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The morphology of collicular and retinal axons ending on small relay (W-like) cells of the primate lateral geniculate nucleus

  • E. A. Lachica (a1) and V. A. Casagrande (a1) (a2)

Abstract

The lateral geniculate nucleus (LGN) of every primate examined contains a set of small relay cells in addition to separate sets of magnocellular and parvocellular relay cells. These small cells receive a direct retinal projection, and an indirect retinal projection via the superior colliculus (SC). Receptive-field analyses of the small LGN cells in the bush baby, a lorisiform primate, indicate that this cell class is composed of subclasses, similar in physiology to cat W cells. In an effort to identify some of these subclasses, we have examined the morphological features of retinal and collicular axonal arbors that end on small W-like cells in the LGN of the bush baby, Galago crassicaudatus. Small cells in this species are found in a prominent pair of koniocellular (K) layers as well as the interlaminar zones (ILZs).

Retinal arbors were examined by bulk iontophoretic injection of horseradish peroxidase into the optic tract. Collicular arbors were filled via iontophoretic injection of biocytin into the superficial layers of the SC. Forty-eight axon arbors were completely reconstructed and quantitatively evaluated. Our findings show that retinal and collicular axon terminals differ in morphology on the basis of a number of criteria. Our analyses also suggest that retinal axons may have a stronger influence on K cells and collicular axons have a stronger influence on ILZ cells. The ramifications of these findings are provocative since these small LGN cells are known to project directly to the cytochrome-oxidase (CO) blobs within striate cortex. This relationship suggests that CO blob cells receive complex visual input not only from magnocellular and parvocellular LGN cells, but also from small cell pathways that are differentially influenced by retinal and collicular cells.

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Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 6, 775.
Berson, D.M. (1987). Retinal W-cell input to the upper superficial gray layer of the cat’s superior colliculus: A conduction-velocity analysis. Journal of Neurophysiology 58, 10351051.
Berson, D.M. (1988 a). Convergence of retinal W-cell and corticotectal input to cells of the cat superior colliculus. Journal of Neurophysiology 60, 18611873.
Berson, D.M. (1988 b). Retinal and cortical inputs to cat superior colliculus: Composition, convergence, and laminar specificity. In Progress in Brain Research, Vol. 75, ed. Hicks, T.P. & Benedek, G., pp. 1726. Amsterdam, New York: Elsevier.
Berson, D.M., Lu, J. & Stein, J.J. (1990). Topographic variations in W-cell input to cat superior colliculus. Experimental Brain Research 79, 459466.
Berson, D.M. & McIlwain, J.T. (1982). Retinal Y-cell activation of deep-layer cells in the superior colliculus of the cat. Journal of Neurophysiology 47, 700714.
Blasdel, G.G. & Lund, J.S. (1983). Termination of afferent axons in macaque striate cortex. Journal of Neuroscience 3, 13891413.
Carey, R.G., Fitzpatrick, D. & Diamond, I.T. (1979). Layer 1 of striate cortex of Tupaia glis and Galago senegalensis: Projections from thalamus and claustrum revealed by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 186, 393438.
Casagrande, V.A., Beck, P.D. & Lachica, E.A. (1989). Intrinsic connections of cytochrome oxidase (CO) blob and nonblob regions in area 17 of a nocturnal primate. Society for Neuroscience Abstracts 15, 1398.
Casagrande, V.A. & DeBruyn, E.J. (1982). The Galago visual system: Aspect of normal organization and developmental plasticity. In The Lesser Bush Baby (Galago) as an Animal Model: Selected Topics, ed. Haines, D.E., pp. 137167. Florida: CRC Press.
Casagrande, V.A., Harting, J.K., Hall, W.C. & Diamond, I.T. (1972). Superior colliculus of the tree shrew: A structural and functional subdivision into superficial and deep layers. Science 177, 444447.
Casagrande, V.A. & Norton, T.T. (1991). Lateral geniculate nucleus: A review of its physiology and function. In The Neural Basis of Visual Function, Vol. 4 of Vision and Visual Dysfunction, ed. Leventhal, A., pp. 4184. London: McMillian Press, Ltd.
Condo, G.J. & Casagrande, V.A. (1990). Organization of cytochrome oxidase staining in the visual cortex of nocturnal primates (Galago crassicaudatus and Galago senegalensis). I. Adult patterns. Journal of Comparative Neurology 293, 632645.
Conley, M. (1988). Laminar organization of geniculostriate projections. A common organizational plan based on layers rather than individual functional classes. Brain, Behavior, and Evolution 32, 187192.
Conley, M., Penny, G.R. & Diamond, I.T. (1987). Terminations of individual optic tract fibers in the lateral geniculate nuclei of Galago crassicaudatus and Tupaia belangeri. Journal of Comparative Neurology 256, 7187.
Conway, J.L. & Schiller, P.H. (1983). Laminar organization of the tree shrew lateral geniculate nucleus. Journal of Neurophysiology 50, 13301342.
Cusick, C.G. & Kaas, J.H. (1986). Interhemispheric connections of cortical connections of visual cortex of owl monkeys (Aotus trivir-gatus), marmosets (Callithrix jacchus), and galagos (Galago crassicaudatus). Journal of Comparative Neurology 230, 311336.
Cynader, M. & Berman, N. (1972). Receptive-field organization of monkey superior colliculus. Journal of Neurophysiology 35, 187201.
DeBruyn, E.J., Casagrande, V.A., Beck, P.D. & Bonds, A.B. (1993). Visual resolution and sensitivity of single cells in the primary visual cortex (VI) of a nocturnal primate (bush baby): Correlations with cortical layers and cytochrome-oxidase patterns. Journal of Neurophysiology 69 (in press).
Diamond, I.T., Conley, M., Fitzpatrick, D. & Raczkowski, D. (1991). Evidence for separate pathways within the tecto-geniculate projection in the tree shrew. Proceedings of the National Academy of Sciences (USA) 88, 13151319.
Diamond, I.T., Conley, M., Itoh, K. & Fitzpatrick, D. (1985). Laminar organization of geniculocortical projections in Galago senegalensis and Aotus trivirgatus. Journal of Comparative Neurology 242, 564610.
Fitzpatrick, D., Carey, R.G. & Diamond, I.T. (1980). The projection of the superior colliculus upon the lateral geniculate body in Tupaia glis and Galago senegalensis. Brain Research 194, 494499.
Fitzpatrick, D. & Raczkowski, D. (1990). Innervation patterns of single physiologically identified geniculocortical axons in the striate cortex of the tree shrew. National Academy of Science (Proceedings) 87, 449453.
Fitzpatrick, D., Itoh, K. & Diamond, I.T. (1983). The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). Journal of Neuroscience 3, 673702.
Florence, S.L. & Casagrande, V.A. (1987). Organization of individual afferent axons in layer IV of striate cortex in a primate. Journal of Neuroscience 7, 38503868.
Giolli, R.A. & Tigges, J. (1970). The primary optic pathways and nuclei of primates. In The Primate Brain, ed. Noback, C.R. & Montagno, W., pp. 2954. New York: Appleton, Century Crofts.
Graham, J. & Casagrande, V.A. (1980). A light microscopic and electron microscopic study of the superficial layers of the superior colliculus of the tree shrew (Tupaia glis). Journal of Comparative Neurology 191, 133151.
Harting, J.K., Huerta, M.F., Hashikawa, T. & Van Lieshout, D.P. (1991). Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: Organization of tectogeniculate pathways in nineteen species. Journal of Comparative Neurology 304, 275306.
Hendrickson, A., Wilson, J.R. & Ogren, M.P. (1978). The neuro-anatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World primates. Journal of Comparative Neurology 182, 123136.
Holdefer, R.N. & Norton, T.T. (1986). Laminar organization of receptive-filed properties in the lateral geniculate nucleus of the tree shrew (Tupaia belangeri). Society for Neuroscience Abstracts 12, 8.
Hubel, D.H. (1975). An autoradiographic study of the retino-cortical projections in the tree shrew (Tupaia glis). Brain Research 96, 4150.
Huerta, M.F. & Harting, J.K (1984). The mammalian superior colliculus: Studies of its morphology and connections. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 687773. New York: Plenum.
Irvin, G.E., Norton, T.T., Sesma, M.A. & Casagrande, V.A. (1986). W-like response properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Research 362, 254270.
Itoh, K., Conley, M. & Diamond, I.T. (1982). Retinal ganglion cell projections to individual layers of the lateral geniculate body in Galago crassicaudatus. Journal of Comparative Neurology 205, 282290.
Kaas, J.H., Huerta, M.F., Weber, J.J. & Harting, J.K. (1978). Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus of primates. Journal of Comparative Neurology 182, 517554.
Kawamura, S., Fukushima, N., Hattori, S. & Kudo, M. (1980). Laminar segregation of cells of origin of ascending projections from the superficial layers of the superior colliculus in the cat. Brain Research 184, 486490.
Kretz, R., Rager, G. & Norton, T.T. (1986). Laminar organization of ON and OFF regions and ocular dominance in the striate cortex of the tree shrew (Tupaia belangeri). Journal of Comparative Neurology 251, 135145.
Lachica, E.A., Hutchins, J.B. & Casagrande, V.A. (1987). Morphology of corticogeniculate axon arbors in a primate. Society for Neuroscience Abstracts 13, 1434.
Lachica, E.A. & Casagrande, V.A. (1988). Development of primate retinogeniculate axon arbors. Visual Neuroscience 1, 103123.
Lachica, E.A. & Casagrande, V.A. (1990). Methods for visualizing and analyzing individual axon arbors. In Methods in Neuroscience, Vol. 13, ed. Conn, M., pp. 230244. Orlando, Florida: Academic Press.
Lachica, E.A., Crooks, M.W. & Casagrande, V.A. (1990). The effects of monocular deprivation on the morphology of retinogeniculate axon arbors in a primate. Journal of Comparative Neurology 296, 303323.
Lachica, E.A., Mavity-Hudson, J.A. & Casagrande, V.A. (1991). Morphological details of primate axons and dendrites revealed by extracellular injection of biocytin: An economic and reliable alternative to PHA-L. Brain Research 564, 111.
Lachica, E.A. & Casagrande, V.A. (1992). Direct W-like geniculate projections to the cytochrome oxidase (CO) blobs in primate visual cortex: Axon morphology. Journal of Comparative Neurology 319, 141158.
Lachica, E.A., Beck, P.D. & Casagrande, V.A. (1992). Parallel pathways in macaque monkey striate cortex: Anatomically defined columns in layer III. Proceedings of the National Academy of Science (USA) 89, 35663570.
Lachica, E.A., Beck, P.D. & Casagrande, V.A. (1993). Intrinsic connections of layer III of striate cortex in squirrel monkeys and bush babies: Correlations with patterns of cytochrome oxidase. Journal of Comparative Neurology (submitted).
Leventhal, A.G., rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in Old-World monkey: Morphology and central projections. Science 213, 11391142.
Livingstone, M.S. & Hubel, D.H. (1982). Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. National Academy of Science (Proceedings) 79, 60986101.
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309356.
Livingstone, M.S. & Hubel, D.H. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 240, 740749.
McConnel, S.K. & LeVay, S. (1986). Anatomical organization of the visual system of the mink, Mustela vision. Journal of Comparative Neurology 250, 109132.
Newsome, W.T. & Allman, J.M. (1980). Interhemispheric connections of visual cortex in the owl monkey, Aotus trivirgatus, and the bush baby, Galago senegalensis. Journal of Comparative Neurology 194, 209233.
Norton, T.T. & Casagrande, V.A. (1982). Laminar organization of receptive-field properties in the lateral geniculate nucleus of bush baby (Galago crassicaudalus). Journal of Neurophysiology 47, 715741.
Norton, T.T., Casagrande, V.A., Irvin, G.E., Sasma, M.A. & Petry, H.M. (1988). Contrast sensitivity functions of W-, X-, Y-like relay cells in lateral geniculate nucleus of bush baby (Galago crassicaudatus). Journal of Neurophysiology 59, 16391656.
Perry, V.H. & Cowey, A. (1984). Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience 12, 11251137.
Raczkowski, D. & Diamond, I.T. (1978). Cells of origin of several efferent pathways from the superior colliculus in Galago senegalen-sis. Brain Research 146, 351357.
Raczkowski, D. & Diamond, I.T. (1981). Projections from the superior colliculus and the neocortex to the pulvinar nucleus in Galago. Journal of Comparative Neurology 200, 231254.
Rockland, K.S. & Pandya, D.N. (1979). Laminar origins and terminations of cortical connections of the occipital lobe in rhesus monkey. Brain Research 179, 320.
Saini, K., Kretz, R. & Rager, R. (1987). Classes of neurons in relation to the laminar organization of the lateral geniculate nucleus in the tree shrew, Tupaia belangeri. Journal of Comparative Neurology 259, 3149.
Schiller, P.H. & Koerner, F. (1971). Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. Journal of Neurophysiology 34, 920936.
Stanford, L.R. (1987). W-cells in the cat retina: Correlated morphological and physiological evidence for two distinct classes. Journal of Neurophysiology 57, 218244.
Stryker, M.P. & Zahs, K.R. (1983). ON and OFF sublaminae in the lateral geniculate nucleus of the ferret. Journal of Neuroscience 3, 19431951.
Sur, M. & Sherman, S.M. (1982). Retinogeniculate terminations in cat: Morphological differences between X- and Y-cell axons. Science 218, 389391.
Symonds, L.L. & Kaas, J.H. (1978). Connections of striate cortex in the prosimian Galago senegalensis. Journal of Comparative Neurology 181, 466512.
Weber, J.T., Huerta, M.F., Kaas, J.H. & Harting, J.K. (1983). The projections of the lateral geniculate nucleus of the squirrel monkey: Studies of the interlaminar zones and the S layers. Journal of Comparative Neurology 213, 135145.
Weller, R.E. & Kaas, J.H. (1982). The organization of the visual system in Galago: Comparisons with monkeys. In The Lesser Bush Baby (Galago) as an Animal Model: Selected Topics, ed. Haines, D.E., pp. 108135. Florida: CRC Press.
Wilson, P.D., Rowe, M.H. & Stone, J. (1976). Properties of relay cells in cat’s lateral geniculate nucleus: A comparison of W cells with X and Y cells. Journal of Neurophysiology 39, 11931209.
Zahs, K.R. & Stryker, M.P. (1988). Segregation of ON and OFF afferents to ferret visual cortex. Journal of Neurophysiology 59, 14101429.

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The morphology of collicular and retinal axons ending on small relay (W-like) cells of the primate lateral geniculate nucleus

  • E. A. Lachica (a1) and V. A. Casagrande (a1) (a2)

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