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The projection of the superior colliculus upon the lateral geniculate body in tupaia glis and galago senegalensis
494
Brain Research, 194 (1980) 494 499 ~, Elsevier/North-Holland Biomedical Press
The projection of the superior colliculus upon the lateral geniculate body in
Tupaia g/is and Go~ago senegalensis D. FITZPATRICK, R. G. CAREY* and I. T. DIAMOND Department of Psychology, Duke University, Durham, N.C. 27706 (U.S.A.) (Accepted March 20th, 1980) Key words: lateral geniculate body -- superior colliculus -- tecto-geniculate projection
In a previous study of the laminar organization of the lateral geniculate body (GL) in the tree shrew, Tupaia glis, and in Galago senegalensis, we restricted HRP to the superficial layers of the striate cortex and found that only certain layers of the lateral geniculate body contained labeled cells 3. We concluded that the small celled layers as well as certain interlaminar zones in both of these species project to the superficial layers of the striate cortex. The present report presents evidence that these same zones of the lateral geniculate body that project to the superficial layers of the striate cortex are further distinguished from the rest of the lateral geniculate body by receiving fibers from the superficial layers of the superior colliculus. A total of 2 tree shrews and 6 galagos were used in these experiments. Iontophoretic injections of a 1:1 tritiated proline-leucine mixture which had been reconstituted to 50-80 #Ci/tzl with 0.1 M acetate buffer at pH 4.8 were made into the superior colliculus of each animal. Following a survival period of 48 h, the animals were deeply anesthetized and perfused with 109~ buffered formalin. The brains were stored for several days in a 3090 sucrose-formalin solution, after which they were sectioned at 40 ktm on a freezing microtome and processed for autoradiography using standard proceduresL Exposure times for the autoradiographs ranged from 4-10 weeks. Following the injection of tritiated amino acids into the superficial layers of the superior colliculus in the tree shrew, labeled fibers can be seen leaving the injection site and passing ventrally and laterally to enter the brachium of the superior colliculus. These fibers course rostrally within the optic tract until they terminate in the lateral geniculate body. The distribution of terminals within the lateral geniculate body is illustrated in the series of coronal sections presented in Fig. la. In section 191 (the most caudal section) silver grains are visible over layer 6 just adjacent to the optic * Present address: Division of Neurobiology, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix, Ariz. 85013, U.S.A.
495 tract. In more rostral sections (195 and 199), silver grains appear in two bands; one occupying the interlaminar zone between layers 4 and 5, and the other lying within layer 3. Finally, a small patch o f silver grains can be seen just medial to layer 1 along the border o f the pulvinar nucleus. A p h o t o m i c r o g r a p h o f a portion o f section 199 is shown in Fig. 2a. Following injections o f tritiated amino acids into the superficial layers o f the superior colliculus in galago, labeled fibers can be traced rostrally within the brachium o f the superior colliculus and the optic tract to their terminations within the lateral geniculate body. Fig. lc and the p h o t o m i c r o g r a p h in Fig. 2b illustrate the distribution o f terminals within the lateral geniculate body. The greatest n u m b e r o f silver grains appear a r o u n d the cells o f layers 4 and 5. Patches o f labeled terminals are also present TUPAIA
GALAGO
1,1,
C. a.
d.
1605
1ram
Fig. 1. A: coronal sections through the lateral geniculate body of the tree shrew illustrating the distribution of labeled terminals following an injection of tritiated amino acids into the superior colliculus. Section 191 is the most caudal, while section 199 is the most rostral. The bracket and arrow in section 199 refer to the photomicrograph shown in Fig. 2a. b: coronal sections through the lateral geniculate body of the tree shrew illustrating the distribution of labeled cells following the application of HRP to the superficial layers of the striate cortex3. Section 148 is caudal to section 154. c" parasagittal sections through the lateral geniculate body of galago illustrating the distribution of labeled terminals following an injection of tritiated amino acids into the superior colliculus. Section 285 is medial to section 293. The arrow and bracket in section 285 refer to the photomicrograph in Fig. 2b. d: parasagittal secsections through the lateral geniculate body of galago illustrating the distribution of labeled cells following the application of HRP to the superficial layers of the striate cortex3. Section 116 is medial to section 114. TO, optic tract.
496
Fig. 2. a: dark-field light-field photomicrograph showing the distribution of autoradiographically labeled terminals in the lateral geniculate body of the tree shrew following all injection of tritiated amino acids into the superior colliculus. This photomicrograph corresponds to the bracketed region of section 199, Fig. la ( . 47). b: dark-field-light-field photomicrograph showing the distribution of autoradiographically labeled terminals in the lateral geniculate body of galago following an injection of tritiated amino acids into the superior colliculus. This photomicrograph corresponds to the bracketed region of section 285, Fig. lc. ( 5 2 ) . in the interlaminar zones between layers 1 and 2 and layers 2 and 3 as well as at the junction of layer 1 and the optic tract. The density of grains over layers 1, 2 and 3 is greater than the background level, but it seems reasonable to conclude that this label may be within fibers destined for layers 4 and 5 and the interlaminar zones. The presence of a pathway from the superficial layers of the superior colliculus to the lateral geniculate body is not a new finding. A tecto-geniculate projection has previously been reported in the squirrel, hedgehog, tree shrew, cat and monkey 2,4,1 ~, >1-16,z'~,~a and the cells of origin of this pathway within the superficial layers of the superior colliculus have also been shown 1,19,23. The significance of the present results lies in a comparison of the distribution of tecto-geniculate terminals with the distribution of labeled cells within the lateral geniculate body following the application of H R P to the superficial layers of the striate cortex (Fig. Ib andd): the cells that lie within the tecto-recipient zones of the lateral geniculate body in both species are the source of fibers projecting to the most superficial layers (presumably layer 1) of the striate cortex 3. The discovery that layers 4 and 5 of the lateral geniculate body of galago are distinguished by input from the superficial layers of the superior colliculus and project to layer I of striate cortex, contributes to our understanding of the laminar organization of the lateral geniculate body in this species. The lateral geniculate body of galago consists of 3 pairs of layers which differ in cell size and layer of termination within the striate cortexa,l°, 27. Layers 1 and 2 consist of large neurons which send their axons to the upper tier of layer IV; these layers appear to be homologous to the magnocellular layers of other primates10,17, is. Layers 3 and 6 consist of medium-sized
497 neurons which send their axons to the lower tier of layer IV of the striate cortex; these layers appear to be homologous to the parvocellular layers of other primates 1°,17,1s. In contrast to the other pairs, layers 4 and 5 which contain small pale staining cells have no obvious counterpart in the lateral geniculate body of simian primates. However, the so-called S layer and the interlaminar zones of the squirrel monkey lateral geniculate body receive fibers from the superficial layers of the superior colliculus 15, suggesting that they may have at least a functional similarity with layers 4 and 5 in galago. The significance of these homologies and similarities is that they allow us to speculate about the retinal input to the various layers of the lateral geniculate body in galago. The magnocellular layers of the lateral geniculate body of several primate species have been shown to receive input from the Y-cell class of retinal ganglion cell, while the parvocellular layers receive input from the X-cell class~, 26. (We use the terms 'X-cell' and 'Y-cell' for convenience and their use does not imply that the issues posed by such a classificatory scheme have been resolved for any species, let alone the galago). Thus, it is likely that layers 1 and 2 of galago are the target of large Y-cell axons while layers 3 and 6 are the target of smaller X-cell axons. We suspect that the retinal input to layers 4 and 5 in galago may be similar to that of the S layers and interlaminar zones of the monkey, both of which have been shown to receive re~_inal input TM, but as yet these layers have not been examined physiologically. However, a number of similarities between layers 4 and 5 in galago and the parvocellular C layers of the lateral geniculate body of the cat suggest that layers 4 and 5 probably receive fine caliber W-cell input. First, the C layers of the cat consist of small pale staining neurons. Second, these geniculate layers receive fibers from the superficial layers of the superior colliculus11,19, 22. Third, the parvocellular C layers project to layer I of the striate cortex. This projection to layer I of the striate cortex in the cat has been shown both by injections of tritiated amino acids into the C layer complex z0 and by experiments in which HRP was restricted to the most superficial layers of the cortex2L Finally, the retinal fibers projecting to the parvocellular C layers of the cat are noticeably finer in caliber than the fibers projecting to the A laminae lz,13. We have noted a similar distinction in the retinal input to layers 4 and 5 of galago. The similarities between the C layers of the cat and layers 4 and 5 of galago taken together suggest that these layers are homologous. Since the C layers in the cat are dominated by W-cell input2S, 29, it is reasonable to argue that layers 4 and 5 of galago also receive fibers from the W-class of retinal ganglion cells. It is not easy to determine which layers of the lateral genieulate body in tree shrew may be homologous to the magnocellular or parvocellular layers in primates ~,~8. Furthermore, while there is electrophysiological evidence for a parcellation of cell types analogous to the X-Y classification in other species, it is not clear whether these classes are segregated into different layers, nor is it certain that there is W-cell input to the lateral geniculate body 25. But, for our purposes, the chief point to emphasize is that the tecto-recipient zones in the tree shrew lateral geniculate body have numerous characteristics in common with the recto-recipient zones of galago and the cat including cell size, layer of termination in striate cortex and fine caliber retinal
498 input a,:'. These similarities suggest that the tecto-recipient zones in all 3 species are homologous. The discovery o f a t e c t o - g e n i c u l o - s t r i a t e cortex projection system in species as divergent as galago, tree shrew a n d cat suggests that this system is an integral part o f the basic plan o f the m a m m a l i a n visual thalamus. F u r t h e r , since this projection terminates in layer I o f the striate cortex, and since it a p p e a r s to be related to small caliber retinal input, we are t e m p t e d to speculate that the tecto-recipient zones o f the lateral geniculate b o d y m a y represent a persistent r e m a i n d e r o f an early stage in the p h y l o g e n y o f the visual t h a l a m u s ; a stage that preceded the d e v e l o p m e n t o f the larger fibered retino-geniculate p a t h w a y s (X- a n d Y-cell class) and the separate tectot h a l a m i c target within the pulvinar. Relying chiefly on the c o m p a r i s o n between m a m m a l s a n d lower vertebrates, Ebbesson '~ also p r o p o s e d that the pulvinar nucleus and lateral geniculate nucleus evolved from a single cellular zone that received both tectal a n d retinal input. This research was s u p p o r t e d by N I M H P r e d o c t o r a l F e l l o w s h i p 07262 to D.F., N I M H P o s t d o c t o r a l F e l l o w s h i p 05867 to R . G . C . a n d N I M H Research G r a n t 04849 to I.T.D. We w o u l d like to t h a n k Pamela M a d r e n a n d Susan Havrilesky for their help in p r e p a r i n g the manuscript. 1 Albano, J. E., Norton, T. T. and Hall, W. C., Laminar origin of projections from the superficial layers of the superior colliculus in the tree shrew, Tupaia glis, Brain Research, 173 (1979) 1-I I. 2 Benevento, L. A. and Fallon, J. H., The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta), J. comp. Neurol., 160 (1975) 339-362. 3 Carey, R. G., Fitzpatrick, D. and Diamond, I. T., Layer I of striate cortex of Tupaiaglis and Galago senegalensis: projections from thalamus and claustrum revealed by retrograde transport of horseradish peroxidase, J. comp. Neurol., 186 (1979) 393-437. 4 Casagrande, V. A., The laminar organization and connections of the lateral geniculate nucleus in tree shrew (Tupaia glis), Anat. Rec., 178 (1974) 323. 5 Casagrande, V. A., Guillery, R. W. and Harting, J. K., Differential effects of monocular deprivation seen in different layers of the lateral geniculate nucleus, J. comp. Neurol., 179 (1978) 469-486. 6 Cleland, B. G., Levick, W. R., Morstyn, R. and Wager, H. G., Lateral geniculate relay of slowly conducting retinal afferents, J. Physiol. (Lond.), 255 (1976) 299-320. 7 Cowan, W. M., Gottlieb, D. 1., Hendrickson, A. E., Price, J. L. and Woolsey, T. A., The autoradiographic demonstration of axonal connections in the central nervous system, Brain Research, 37 (1972) 21-51. 8 Dreher, B. Y., Fukada, Y. and Rodieck, R. W., Identification, classification and anatomical segregation of cells with X-like properties and Y-like properties in the lateral geniculate nucleus of Old World primates, J. Physiol. (Lond.), 258 (1976) 433-452. 9 Ebhesson, S. O. E., A proposal for a common nomenclature for some optic nuclei in vertebrates and the evidence for a common origin of two such cell groups, Brain Behav. Evol., 6 (1972) 75-91. 10 Glendenning, K. K., Kofron, E. A. and Diamond, I. T., Laminar organization of projections of the lateral geniculate nucleus to the striate cortex in Galago, Brain Research, 105 (1976) 538-546. 11 Graham, J., An autoradiographic study of the efferent connections of the superior colliculus of the cat, J. comp. Neurol., 173 (1977) 629-654. 12 Guillery, R. W., The laminar distribution of retinal fibers in the dorsal lateral geniculate nucleus of the cat: a new interpretation, J. comp. NeuroL, 138 (1970) 339-368. 13 Guillery, R. W. and Oberdorfer, M. D., A study of fine and coarse retino-fugal axons terminating in the geniculate C laminae and in the medial interlaminar nucleus of the mink, J. comp. Neurol., 176 (1977) 515-526.
499 14 Hall, W. D. and Ebner, F. F., Parallels in the visual afferent projections of the thalamus in the hedgehog (Paraechinus hypomelas) and the turtle (Pseudemys scripta), Brain Behav. Evol., 3 (1970) 135-154. 15 Harting, J. K., Casagrande, V. A. and Weber, J. T., The projection of the primate superior colliculus upon the dorsal lateral geniculate nucleus: autoradiographic demonstration of interlaminar distribution of tectogeniculate axons, Brain Research, 150 (1978) 593-599. 16 Harting, J. K., Hall, W. C., Diamond, I. T. and Martin, G. F., Anterograde degeneration study of the superior colliculus in Tupaia glis: evidence for a subdivision between superficial and deep layers, J. comp. Neurol., 148 (1973) 361-386. 17 Hassler, R., Comparative anatomy of the central visual systems in day and night primates. In Hassler and Stephen (Eds.), Evolution of the Forebrain, Thieme, Stuttgart, 1966, pp. 419-434. 18 Kaas, J. H., Huerta, M. F., Weber, J. T. and Harting, J. K., Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus of primates, J. comp. Neurol., 182 (1978) 517-554. 19 Langer, T. P. and Colby, C. L., Subcortical projections to the dorsal lateral geniculate nucleus, Neurosci. Abstr., 5 (1979) 792. 20 LeVay, S. and Gilbert, C. D., Laminar patterns of geniculocortical projections in cat, Brain Research, 113 (1976) 1-19. 21 Leventhal, A. G., Evidence that different classes of relay cells of the cats lateral geniculate nucleus terminate in different layers of the striate cortex, Exp. Brain Res., 37 (1979) 349-372. 22 Niimi, K., Miki, M. and Kawamura, S., Ascending projections of the superior colliculus in the cat, Okajima Folia Anat. Jap., 47 (1970) 269-289. 23 Robson, J. A. and Hall, W. C., Projections from the superior colliculus to the dorsal lateral geniculate nucleus of the grey squirrel (Sciurus carolinensis), Brain Research, 113 (1976) 379-385. 24 Schiller, P. H. and Malpeli, J. G., Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey, J. Neurophysiol., 41 (1978) 788-797. 25 Sherman, S. M., Norton, I. T. and Casagrande, V. A., X- and Y-cells in the dorsal lateral geniculate nucleus of the tree shrew (Tupaia glis), Brain Research, 93 (1975) 152-157. 26 Sherman, S. M., Wilson, J. K., 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. 27 Tigges, M. and Tigges, J., The retinofugal fibers and their terminal nuclei in Galago crassicaudatus, (primates), J. comp. Neurol., 138 (1970) 87-102. 28 Wilson, P. D., Row, M. H. and Stone, J., Properties of relay cells in the cat's lateral geniculate nucleus: a comparison of W-cells and X- and Y-cells, J. Neurophysiol., 39 (1976) 1193-1209. 29 Wilson, P. D. and Stone, J., Evidence of W-cell input to the cat's visual cortex via the C laminae of the lateral geniculate nucleus, Brain Research, 92 (1975) 472-478.
Brain Research, 194 (1980) 494 499 ~, Elsevier/North-Holland Biomedical Press
The projection of the superior colliculus upon the lateral geniculate body in
Tupaia g/is and Go~ago senegalensis D. FITZPATRICK, R. G. CAREY* and I. T. DIAMOND Department of Psychology, Duke University, Durham, N.C. 27706 (U.S.A.) (Accepted March 20th, 1980) Key words: lateral geniculate body -- superior colliculus -- tecto-geniculate projection
In a previous study of the laminar organization of the lateral geniculate body (GL) in the tree shrew, Tupaia glis, and in Galago senegalensis, we restricted HRP to the superficial layers of the striate cortex and found that only certain layers of the lateral geniculate body contained labeled cells 3. We concluded that the small celled layers as well as certain interlaminar zones in both of these species project to the superficial layers of the striate cortex. The present report presents evidence that these same zones of the lateral geniculate body that project to the superficial layers of the striate cortex are further distinguished from the rest of the lateral geniculate body by receiving fibers from the superficial layers of the superior colliculus. A total of 2 tree shrews and 6 galagos were used in these experiments. Iontophoretic injections of a 1:1 tritiated proline-leucine mixture which had been reconstituted to 50-80 #Ci/tzl with 0.1 M acetate buffer at pH 4.8 were made into the superior colliculus of each animal. Following a survival period of 48 h, the animals were deeply anesthetized and perfused with 109~ buffered formalin. The brains were stored for several days in a 3090 sucrose-formalin solution, after which they were sectioned at 40 ktm on a freezing microtome and processed for autoradiography using standard proceduresL Exposure times for the autoradiographs ranged from 4-10 weeks. Following the injection of tritiated amino acids into the superficial layers of the superior colliculus in the tree shrew, labeled fibers can be seen leaving the injection site and passing ventrally and laterally to enter the brachium of the superior colliculus. These fibers course rostrally within the optic tract until they terminate in the lateral geniculate body. The distribution of terminals within the lateral geniculate body is illustrated in the series of coronal sections presented in Fig. la. In section 191 (the most caudal section) silver grains are visible over layer 6 just adjacent to the optic * Present address: Division of Neurobiology, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix, Ariz. 85013, U.S.A.
495 tract. In more rostral sections (195 and 199), silver grains appear in two bands; one occupying the interlaminar zone between layers 4 and 5, and the other lying within layer 3. Finally, a small patch o f silver grains can be seen just medial to layer 1 along the border o f the pulvinar nucleus. A p h o t o m i c r o g r a p h o f a portion o f section 199 is shown in Fig. 2a. Following injections o f tritiated amino acids into the superficial layers o f the superior colliculus in galago, labeled fibers can be traced rostrally within the brachium o f the superior colliculus and the optic tract to their terminations within the lateral geniculate body. Fig. lc and the p h o t o m i c r o g r a p h in Fig. 2b illustrate the distribution o f terminals within the lateral geniculate body. The greatest n u m b e r o f silver grains appear a r o u n d the cells o f layers 4 and 5. Patches o f labeled terminals are also present TUPAIA
GALAGO
1,1,
C. a.
d.
1605
1ram
Fig. 1. A: coronal sections through the lateral geniculate body of the tree shrew illustrating the distribution of labeled terminals following an injection of tritiated amino acids into the superior colliculus. Section 191 is the most caudal, while section 199 is the most rostral. The bracket and arrow in section 199 refer to the photomicrograph shown in Fig. 2a. b: coronal sections through the lateral geniculate body of the tree shrew illustrating the distribution of labeled cells following the application of HRP to the superficial layers of the striate cortex3. Section 148 is caudal to section 154. c" parasagittal sections through the lateral geniculate body of galago illustrating the distribution of labeled terminals following an injection of tritiated amino acids into the superior colliculus. Section 285 is medial to section 293. The arrow and bracket in section 285 refer to the photomicrograph in Fig. 2b. d: parasagittal secsections through the lateral geniculate body of galago illustrating the distribution of labeled cells following the application of HRP to the superficial layers of the striate cortex3. Section 116 is medial to section 114. TO, optic tract.
496
Fig. 2. a: dark-field light-field photomicrograph showing the distribution of autoradiographically labeled terminals in the lateral geniculate body of the tree shrew following all injection of tritiated amino acids into the superior colliculus. This photomicrograph corresponds to the bracketed region of section 199, Fig. la ( . 47). b: dark-field-light-field photomicrograph showing the distribution of autoradiographically labeled terminals in the lateral geniculate body of galago following an injection of tritiated amino acids into the superior colliculus. This photomicrograph corresponds to the bracketed region of section 285, Fig. lc. ( 5 2 ) . in the interlaminar zones between layers 1 and 2 and layers 2 and 3 as well as at the junction of layer 1 and the optic tract. The density of grains over layers 1, 2 and 3 is greater than the background level, but it seems reasonable to conclude that this label may be within fibers destined for layers 4 and 5 and the interlaminar zones. The presence of a pathway from the superficial layers of the superior colliculus to the lateral geniculate body is not a new finding. A tecto-geniculate projection has previously been reported in the squirrel, hedgehog, tree shrew, cat and monkey 2,4,1 ~, >1-16,z'~,~a and the cells of origin of this pathway within the superficial layers of the superior colliculus have also been shown 1,19,23. The significance of the present results lies in a comparison of the distribution of tecto-geniculate terminals with the distribution of labeled cells within the lateral geniculate body following the application of H R P to the superficial layers of the striate cortex (Fig. Ib andd): the cells that lie within the tecto-recipient zones of the lateral geniculate body in both species are the source of fibers projecting to the most superficial layers (presumably layer 1) of the striate cortex 3. The discovery that layers 4 and 5 of the lateral geniculate body of galago are distinguished by input from the superficial layers of the superior colliculus and project to layer I of striate cortex, contributes to our understanding of the laminar organization of the lateral geniculate body in this species. The lateral geniculate body of galago consists of 3 pairs of layers which differ in cell size and layer of termination within the striate cortexa,l°, 27. Layers 1 and 2 consist of large neurons which send their axons to the upper tier of layer IV; these layers appear to be homologous to the magnocellular layers of other primates10,17, is. Layers 3 and 6 consist of medium-sized
497 neurons which send their axons to the lower tier of layer IV of the striate cortex; these layers appear to be homologous to the parvocellular layers of other primates 1°,17,1s. In contrast to the other pairs, layers 4 and 5 which contain small pale staining cells have no obvious counterpart in the lateral geniculate body of simian primates. However, the so-called S layer and the interlaminar zones of the squirrel monkey lateral geniculate body receive fibers from the superficial layers of the superior colliculus 15, suggesting that they may have at least a functional similarity with layers 4 and 5 in galago. The significance of these homologies and similarities is that they allow us to speculate about the retinal input to the various layers of the lateral geniculate body in galago. The magnocellular layers of the lateral geniculate body of several primate species have been shown to receive input from the Y-cell class of retinal ganglion cell, while the parvocellular layers receive input from the X-cell class~, 26. (We use the terms 'X-cell' and 'Y-cell' for convenience and their use does not imply that the issues posed by such a classificatory scheme have been resolved for any species, let alone the galago). Thus, it is likely that layers 1 and 2 of galago are the target of large Y-cell axons while layers 3 and 6 are the target of smaller X-cell axons. We suspect that the retinal input to layers 4 and 5 in galago may be similar to that of the S layers and interlaminar zones of the monkey, both of which have been shown to receive re~_inal input TM, but as yet these layers have not been examined physiologically. However, a number of similarities between layers 4 and 5 in galago and the parvocellular C layers of the lateral geniculate body of the cat suggest that layers 4 and 5 probably receive fine caliber W-cell input. First, the C layers of the cat consist of small pale staining neurons. Second, these geniculate layers receive fibers from the superficial layers of the superior colliculus11,19, 22. Third, the parvocellular C layers project to layer I of the striate cortex. This projection to layer I of the striate cortex in the cat has been shown both by injections of tritiated amino acids into the C layer complex z0 and by experiments in which HRP was restricted to the most superficial layers of the cortex2L Finally, the retinal fibers projecting to the parvocellular C layers of the cat are noticeably finer in caliber than the fibers projecting to the A laminae lz,13. We have noted a similar distinction in the retinal input to layers 4 and 5 of galago. The similarities between the C layers of the cat and layers 4 and 5 of galago taken together suggest that these layers are homologous. Since the C layers in the cat are dominated by W-cell input2S, 29, it is reasonable to argue that layers 4 and 5 of galago also receive fibers from the W-class of retinal ganglion cells. It is not easy to determine which layers of the lateral genieulate body in tree shrew may be homologous to the magnocellular or parvocellular layers in primates ~,~8. Furthermore, while there is electrophysiological evidence for a parcellation of cell types analogous to the X-Y classification in other species, it is not clear whether these classes are segregated into different layers, nor is it certain that there is W-cell input to the lateral geniculate body 25. But, for our purposes, the chief point to emphasize is that the tecto-recipient zones in the tree shrew lateral geniculate body have numerous characteristics in common with the recto-recipient zones of galago and the cat including cell size, layer of termination in striate cortex and fine caliber retinal
498 input a,:'. These similarities suggest that the tecto-recipient zones in all 3 species are homologous. The discovery o f a t e c t o - g e n i c u l o - s t r i a t e cortex projection system in species as divergent as galago, tree shrew a n d cat suggests that this system is an integral part o f the basic plan o f the m a m m a l i a n visual thalamus. F u r t h e r , since this projection terminates in layer I o f the striate cortex, and since it a p p e a r s to be related to small caliber retinal input, we are t e m p t e d to speculate that the tecto-recipient zones o f the lateral geniculate b o d y m a y represent a persistent r e m a i n d e r o f an early stage in the p h y l o g e n y o f the visual t h a l a m u s ; a stage that preceded the d e v e l o p m e n t o f the larger fibered retino-geniculate p a t h w a y s (X- a n d Y-cell class) and the separate tectot h a l a m i c target within the pulvinar. Relying chiefly on the c o m p a r i s o n between m a m m a l s a n d lower vertebrates, Ebbesson '~ also p r o p o s e d that the pulvinar nucleus and lateral geniculate nucleus evolved from a single cellular zone that received both tectal a n d retinal input. This research was s u p p o r t e d by N I M H P r e d o c t o r a l F e l l o w s h i p 07262 to D.F., N I M H P o s t d o c t o r a l F e l l o w s h i p 05867 to R . G . C . a n d N I M H Research G r a n t 04849 to I.T.D. We w o u l d like to t h a n k Pamela M a d r e n a n d Susan Havrilesky for their help in p r e p a r i n g the manuscript. 1 Albano, J. E., Norton, T. T. and Hall, W. C., Laminar origin of projections from the superficial layers of the superior colliculus in the tree shrew, Tupaia glis, Brain Research, 173 (1979) 1-I I. 2 Benevento, L. A. and Fallon, J. H., The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta), J. comp. Neurol., 160 (1975) 339-362. 3 Carey, R. G., Fitzpatrick, D. and Diamond, I. T., Layer I of striate cortex of Tupaiaglis and Galago senegalensis: projections from thalamus and claustrum revealed by retrograde transport of horseradish peroxidase, J. comp. Neurol., 186 (1979) 393-437. 4 Casagrande, V. A., The laminar organization and connections of the lateral geniculate nucleus in tree shrew (Tupaia glis), Anat. Rec., 178 (1974) 323. 5 Casagrande, V. A., Guillery, R. W. and Harting, J. K., Differential effects of monocular deprivation seen in different layers of the lateral geniculate nucleus, J. comp. Neurol., 179 (1978) 469-486. 6 Cleland, B. G., Levick, W. R., Morstyn, R. and Wager, H. G., Lateral geniculate relay of slowly conducting retinal afferents, J. Physiol. (Lond.), 255 (1976) 299-320. 7 Cowan, W. M., Gottlieb, D. 1., Hendrickson, A. E., Price, J. L. and Woolsey, T. A., The autoradiographic demonstration of axonal connections in the central nervous system, Brain Research, 37 (1972) 21-51. 8 Dreher, B. Y., Fukada, Y. and Rodieck, R. W., Identification, classification and anatomical segregation of cells with X-like properties and Y-like properties in the lateral geniculate nucleus of Old World primates, J. Physiol. (Lond.), 258 (1976) 433-452. 9 Ebhesson, S. O. E., A proposal for a common nomenclature for some optic nuclei in vertebrates and the evidence for a common origin of two such cell groups, Brain Behav. Evol., 6 (1972) 75-91. 10 Glendenning, K. K., Kofron, E. A. and Diamond, I. T., Laminar organization of projections of the lateral geniculate nucleus to the striate cortex in Galago, Brain Research, 105 (1976) 538-546. 11 Graham, J., An autoradiographic study of the efferent connections of the superior colliculus of the cat, J. comp. Neurol., 173 (1977) 629-654. 12 Guillery, R. W., The laminar distribution of retinal fibers in the dorsal lateral geniculate nucleus of the cat: a new interpretation, J. comp. NeuroL, 138 (1970) 339-368. 13 Guillery, R. W. and Oberdorfer, M. D., A study of fine and coarse retino-fugal axons terminating in the geniculate C laminae and in the medial interlaminar nucleus of the mink, J. comp. Neurol., 176 (1977) 515-526.
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