with transneuronal autoradiography in an attempt to determine how the organization of these projections is related to the organization of lower levels of the visual pathway: particularly how and to what extent segregation of various types of retinal afferents in the L G N is associated with segregation of L G N terminals in the visual cortex. One mCi each of [aH]proline and [3H]fucose were injected into the vitreous chamber of the eye of one adult squirrel monkey and one adult owl monkey. After a 3 week survival time the animals were perfused transcardially with 0.9 ~ saline followed by 10 ~ formalin. Every 10th transverse frozen section (20 #m) was processed and analyzed as described before1,16, 23. There is some disagreement over terminology for the cytoarchitecture of area 17, particularly in regard to various subdivisions of layers III and IV. We have adopted the terminology proposed by Lund t4 because it is a much less arbitrary criterion than the use of descriptive similarity, and has the further advantage that what is called layer IV in one animal, e.g. macaque, will then correspond to what is called layer IV in another, e.g. squirrel monkey, in that they are both derivatives of the same embryological cell group. In this scheme (Fig. l) layer III is very much reduced in width
Fig. 1. Light- and dark-field photomicrographs of striate cortex of a squirrel monkey to show the laminar distribution of grains in layer IV of striate cortex contralateral to the injected eye. The heaviest projection is seen ending in layer IVCfl, with lighter grain densities found in IVCa, possibly extending into the bottom of IVB. A thin patchy band of grains is also visible in layer IVA.
373 while layer IV is enlarged and divided into three major sublaminae; IVA, IVB and IVC. As in the macaque, the narrow layer IVA is more apparent in some regions of striate cortex than others and is often difficult to distinguish from layer III in Nissl material. In owl monkeys, layer IVA seems severely reduced and may be absent altogether (Fig. 2). Layer IVB is sparsely populated with both large (pyramidal) and small (stellate)neurons, and is the location of the stria of Gennari. Layer IVC is populated exclusively with small (stellate) neurons, and is further subdivided into a less dense IVCa, and a more dense IVCfl. In autoradiographs of striate cortex of the squirrel monkey, both ipsilateral and contralateral to the injected eye, grains were found in layer IVA and in both subdivisions of layer IVC (Fig. 1). In this respect the LGN projection in this species is identical to that described previously in the macaque4,8,16,23. However, there was no tendency for the grains in layer IVC to be segregated into horizontally arranged patches or columns. Layer IVA, however, did contain some irregularly occurring patches (Fig. 1), but unevenness in the grain distribution in layer IVA of the macaque can also be observed, even within a single 'column'4,16. We also noted that the grain density in IVCa appears to be less than in IVCfl and that overall grain densities are lower in the ipsilateral cortex. In the owl monkey, both ipsilateral and contralateral to the injected eye, grains were confined entirely to layer IVC, with no evidence for a projection to a possible layer IVA (Fig. 2). Like the squirrel monkey (Fig. 1), grains also seemed to encroach slightly on layer IVB and a distinction between the densities in IVCa and IVCfl was also apparent (Fig. 2), Apart from differences in terminology, this laminar distribution of grains corresponds very well with that previously reported in the owl monkey11. However, contrary to earlier reports 26, we were able to obtain evidence for a fairly regular sequence of patches or alternating areas of high and low grain density. These patches seemed to be present only in layer IVCa and in our material could only be seen in the cortex ipsilateral to the injected eye (Fig. 2). Furthermore, they could only be seen in the upper bank of the calcarine fissure in about the middle of its anterior half. They varied in width from 200-400 #m, which is similar to the range of widths of patches seen in the macaque monkey7,23. In both squirrel and owl monkeys the amount of grains present in layer VI was denser than that found in layer V but we could not be sure that this was due to labeled terminals or axons. However, an LGN projection to layer VI of area 17 has been reported by others 4,16. There was no evidence for any projections outside of area 17. The major results of this investigation involve the projection from the LGN to visual cortex in the squirrel monkey and owl monkey and can be summarized as follows: (l) LGN projections appear to be restricted to area 17 in both species; (2) the laminar distribution of terminals within area 17 of squirrel monkeys is nearly identical to that observed in the macaque monkey, whereas LGN terminals appear to be largely restricted to layer IVC in owl monkeys; (3) there does not appear to be any segregation in area 17 of geniculate axons relaying ipsilateral and contralateral retinal input in squirrel monkeys, but there could be some degree of ocular segregation in owl monkeys. There is a type of segregated input to layer IVA in squirrel monkey, but this does not seem related to ocularity. Our data in squirrel monkey appears to be in
Fig. 2. Top: light- and dark-field photomicrographs of striate cortex of an owl monkey to show the laminar distribution of grains in layer IV of striate cortex contralateral to the injected eye. The distribution of grains within layers IVCa and IVCfl is very similar to that seen in squirrel monkeys. However, there are no grains above layer IVB, suggesting that there is no projection to a possible layer IVA in this species. Bottom: dark-field photomicrograph of owl monkey striate cortex ipsilateral to the injected eye. The grains in layer IVCa are clearly distributed in patches, while grains in IVCfl of the ipsilateral side (like all levels of layer IV on the contralateral side) are continuously distributed.
375 agreement with current 4 and previous reports s,2t. The owl monkey differs from both the squirrel monkey and the macaque, in that it does not appear to have an LGN projection to a possible layer IVA. The finding of segregated patches in the owl monkey was unexpected 11. It may be that these patches represent ocular dominance columns in the owl monkey and such columns have been demonstrated physiologically in another New World monkey, the spider monkeyO,L Previous authors tl did not completely rule out the existence of such columns in owl monkeys, however, pointing out that the autoradiographs might require a particular plane of section. The apparent restriction of ocular dominance columns to deep regions of the calcarine fissure may also be an artifact of plane of section. If not, however, a physiological comparison of areas of striate cortex which have ocular segregation with those that do not would be very informative. A unique feature of the owl monkey ocular dominance system is that the segregation is apparent only in layer IVCa. This does not seem to have been reported before. The possibility must be considered that the lack of apparent ocular segregation in layer IVCfl or in the cortex contralateral to the injected eye is due to 'spillage' in the geniculate ~3. In owl monkeys, layer IVCa presumably receives input from magnocellular layers, and layer IVCfl from parvocellular layers, as is true for both rhesus and squirrel monkeys. Due to the arrangement of LGN layers in owl monkeys 10, the magnocellular layers both ipsilateral and contralateral to the injected eye would be subject to spillage, however, the external magnocellular layer on the ipsilateral side would be twice as affected as the internal magnocellular layer on the contralateral side. Yet it is on the ipsilateral side where the columns in cortical layer IVCa are apparent, and not on the contralateral side. Although the internal parvocellular layer on the contralateral side is subject to spillage from retinal fibers, the external parvocellular layer on the ipsilateral side is not. Thus, even allowing for some geniculate spillage, columns in layer IVCfl, if present, should be visible at least in the cortex ipsilateral to the injected eye and they are not. It is unlikely that LGN spillage could completely account for either of these observations. The possibility of a 'spillage' artifact 18 may explain instead, the absence of segregation in the squirrel monkey. However, since the pattern of segregation of ipsilateral from contralateral retinal fibers is the same in both macaque and squirrel monkeys, it is difficult to see how such spillage would completely obscure ocular dominance columns in the squirrel monkey cortex, while leaving them so distinct in macaque monkey cortex. In both the macaque and the owl monkey it has been shown that the magnocellular layers of the LGN receive input from Y-like retinal ganglion cells, while parvocellular layers get input from X-like retinal afferentsZ,7, is. Although retinal input to the LGN in squirrel monkeys has not been characterized in X-Y terms, it has been shown that fast optic tract fibers probably project to magnocellular layers and slow tract fibers to parvocellular layers zo. Thus, in all 3 primate species it appears that different retinal inputs cart be segregated into separate LGN layers. This is in contrast to the cat where X- and Y-retinal inputs are largely intermixed in layers A and A1 and to a lesser extent in layer C z4, although physiologically they remain quite distinct. It is interesting that these differences in the degree of differentiation in the LGN and in the retinogeniculate projections are clearly
376 reflected in the degree of differentiation seen in the striate cortex and in geniculostriate projections. In both macaque and squirrel monkey, parvoceilular and magnocellular inputs (and presumably X and Y, respectively) to striate cortex are segregated into separate subdivisions of layer IV; parvocellular layers project to layer IVA and to IVCfl, while magnocellular layers project to layer IVCa. In the cat, on the other hand, the projections of X- and Y-geniculate relay cells are not completely segregated anatomically within striate cortex, both terminating within a relatively undifferentiated layer IV, and in layer VP 2. Here, as in the LGN however, there is evidence that the X- and Y-pathways remain to some extent physiologically distinct at least as far as the first cortical synapse ~,19, despite the lack of anatomical segregation. Furthermore, the C-laminae of the cat LGN which relay W-cell activity to striate cortex is, project to areas above and below the A and A1 projections lz. Thus, in all cases laminar segregation of functional cell types in the LGN corresponds to laminar segregation of their projections to striate cortex. This is in marked contrast to the tendency for inputs originating in the two eyes to be segregated into horizontally arranged columns or patches rather than into layers 7,11,13. The significance of this may be that such laminar segregation of afferent terminals, potentially at least, provides functionally distinct subsets of afferent fibers access to different populations of cortical cells, while horizontal segregation provides certain afferents with access to separate individuals within a common population of ceils. As further support for the argument that cortical layers represent different functional thalamic targets just as well as different cortical areas, are the findings in the macaque monkey which show that while the LGN does not project to any layer above IVA 4,18, the inferior pulvinar and adjacent lateral pulvinar, project to all layers above layer IVA in area 17, i.e. layers I, II and III 1,15,16. These pulvinar paths to the supragranular layers are believed to be routes whereby information from the superior colliculus and prestriate cortex can reach primary visual cortex 1,16. In the cat the superior colliculus receives W-cell input from the retina and in the monkey similar types of ganglion ceils also project to the superior colliculus with X-cell input probably being absenP 7. If the tectal path to the inferior pulvinar is carrying different information than that sorted by the geniculate layers then these extrageniculate inputs provide another example of the laminar segregation of functional inputs in primary visual cortex. In this latter case the functional separation takes place at the thalamic level between nuclei rather than within a nucleus. These extrageniculate projections to the supragranular layers are also segregated horizontally into patches, but it is not possible to say if this pattern of input represents ocularity as does the geniculostriate system 16. While these extrageniculate paths may also exist in the squirrel monkey 15, it remains to be seen if they exist in the owl monkey. But we can conclude from the present study that if the L G N projection to layer IVC in owl monkeys is like that of macaque 7 and squirrel monkeys 4, then the ocular dominance system reported here would seem to involve only the Y-channel in this animal whereas it apparently involves both X- and Y-channels in the macaque. These predictions need to be tested in physiological terms, but if substantiated, would mean that our eventual understanding of the function of ocular dominance columns will be facilitated by an analysis of
377 this t y p e o f v a r i a t i o n , a n d t h a t a n y c o m p l e t e e x p l a n a t i o n o f t h e f u n c t i o n o f o c u l a r d o m i n a n c e systems m u s t t a k e i n t o a c c o u n t t h e n a t u r e o f t h e t h a l a m i c afferents involved. T h i s w o r k was s u p p o r t e d by N I H G r a n t E Y 2940. T h e a u t h o r s are g r a t e f u l t o D r . F r a n k B e l l u h a n a n d M r . W. J o n e s for t h e i r expert care of the monkeys.
1 Benevento, L. A. and Rezak, M., Extrageniculate projections to layers VI and I of striate cortex (area 17) in the rhesus monkey Macaca mulatta, Brain Research, 96 (1975) 51-55. 2 Dreher, B., Fukada, Y. and Rodieck, R. W., Identification, classification and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of old world primate, J. Physiol. ( Lond.) , 258 (1976) 433-452. 3 Ferraz de Oliveira, L. and Ripps, H., The 'area centralis' of the owl monkey (Aotes trivirgatus), Vision Res., 8 (1968) 223-228. 4 Hendrickson, A. E., Wilson, J. R. and Ogren, P. O., Organization of pathways between dorsal lateral geniculate nucleus and visual cortex in Old and New World primates, J. comp. Neurol., submitted for publication. 5 Hoffmann, K. P. and Stone, J., Conduction velocity of afferents to cat visual cortex: a correlation with cortical receptive field properties, Brain Research, 32 (1971) 460-466. 6 Hubel, D. H. and Wiesel, T. N., Receptive fields and functional architecture of monkey striate cortex, J. Physiol. (Lond.), 195 (1968) 215-243. 7 Hubel, D. H. and Wiesel, T. N., Laminar and columnar distribution of geniculocortical fibers in the macaque monkey, J. comp. Neurol., 146 (1972) 421-450. 8 Hubel, D. H., Wiesel, T. N. and LeVay, S., Functional architecture of area 17 in normal and monocularly deprived macaque monkeys, Cold Spr. Harb. Syrup. quant. Biol., 40 (1975) 581-589. 9 Jones, A. E., The reginal structure of (Aotes trivirgatus) the owl monkey, J. comp. NeuroL, 125 (1965) 19-28. 10 Kaas, J. H.,Guillery, R.W. andAllman, J. M.,Someprinciplesoforganizationinthedorsallateral geniculate nucleus, Brain Behav. Evol., 6 (1972) 253-299. 11 Kaas, J. H., Lin, C. S. and Casagrande, V. A., The relay ofipsilateral and contralateral retinal input from the lateral geniculate nucleus to striate cortex in the owl monkey: a transneuronal transport study, Brain Research, 106 (1976) 371-378. 12 LeVay, S. and Gilbert, C. D., Laminar patterns of geniculocortical projection in the cat, Brain Research, 113 (1976) 1-19. 13 LeVay, S., Stryker, M. P. and Shatz, C. J., Ocular dominance columns and their development in layer IV of the cat's visual cortex: a quantitative study, J. comp. Neurol., 179 (1978) 223-244. 14 Lund, J. S., Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta), J. comp. Neurol., 147 (1973) 455-496. 15 Ogren, M. P. and Hendrickson, A. E., The distribution of pulvinar terminals in visual areas 17 and 18 of the monkey, Brain Research, 137 (1978) 343-350. 16 Rezak, M. and Benevento, L. A., A comparison of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to striate cortex (area 17) in the macaque monkey, Brain Research, submitted for publication. 17 Schiller, P. H. and Malpeli, J. G., Properties and tectal projections of monkey retinal ganglion cells, J. Neurophysiol., 40 (1977) 428-445. 18 Sherman, S. M., Wilson, J. R., Kaas, J. H. and Webb, S. V., X- and Y-cells in the dorsal lateral geniculate nucleus of the owl monkey (Aotus trivirgatus), Science, 192 (1976) 475-477. 19 Stone, J., Morphology and physiology of the geniculocortical synapse in the cat: The question of parallel input to the striate cortex, Invest. Ophthal., 11 (1972) 338-346. 20 Tigges, J. and O'Steen, W. K., Termination of retinofugal fibers in squirrel monkey: a reinvestigation using autoradiographic methods, Brain Research, 79 (1974) 489-495. 21 Tigges, J., Tigges, M. and Perachio, A. A., Complementary laminar terminations of afferents to area 17 originating in area 18 and in the lateral geniculate nucleus in squirrel monkey, J. eomp. NeuroL, 176 (1977) 87-100.
378 22 Webb, S. V. and Kaas, J. H., The sizes and distribution of ganglion cells in the retina of the owl monkey, Aotus trivirgatus, Vision Res., 16 (1976) 1247-1254. 23 Wiesel, T. N., Hubel, D. H. and Lam, D. M. K., Autoradiographic demonstration of oculardominance columns in the monkey striate cortex by means of transneuronal transport, Brain Research, 79 (1974) 273-279. 24 Wilson, P. D., Rowe, M. H. and Stone, J., Properties ofrelay cells in cat's lateral geniculate nucleus: a comparison of W-cells with X- and Y-cells, J. NeurophysioL, 39 (1976) 1193-1209.
371
Short Communications Some observations on the patterns of segregated geniculate inputs to the visual cortex in New World primates: an autoradiographic study MICHAEL H. ROWE*, L. A. BENEVENTO** and MICHAEL REZAK
Department of Anatomy, College of Medicine, University of Illinois Medical Center, Chicago, IlL 60680
(U.S.A.) (Accepted August 31 st, 1978)
Both the internal structure and the pattern of primary afferent connections of striate cortex (area 17) appear to vary considerably among primates. For example, the striate cortex of the Old World macaque monkey is usually described as having an expanded layer IV, comprised of 3 sublayers, IVA, IVB and IVC. Some investigators14 regard layer IVC as consisting of two parts, an upper IVCa and a lower IVCfl. Layers IVA and IVCfl are the sites of termination of axons arising from the parvocellular layers of the dorsal lateral geniculate nucleus (LGN) 4,7,16. Layer IVCa receives input from the magnocellular layers, while layer IVB apparently gets little or no LGN input 7. In all geniculo-recepient layers of macaque monkey striate cortex, there is a horizontal segregation of geniculate terminals relaying ipsilateral and contralateral retinal input into discrete non-overlapping patches4.7,1n,2a which correspond to the physiologically described ocular dominance columns6. In contrast, the striate cortex of the New World owl monkey (Aotus trivirgatus) is generally described as having an expanded layer III and a relatively undifferentiated layer IV 11. LGN afferents terminate in a single horizontal band which includes layer IV and extends into layer II111. Furthermore, there does not appear to be any segregation of LGN terminals relaying ipsilateral and contralateral retinal input as there is in the macaque. These differences may represent characteristic differences between the Old and New World monkeys, but since the macaque monkey is diurnal and largely terrestrial and the owl monkey is nocturnal and arboreal, it seems equally possible that ecological factors may be responsible. Thus the retina of the macaque monkey contains both rods and cones and has a well-developed fovea, while the retina of the owl monkey contains few or no cones 3,9 and typically has an area centralis rather than a fovea9,22. The pattern of segregation of ipsilateral from contralateral retinal input to the LGN also differs considerably1°. It seems reasonable to expect that the organization of striate cortex would reflect the organization of lower levels of the visual pathway more than the * Present Address: Department of Psychology, University of California, Riverside, Calif. 92521
(U.S.A.) ** To whom correspondence and reprint requests should de addressed.
372 taxonomic status of the animals. In this regard the squirrel monkey (Saimiri sciureus) is of particular interest. Although the squirrel monkey is a New World monkey like Aotus, it is diurnal like the macaque, and more closely resembles the macaque in the organization of the retina and L G N 2°. We have examined the pattern of L G N projections in the squirrel monkey and the owl monkey with transneuronal autoradiography in an attempt to determine how the organization of these projections is related to the organization of lower levels of the visual pathway: particularly how and to what extent segregation of various types of retinal afferents in the L G N is associated with segregation of L G N terminals in the visual cortex. One mCi each of [aH]proline and [3H]fucose were injected into the vitreous chamber of the eye of one adult squirrel monkey and one adult owl monkey. After a 3 week survival time the animals were perfused transcardially with 0.9 ~ saline followed by 10 ~ formalin. Every 10th transverse frozen section (20 #m) was processed and analyzed as described before1,16, 23. There is some disagreement over terminology for the cytoarchitecture of area 17, particularly in regard to various subdivisions of layers III and IV. We have adopted the terminology proposed by Lund t4 because it is a much less arbitrary criterion than the use of descriptive similarity, and has the further advantage that what is called layer IV in one animal, e.g. macaque, will then correspond to what is called layer IV in another, e.g. squirrel monkey, in that they are both derivatives of the same embryological cell group. In this scheme (Fig. l) layer III is very much reduced in width
Fig. 1. Light- and dark-field photomicrographs of striate cortex of a squirrel monkey to show the laminar distribution of grains in layer IV of striate cortex contralateral to the injected eye. The heaviest projection is seen ending in layer IVCfl, with lighter grain densities found in IVCa, possibly extending into the bottom of IVB. A thin patchy band of grains is also visible in layer IVA.
373 while layer IV is enlarged and divided into three major sublaminae; IVA, IVB and IVC. As in the macaque, the narrow layer IVA is more apparent in some regions of striate cortex than others and is often difficult to distinguish from layer III in Nissl material. In owl monkeys, layer IVA seems severely reduced and may be absent altogether (Fig. 2). Layer IVB is sparsely populated with both large (pyramidal) and small (stellate)neurons, and is the location of the stria of Gennari. Layer IVC is populated exclusively with small (stellate) neurons, and is further subdivided into a less dense IVCa, and a more dense IVCfl. In autoradiographs of striate cortex of the squirrel monkey, both ipsilateral and contralateral to the injected eye, grains were found in layer IVA and in both subdivisions of layer IVC (Fig. 1). In this respect the LGN projection in this species is identical to that described previously in the macaque4,8,16,23. However, there was no tendency for the grains in layer IVC to be segregated into horizontally arranged patches or columns. Layer IVA, however, did contain some irregularly occurring patches (Fig. 1), but unevenness in the grain distribution in layer IVA of the macaque can also be observed, even within a single 'column'4,16. We also noted that the grain density in IVCa appears to be less than in IVCfl and that overall grain densities are lower in the ipsilateral cortex. In the owl monkey, both ipsilateral and contralateral to the injected eye, grains were confined entirely to layer IVC, with no evidence for a projection to a possible layer IVA (Fig. 2). Like the squirrel monkey (Fig. 1), grains also seemed to encroach slightly on layer IVB and a distinction between the densities in IVCa and IVCfl was also apparent (Fig. 2), Apart from differences in terminology, this laminar distribution of grains corresponds very well with that previously reported in the owl monkey11. However, contrary to earlier reports 26, we were able to obtain evidence for a fairly regular sequence of patches or alternating areas of high and low grain density. These patches seemed to be present only in layer IVCa and in our material could only be seen in the cortex ipsilateral to the injected eye (Fig. 2). Furthermore, they could only be seen in the upper bank of the calcarine fissure in about the middle of its anterior half. They varied in width from 200-400 #m, which is similar to the range of widths of patches seen in the macaque monkey7,23. In both squirrel and owl monkeys the amount of grains present in layer VI was denser than that found in layer V but we could not be sure that this was due to labeled terminals or axons. However, an LGN projection to layer VI of area 17 has been reported by others 4,16. There was no evidence for any projections outside of area 17. The major results of this investigation involve the projection from the LGN to visual cortex in the squirrel monkey and owl monkey and can be summarized as follows: (l) LGN projections appear to be restricted to area 17 in both species; (2) the laminar distribution of terminals within area 17 of squirrel monkeys is nearly identical to that observed in the macaque monkey, whereas LGN terminals appear to be largely restricted to layer IVC in owl monkeys; (3) there does not appear to be any segregation in area 17 of geniculate axons relaying ipsilateral and contralateral retinal input in squirrel monkeys, but there could be some degree of ocular segregation in owl monkeys. There is a type of segregated input to layer IVA in squirrel monkey, but this does not seem related to ocularity. Our data in squirrel monkey appears to be in
Fig. 2. Top: light- and dark-field photomicrographs of striate cortex of an owl monkey to show the laminar distribution of grains in layer IV of striate cortex contralateral to the injected eye. The distribution of grains within layers IVCa and IVCfl is very similar to that seen in squirrel monkeys. However, there are no grains above layer IVB, suggesting that there is no projection to a possible layer IVA in this species. Bottom: dark-field photomicrograph of owl monkey striate cortex ipsilateral to the injected eye. The grains in layer IVCa are clearly distributed in patches, while grains in IVCfl of the ipsilateral side (like all levels of layer IV on the contralateral side) are continuously distributed.
375 agreement with current 4 and previous reports s,2t. The owl monkey differs from both the squirrel monkey and the macaque, in that it does not appear to have an LGN projection to a possible layer IVA. The finding of segregated patches in the owl monkey was unexpected 11. It may be that these patches represent ocular dominance columns in the owl monkey and such columns have been demonstrated physiologically in another New World monkey, the spider monkeyO,L Previous authors tl did not completely rule out the existence of such columns in owl monkeys, however, pointing out that the autoradiographs might require a particular plane of section. The apparent restriction of ocular dominance columns to deep regions of the calcarine fissure may also be an artifact of plane of section. If not, however, a physiological comparison of areas of striate cortex which have ocular segregation with those that do not would be very informative. A unique feature of the owl monkey ocular dominance system is that the segregation is apparent only in layer IVCa. This does not seem to have been reported before. The possibility must be considered that the lack of apparent ocular segregation in layer IVCfl or in the cortex contralateral to the injected eye is due to 'spillage' in the geniculate ~3. In owl monkeys, layer IVCa presumably receives input from magnocellular layers, and layer IVCfl from parvocellular layers, as is true for both rhesus and squirrel monkeys. Due to the arrangement of LGN layers in owl monkeys 10, the magnocellular layers both ipsilateral and contralateral to the injected eye would be subject to spillage, however, the external magnocellular layer on the ipsilateral side would be twice as affected as the internal magnocellular layer on the contralateral side. Yet it is on the ipsilateral side where the columns in cortical layer IVCa are apparent, and not on the contralateral side. Although the internal parvocellular layer on the contralateral side is subject to spillage from retinal fibers, the external parvocellular layer on the ipsilateral side is not. Thus, even allowing for some geniculate spillage, columns in layer IVCfl, if present, should be visible at least in the cortex ipsilateral to the injected eye and they are not. It is unlikely that LGN spillage could completely account for either of these observations. The possibility of a 'spillage' artifact 18 may explain instead, the absence of segregation in the squirrel monkey. However, since the pattern of segregation of ipsilateral from contralateral retinal fibers is the same in both macaque and squirrel monkeys, it is difficult to see how such spillage would completely obscure ocular dominance columns in the squirrel monkey cortex, while leaving them so distinct in macaque monkey cortex. In both the macaque and the owl monkey it has been shown that the magnocellular layers of the LGN receive input from Y-like retinal ganglion cells, while parvocellular layers get input from X-like retinal afferentsZ,7, is. Although retinal input to the LGN in squirrel monkeys has not been characterized in X-Y terms, it has been shown that fast optic tract fibers probably project to magnocellular layers and slow tract fibers to parvocellular layers zo. Thus, in all 3 primate species it appears that different retinal inputs cart be segregated into separate LGN layers. This is in contrast to the cat where X- and Y-retinal inputs are largely intermixed in layers A and A1 and to a lesser extent in layer C z4, although physiologically they remain quite distinct. It is interesting that these differences in the degree of differentiation in the LGN and in the retinogeniculate projections are clearly
376 reflected in the degree of differentiation seen in the striate cortex and in geniculostriate projections. In both macaque and squirrel monkey, parvoceilular and magnocellular inputs (and presumably X and Y, respectively) to striate cortex are segregated into separate subdivisions of layer IV; parvocellular layers project to layer IVA and to IVCfl, while magnocellular layers project to layer IVCa. In the cat, on the other hand, the projections of X- and Y-geniculate relay cells are not completely segregated anatomically within striate cortex, both terminating within a relatively undifferentiated layer IV, and in layer VP 2. Here, as in the LGN however, there is evidence that the X- and Y-pathways remain to some extent physiologically distinct at least as far as the first cortical synapse ~,19, despite the lack of anatomical segregation. Furthermore, the C-laminae of the cat LGN which relay W-cell activity to striate cortex is, project to areas above and below the A and A1 projections lz. Thus, in all cases laminar segregation of functional cell types in the LGN corresponds to laminar segregation of their projections to striate cortex. This is in marked contrast to the tendency for inputs originating in the two eyes to be segregated into horizontally arranged columns or patches rather than into layers 7,11,13. The significance of this may be that such laminar segregation of afferent terminals, potentially at least, provides functionally distinct subsets of afferent fibers access to different populations of cortical cells, while horizontal segregation provides certain afferents with access to separate individuals within a common population of ceils. As further support for the argument that cortical layers represent different functional thalamic targets just as well as different cortical areas, are the findings in the macaque monkey which show that while the LGN does not project to any layer above IVA 4,18, the inferior pulvinar and adjacent lateral pulvinar, project to all layers above layer IVA in area 17, i.e. layers I, II and III 1,15,16. These pulvinar paths to the supragranular layers are believed to be routes whereby information from the superior colliculus and prestriate cortex can reach primary visual cortex 1,16. In the cat the superior colliculus receives W-cell input from the retina and in the monkey similar types of ganglion ceils also project to the superior colliculus with X-cell input probably being absenP 7. If the tectal path to the inferior pulvinar is carrying different information than that sorted by the geniculate layers then these extrageniculate inputs provide another example of the laminar segregation of functional inputs in primary visual cortex. In this latter case the functional separation takes place at the thalamic level between nuclei rather than within a nucleus. These extrageniculate projections to the supragranular layers are also segregated horizontally into patches, but it is not possible to say if this pattern of input represents ocularity as does the geniculostriate system 16. While these extrageniculate paths may also exist in the squirrel monkey 15, it remains to be seen if they exist in the owl monkey. But we can conclude from the present study that if the L G N projection to layer IVC in owl monkeys is like that of macaque 7 and squirrel monkeys 4, then the ocular dominance system reported here would seem to involve only the Y-channel in this animal whereas it apparently involves both X- and Y-channels in the macaque. These predictions need to be tested in physiological terms, but if substantiated, would mean that our eventual understanding of the function of ocular dominance columns will be facilitated by an analysis of
377 this t y p e o f v a r i a t i o n , a n d t h a t a n y c o m p l e t e e x p l a n a t i o n o f t h e f u n c t i o n o f o c u l a r d o m i n a n c e systems m u s t t a k e i n t o a c c o u n t t h e n a t u r e o f t h e t h a l a m i c afferents involved. T h i s w o r k was s u p p o r t e d by N I H G r a n t E Y 2940. T h e a u t h o r s are g r a t e f u l t o D r . F r a n k B e l l u h a n a n d M r . W. J o n e s for t h e i r expert care of the monkeys.
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