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

Published online by Cambridge University Press:  02 June 2009

Earl L. Smith III ,
Yuzo M. Chino ,
William H. Ridder III ,
Kosuke Kitagawa  and
Andy Langston
Earl L. Smith III
Affiliation:
College of Optometry, University of Houston, Houston
Yuzo M. Chino
Affiliation:
College of Optometry, University of Houston, Houston
William H. Ridder III
Affiliation:
College of Optometry, University of Houston, Houston
Kosuke Kitagawa
Affiliation:
College of Optometry, University of Houston, Houston
Andy Langston
Affiliation:
College of Optometry, University of Houston, Houston
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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.

Keywords

Orientation selectivityThalamusPrimateReceptive-fieldellipticityS potential
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 6 , December 1990 , pp. 525 - 545
Copyright
Copyright © Cambridge University Press 1990

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References

Batschelet, E. (1981). Circular Statistics in Biology. New York: Academic Press.Google Scholar
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, 503–509.CrossRefGoogle ScholarPubMed
Bennett, A.G. & Francis, J.L. (1962). Visual Optics. In The Eye, Vol. 4, ed. Davson, H., pp. 25–26. New York: Academic Press.Google Scholar
Bishop, P.O., Burke, W. & Davis, R. (1958). Synapse discharge by single fibers in mammalian visual system. Nature 182, 728–730.CrossRefGoogle ScholarPubMed
Bishop, P.O., Burke, W. & Davis, R. (1962). The interpretation of the extracellular response of single lateral geniculate cells. Journal of Physiology (London) 162, 451–472.CrossRefGoogle ScholarPubMed
Blasdel, G.G. & Fitzpatrick, D. (1984). Physiological organization of layer 4 in macaque striate cortex. Journal of Neuroscience 4, 880–895.CrossRefGoogle ScholarPubMed
Blasdel, G.G. & Lund, J.S. (1983). Termination of afferent axons in macaque striate cortex. Journal of Neuroscience 3, 1389–1413.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: light microscopy. Philosophical Transactions of the Royal Society B (London) 225, 109–184.Google Scholar
Boycott, B.B. & Wassle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology (London) 240, 397–419.CrossRefGoogle ScholarPubMed
Caceci, M. & Cacheris, W.P. (1984). Fitting curves to data. Byte 9, 340–362.Google Scholar
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, 473–496.CrossRefGoogle ScholarPubMed
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, 544–564.CrossRefGoogle Scholar
De Monasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. Journal of Physiology (London) 251, 167–195.CrossRefGoogle ScholarPubMed
Derrington, A.M. & Lennie, P. (1984). Spatial- and temporal-contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology (London) 357, 219–240.CrossRefGoogle ScholarPubMed
DeValois, R.L., Alberecht, D.G. & Thorell, L. (1982). Spatial-frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545–560.CrossRefGoogle Scholar
Eldridge, J.L. (1979). A reversible ophthalmoscope using a corner-cubeprism. Journal of Physiology (London) 295, 1–2.Google Scholar
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells in the cat. Journal of Physiology (London) 187, 517–552.CrossRefGoogle ScholarPubMed
Geisert, E.E. Jr. (1980). Cortical projections of the lateral geniculate nucleus in the cat. Journal of Comparative Neurology 190, 793–812.CrossRefGoogle ScholarPubMed
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, 1529–1543.Google ScholarPubMed
Gouras, P. (1974). Opponent-color cells in different layers of foveal striate cortex. Journal of Physiology (London) 238, 583–602.CrossRefGoogle Scholar
Hammond, P. (1974). Cat retinal ganglion cells: size and shape of receptive-field centers. Journal of Physiology (London) 242, 99–118.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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, 123–136.CrossRefGoogle ScholarPubMed
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, 1771–1779.CrossRefGoogle ScholarPubMed
Hochstein, S. & Shapley, R.M. (1976). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. Journal of Physiology (London) 262, 265–284.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology (London) 195, 215–243.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1972). Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. Journal of Comparative Neurology 146, 421–450.CrossRefGoogle ScholarPubMed
Kaplan, E. & Shapley, R.M. (1984 a). X and Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology (London) 330, 125–143.CrossRefGoogle Scholar
Kaplan, E. & Shapley, R.M. (1984 b). The origin of the S (slow) potential in the mammalian lateral geniculate nucleus. Experimental Brain Research 55, 111–116.CrossRefGoogle Scholar
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, 2755–2757.CrossRefGoogle ScholarPubMed
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, 267–288.CrossRefGoogle ScholarPubMed
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, s151–s166.Google Scholar
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).Google Scholar
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).Google Scholar
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, 177–184.Google Scholar
Kolb, H. & DeKorver, L. (1988). Synaptic input to midget ganglion cells of the human retina. Investigative Ophthalmology and Visual Science (Suppl.) 29, 326.Google Scholar
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, 547–557.CrossRefGoogle ScholarPubMed
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, 50–56.CrossRefGoogle ScholarPubMed
LeVay, S. & Ferster, D. (1979). Proportion of the interneurones in the cat' lateral geniculate nucleus. Brain Research 164, 304–308.CrossRefGoogle Scholar
Leventhal, A.G. (1983). Relationship between preferred orientation and receptive-field position of neurons in cat striate cortex. Journal of Comparative Neurology 220, 476–483.CrossRefGoogle ScholarPubMed
Leventhal, A.G. & Schall, J.D. (1983). Structural basis of orientation sensitivity of cat retinal ganglion cells. Journal of Comparative Neurology 220, 465–475.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in Old World monkey: morphology and central projections. Science 213, 1139–1142.CrossRefGoogle ScholarPubMed
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.Google Scholar
Levick, W.R. & Thibos, L.N. (1980). Orientation bias of cat retinal ganglion cells. Nature 286, 389–390.CrossRefGoogle ScholarPubMed
Levick, W.R. & Thibos, L.N. (1982). Analysis of orientation bias in cat retina. Journal of Physiology (London) 329, 243–261.CrossRefGoogle ScholarPubMed
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, 457–474.CrossRefGoogle Scholar
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.CrossRefGoogle ScholarPubMed
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, 569–594.CrossRefGoogle ScholarPubMed
Mardia, K.V. (1972). Statistics of Direction Data. New York: Academic Press.Google Scholar
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, 1–22.CrossRefGoogle Scholar
Michael, C.R. (1978). Color-vision mechanisms in monkey striate cortex: dual-opponent cells with concentric receptive fields. Journal of Neurophysiology 41, 572–588.CrossRefGoogle ScholarPubMed
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, 53–77.CrossRefGoogle ScholarPubMed
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, 1101–1123.CrossRefGoogle Scholar
Polyak, S.L. (1941). The Retina. Chicago; Illinois: The University of Chicago Press.Google Scholar
Rodieck, R.W. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research 5, 583–601.CrossRefGoogle ScholarPubMed
Rodieck, R.W., Binmoeller, K.F. & Dineen, J. (1985). Parasol and midget ganglion cells of the human retina. Journal of Comparative Neurology 233, 115–132.CrossRefGoogle ScholarPubMed
Rovamo, J., Virsu, V. & Hyvarinen, L. (1982). Resolution of gratings oriented along and across meridians in peripheral vision. Investigative Ophthalmology and Visual Science 23, 666–670.Google ScholarPubMed
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, 18–23.CrossRefGoogle ScholarPubMed
Schein, S.J. (1988). Anatomy of macaque fovea and spatial densities of neurons in foveal representation. Journal of Comparative Neurology 269, 479–505.CrossRefGoogle ScholarPubMed
Schein, S.J. & De Monasterio, F.M. (1987). Mapping of retinal and geniculate neurons onto striate cortex of macaque. Journal of Neuroscience 7, 996–1009.CrossRefGoogle ScholarPubMed
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, 4287–4302.CrossRefGoogle ScholarPubMed
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, 233–236.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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, 107–120.CrossRefGoogle Scholar
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, 9259–9263.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 267–275.CrossRefGoogle ScholarPubMed
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, 155–174.CrossRefGoogle ScholarPubMed
Thibos, L.N. & Levick, W.R. (1983). Bimodal receptive fields of cat retinal ganglion cells. Vision Research 23, 1561–1572.CrossRefGoogle ScholarPubMed
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, 1–10.CrossRefGoogle ScholarPubMed
Vidyasagar, T.R. (1984). Contribution of inhibitory mechanisms to the orientation sensitivity of cat dLGN neurons. Experimental Brain Research 55, 192–195.CrossRefGoogle Scholar
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, 196–200.CrossRefGoogle Scholar
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, 157–169.CrossRefGoogle Scholar
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. Journal of Comparative Neurology 289, 434–454.CrossRefGoogle ScholarPubMed
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, 336–346.CrossRefGoogle Scholar
Wilson, J.R. (1989). Synaptic organization of individual neurons in the macaque lateral geniculate nucleus. Journal of Neuroscience 9, 2931–2953.CrossRefGoogle ScholarPubMed
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, 411–436.Google ScholarPubMed
Wong-Riley, M.T.T. (1979). Columnar cortico-cortical interconnections within the visual system of the squirrel and macaque monkeys. Brain Research 162, 201–217.CrossRefGoogle ScholarPubMed