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Orientation bias of neurons in the lateral geniculate nucleus of macaque monkeys

  • Earl L. Smith (a1), Yuzo M. Chino (a1), William H. Ridder (a1), Kosuke Kitagawa (a1) and Andy Langston (a1)...

Abstract

The purpose of this investigation was to analyze the influence of stimulus orientation on the responses of individual neurons in the monkey's lateral geniculate nucleus (LGN). Our specific goals were to assess the prevalence and the degree of orientation tuning in the monkey LGN and to determine if the preferred stimulus orientations of LGN neurons varied as a function of receptive-field position. The primary motivation for this research was to gain insight into the receptive-field configuration of LGN neurons and consequently into the neural mechanisms which determine the spatial organization of LGN receptive fields in primates.

In both the parvocellular and magnocellular layers, the responses of the majority of individual neurons to sine-wave gratings varied as a function of stimulus orientation. The influence of stimulus orientation was, however, highly dependent on the spatial characteristics of the stimulus; the greatest degree of orientation bias was observed for spatial frequencies higher than the cell's optimal spatial frequency. On a population basis, the degree of orientation bias was similar for all major classes of LGN neurons (e.g. ON vs. OFF center; parvocellular vs. magnocellular) and did not vary systematically with receptive-field eccentricity. At a given receptive-field location, LGN neurons, particularly cells in the parvocellular laminae, tended to prefer either radially oriented stimuli or stimuli oriented more horizontally than their polar axis. Our analyses of the orientation-dependent changes in spatial-frequency response functions, which was based on the Soodak et al., (1987; Soodak, 1986) two-dimensional, difference-of-Gaussian receptive-field model, suggested that the orientation bias in LGN neurons was due to an elongation of the receptive-field center mechanism which in some cases appeared to consist of multiple subunits. Direct comparisons of the orientation-tuning characteristics of LGN cells and their retinal inputs (S potentials) indicated that the orientation bias in the monkey LGN reflects primarily the functional properties of individual retinal ganglion cells. We conclude that orientation sensitivity is a significant property of subcortical neurons in the primate's geniculo-cortical pathway.

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Batschelet, E. (1981). Circular Statistics in Biology. New York: Academic Press.
Bauer, R. & Dow, B.M. (1989). Complementary global maps for orientation coding in upper and lower layers of the monkey's foveal striate cortex. Experimental Brain Research 76, 503509.
Bennett, A.G. & Francis, J.L. (1962). Visual Optics. In The Eye, Vol. 4, ed. Davson, H., pp. 2526. New York: Academic Press.
Bishop, P.O., Burke, W. & Davis, R. (1958). Synapse discharge by single fibers in mammalian visual system. Nature 182, 728730.
Bishop, P.O., Burke, W. & Davis, R. (1962). The interpretation of the extracellular response of single lateral geniculate cells. Journal of Physiology (London) 162, 451472.
Blasdel, G.G. & Fitzpatrick, D. (1984). Physiological organization of layer 4 in macaque striate cortex. Journal of Neuroscience 4, 880895.
Blasdel, G.G. & Lund, J.S. (1983). Termination of afferent axons in macaque striate cortex. Journal of Neuroscience 3, 13891413.
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: light microscopy. Philosophical Transactions of the Royal Society B (London) 225, 109184.
Boycott, B.B. & Wassle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology (London) 240, 397419.
Caceci, M. & Cacheris, W.P. (1984). Fitting curves to data. Byte 9, 340362.
Cleland, B.G., Dubin, M.W. & Levick, W.R. (1971). Sustained and transient neurones in the cat's retina and lateral geniculate nucleus. Journal of Physiology (London) 217, 473496.
Connolly, M. & Van Essen, D. (1984). The representation of the visual field in parvocellular and magnocellular layers of the lateral geniculate nucleus in the macaque monkey. Journal of Comparative Neurology 226, 544564.
De Monasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. Journal of Physiology (London) 251, 167195.
Derrington, A.M. & Lennie, P. (1984). Spatial- and temporal-contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology (London) 357, 219240.
DeValois, R.L., Alberecht, D.G. & Thorell, L. (1982). Spatial-frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545560.
Eldridge, J.L. (1979). A reversible ophthalmoscope using a corner-cubeprism. Journal of Physiology (London) 295, 12.
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells in the cat. Journal of Physiology (London) 187, 517552.
Geisert, E.E. Jr. (1980). Cortical projections of the lateral geniculate nucleus in the cat. Journal of Comparative Neurology 190, 793812.
Gizzi, M.S., Katz, E., Schumer, R.A. & Movshon, J.A. (1990). Selectivity for orientation and direction of motion in single neurons in cat striate and extrastriate visual cortex. Journal of Neuroscience 63, 15291543.
Gouras, P. (1974). Opponent-color cells in different layers of foveal striate cortex. Journal of Physiology (London) 238, 583602.
Hammond, P. (1974). Cat retinal ganglion cells: size and shape of receptive-field centers. Journal of Physiology (London) 242, 99118.
Hawken, M.J. & Parker, A.J. (1984). Contrast sensitivity and orientation selectivity in lamina IV of the striate cortex of Old World monkeys. Experimental Brain Research 54, 376–372.
Hendrickson, A.E., Wilson, J.R. & Ogren, M.P. (1978). The neuroanatomical organizations of pathways between dorsal lateral geniculate nucleus and visual cortex in Old and New World primates. Journal of Comparative Neurology 182, 123136.
Henry, G.H., Bishop, P.O., Tupper, R.M. & Dreher, B. (1973). Orientation specificity and response variability of cells in the striate cortex. Vision Research 13, 17711779.
Hochstein, S. & Shapley, R.M. (1976). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. Journal of Physiology (London) 262, 265284.
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology (London) 195, 215243.
Hubel, D.H. & Wiesel, T.N. (1972). Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. Journal of Comparative Neurology 146, 421450.
Kaplan, E. & Shapley, R.M. (1984 a). X and Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology (London) 330, 125143.
Kaplan, E. & Shapley, R.M. (1984 b). The origin of the S (slow) potential in the mammalian lateral geniculate nucleus. Experimental Brain Research 55, 111116.
Kaplan, E. & Shapley, R.M. (1986). The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proceedings of the National Academy of Science of the U.S.A 83, 27552757.
Kaplan, E., Purpura, K. & Shapley, R.M. (1987). Contrast affects the transmission of visual information through the mammalian lateral geniculate nucleus. Journal of Physiology (London) 391, 267288.
Kaplan, E., Shapley, R.M. & Purpura, K. (1988). Color and luminance contrasts as tools for probing the organization of the primate retina. Proceedings of the 10th Taniguchi Symposium, Neuroscience Research (Suppl.) 2, s151s166.
Kaplan, E., Shapley, R.M. & Purpura, K. (1989). Spatial and spectral mechanisms of primate retinal ganglion cells. In: Seeing Contour and Color, ed. Kulikowski, J. (in press).
Kaplan, E., Lee, B.B. & Shapley, R.M. (1990). New views of primate retinal function. Progress in Retinal Research, New York: Pergamon Press (in press).
Kolb, H., Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: light microscopy (Appendix). A second type of midget bipolar cell in the primate retina. Philosophical Transactions of the Royal Society B (London) 255, 177184.
Kolb, H. & DeKorver, L. (1988). Synaptic input to midget ganglion cells of the human retina. Investigative Ophthalmology and Visual Science (Suppl.) 29, 326.
Lee, B.B., Creutzfeldt, O.D. & Elepfandt, A. (1979). The responses of magnocellular and parvocellular cells of the monkey's lateral geniculate body to moving stimuli. Experimental Brain Research 35, 547557.
Lee, B.B., Virsu, V. & Creutzfeldt, O.D.. (1983). Linear signal transmission from prepotentials to cells in the macaque lateral geniculate nucleus. Experimental Brain Research 52, 5056.
LeVay, S. & Ferster, D. (1979). Proportion of the interneurones in the cat' lateral geniculate nucleus. Brain Research 164, 304308.
Leventhal, A.G. (1983). Relationship between preferred orientation and receptive-field position of neurons in cat striate cortex. Journal of Comparative Neurology 220, 476483.
Leventhal, A.G. & Schall, J.D. (1983). Structural basis of orientation sensitivity of cat retinal ganglion cells. Journal of Comparative Neurology 220, 465475.
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in Old World monkey: morphology and central projections. Science 213, 11391142.
Leventhal, A.G., Zhou, Y., Ault, S.J. & Thompson, K.G. (1989). Cortical contribution to the orientation sensitivity of relay cells in the cat lateral geniculate nucleus (LGND). Society for Neuroscience Abstracts 15, 176.
Levick, W.R. & Thibos, L.N. (1980). Orientation bias of cat retinal ganglion cells. Nature 286, 389390.
Levick, W.R. & Thibos, L.N. (1982). Analysis of orientation bias in cat retina. Journal of Physiology (London) 329, 243261.
Lin, C.-S. & Kaas, J.H. (1977). Projections from cortical visual areas 17, 18, and MT onto the dorsal lateral geniculate nucleus in owl monkeys. Journal of Comparative Neurology 173, 457474.
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309356.
Malpeli, J.G. & Baker, F.H. (1975). The representation of the visual field in the lateral geniculate nucleus of Macaca mulatta. Journal of Comparative Neurology 161, 569594.
Mardia, K.V. (1972). Statistics of Direction Data. New York: Academic Press.
McIlwain, J.T. & Creutzfeldt, O.D. (1967). Microelectrode study of excitation and inhibition in the lateral geniculate nucleus of the cat. Journal of Neurophysiology 30, 122.
Michael, C.R. (1978). Color-vision mechanisms in monkey striate cortex: dual-opponent cells with concentric receptive fields. Journal of Neurophysiology 41, 572588.
Movshon, J.A., Thompson, I.D. & Tolhurat, D.J. (1978). Spatial summation in the receptive fields of simple cells in the cat's striate cortex. Journal of Physiology (London) 283, 5377.
Perry, V.H., Oehler, R. & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 11011123.
Polyak, S.L. (1941). The Retina. Chicago; Illinois: The University of Chicago Press.
Rodieck, R.W. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research 5, 583601.
Rodieck, R.W., Binmoeller, K.F. & Dineen, J. (1985). Parasol and midget ganglion cells of the human retina. Journal of Comparative Neurology 233, 115132.
Rovamo, J., Virsu, V. & Hyvarinen, L. (1982). Resolution of gratings oriented along and across meridians in peripheral vision. Investigative Ophthalmology and Visual Science 23, 666670.
Schall, J.D., Perry, V.H. & Leventhal, A.G. (1986). Retinal ganglion cell dendritic fields in Old World monkeys are oriented radially. Brain Research 368, 1823.
Schein, S.J. (1988). Anatomy of macaque fovea and spatial densities of neurons in foveal representation. Journal of Comparative Neurology 269, 479505.
Schein, S.J. & De Monasterio, F.M. (1987). Mapping of retinal and geniculate neurons onto striate cortex of macaque. Journal of Neuroscience 7, 9961009.
Shou, T. & Leventhal, A.G. (1989). Organized arrangement of orientation-sensitive relay cells in the cat's dorsal lateral geniculate nucleus. Journal of Neuroscience 9, 42874302.
Shou, T., Ruan, D. & Zhou, Y. (1986). The orientation bias of LGN neurons shows topographic relation to area centralis in the cat retina. Experimental Brain Research 64, 233236.
Smith, E.L. III, Chino, Y.M., Ridder, W.R. III, Langston, A. & Kitagawa, K. (1989 a). Orientation bias of neurons in the lateral geniculate nucleus of macaque monkeys. Society for Neuroscience Abstracts 15, 176.
Smith, E.L. III, Harwerth, R.S., Ridder, W.R. III, Chino, Y.M., Crawford, M.L.J. & DeSantis, L. (1989 b). Neurophysiological alterations produced by experimental glaucoma in monkeys. Investigative Ophthalmology and Visual Science (Suppl.) 30, 55.
So, T.T. & Shaoley, R.M. (1981). Spatial tuning of cells in and around lateral geniculate nucleus of the cat: X and Y relay cells and perigeniculate interneurons. Journal of Neurophysiology 45, 107120.
Soodak, R.E. (1986). Two-dimensional modeling of visual receptive fields using Gaussian subunits. Proceedings of the National Academy of Science of the U.S.A. 83, 92599263.
Soodak, R.E., Shapley, R.M. & Kaplan, E. (1985). Unusual orientation tuning in the LGN and perigeniculate nucleus of the cat. Investigative Ophthalmology and Visual Science (Suppl.) 26, 264.
Soodak, R.E., Shapley, R.M. & Kaplan, E. (1987). Linear mechanism of orientation tuning in the retina and lateral geniculate nucleus of the cat. Journal of Neurophysiology 58, 267275.
Spatz, W.B., Tigges, J. & Tigges, M. (1970). Subcortical projections cortical associations and some intrinsic interlaminar connections of the striate cortex in the squirrel monkey (Saimiri). Journal of Comparative Neurology 140, 155174.
Thibos, L.N. & Levick, W.R. (1983). Bimodal receptive fields of cat retinal ganglion cells. Vision Research 23, 15611572.
Thibos, L.N. & Levick, W.R. (1985). Orientation bias of brisk-transient Y cells of the cat retina for drifting and alternating gratings. Experimental Brain Research 58, 110.
Vidyasagar, T.R. (1984). Contribution of inhibitory mechanisms to the orientation sensitivity of cat dLGN neurons. Experimental Brain Research 55, 192195.
Vidyasagar, T.R. & Heide, W. (1984). Geniculate orientation biases seen with moving sine-wave gratings: implications for a model of simple cell afferent connectivity. Experimental Brain Research 57, 196200.
Vidyasagar, T.R. & Urbas, J.V. (1982). Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18. Experimental Brain Research 46, 157169.
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. Journal of Comparative Neurology 289, 434454.
Weber, A.J. & Kalil, R.E. (1983). The percentage of interneurones in the dorsal lateral geniculate nucleus of the cat and observations of several variables that affect the sensitivity of horseradish peroxidase as a retrograde marker. Journal of Comparative Neurology 220, 336346.
Wilson, J.R. (1989). Synaptic organization of individual neurons in the macaque lateral geniculate nucleus. Journal of Neuroscience 9, 29312953.
Wilson, J.R., Friedlander, M.J. & Sherman, S.M. (1984). Fine structural morphology of identified X and Y cells in the cat's lateral geniculate nucleus. Proceedings of the Royal Society B (London) 221, 411436.
Wong-Riley, M.T.T. (1979). Columnar cortico-cortical interconnections within the visual system of the squirrel and macaque monkeys. Brain Research 162, 201217.
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