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Anatomical pathways for color vision in the human retina

Published online by Cambridge University Press:  02 June 2009

Helga Kolb
Helga Kolb
Affiliation:
Departments of Physiology and Ophthalmology, University of Utah School of Medicine, Salt Lake City
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Abstract

The major neurons and neural circuits that are involved in the transmission of color signals through the human retina to produce the color and spatially opponent P cell or midget ganglion cell responses are described. The older findings of single cone to midget bipolar connectivity is reviewed, and the single midget bipolar cell to midget ganglion cell connectivity as revealed by a recent serial section electron microscope study is described in detail. Our present knowledge concerning the discrimination of the blue-cone subtype from the other longer wavelength cones in the human at the outer plexiform layer is summarized, and our most recent findings concerning horizontal cell connectivity to the different spectral types of cones are discussed. Finally, a hypothetical pathway is proposed for color-opponent surrounds of midget ganglion cells using both horizontal cells at the outer plexiform layer and amacrine cell pathways at the inner plexiform layer.

Keywords

Human retinaConesMidget bipolar cellsMidget ganglion cellsHorizontal cellsAmacrine cells
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 1-2 , August 1991 , pp. 61 - 74
Copyright
Copyright © Cambridge University Press 1991

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References

Ahnelt, P.K., Keri, C. & Kolb, H. (1990). Identification of pedicles of putative blue-sensitive cones in human and primate retina. Journal of Comparative Neurology 293, 39–53.CrossRefGoogle Scholar
Ahnelt, P.K., Kolb, H. & Pflug, R. (1987). Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina. Journal of Comparative Neurology 255, 18–34.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: light microscopy. Philosophical Transactions of the Royal Society B (London) 255, 109–184.Google Scholar
Boycott, B.B., Hopkins, J.M. & Sperling, H.G. (1987). Cone connections of the horizontal cells of the rhesus monkey's retina. Proceedings of the Royal Society B (London) 299, 345–379.Google Scholar
Boycott, B.B. & Kolb, H. (1973). The horizontal cells of the rhesus monkey retina. Journal of Comparative Neurology 148, 115–140.CrossRefGoogle ScholarPubMed
Boynton, R.M. (1988). Color Vision. Annual Review of Psychology 39, 69–100.CrossRefGoogle ScholarPubMed
Creutzfeldt, O.D., Lee, B.B. & Elepfandt, A. (1979). A quantitative study of chromatic organization and receptive fields of cells in the lateral geniculate body of the rhesus monkey. Experimental Brain Research 35, 527–545.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit: a depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Raviola, E. (1990). Physiology of HI horizontal cells in the primate retina. Proceedings of the Royal Society B (London) 239, 213–230.Google Scholar
Demonasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. Journal of Physiology (London) 251, 167–196.Google Scholar
Demonasterio, F.M., Gouras, P. & Tolhurst, D.J. (1975a). Trichromatic colour opponency in ganglion cells of the rhesus monkey retina. Journal of Physiology (London) 251, 197–216.Google Scholar
Demonasterio, F.M., Gouras, P. & Tolhurst, D.J. (1975b). Concealed colour opponency in ganglion cells of the rhesus monkey retina. Journal of Physiology (London) 251, 217–229.Google Scholar
Demonasterio, F.M., Schein, S.J. & McCrane, E.P. (1981). Staining of blue-sensitive cones of the macaque retina by fluorescent dye. Science 213, 1278–1281.CrossRefGoogle ScholarPubMed
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. Journal of Physiology (London) 357, 219–240.Google Scholar
Devalois, R.L. (1960). Color-vision mechanisms in the monkey. Journal of General Physiology 43, 115–128.CrossRefGoogle Scholar
Devalois, R.L., Morgan, H.C., Polson, M.C., Mead, W.R. & Hull, E.M. (1974). Psychophysical studies of monkey vision, I: Macaque luminosity and color-vision tests. Vision Research 14, 53–67.CrossRefGoogle Scholar
Ehinger, B., Ottersen, O.P., Storm-Mathisen, J. & Dowling, J.E. (1988). Bipolar cells in the turtle retina are strongly immunoreactive for glutamate. Proceedings of the National Academy of Sciences of the U.S.A. 85, 8321–8325.CrossRefGoogle ScholarPubMed
Fisher, S.K., Linberg, K.A. & Kolb, H. (1986). A Golgi study of bipolar and horizontal cells in the human retina. Investigative Ophthalmology and Visual Science (Suppl.) 27, 203.Google Scholar
Fuortes, M.G.F. & Simon, E.J. (1974). Interactions leading to horizontal cell responses in the turtle retina. Journal of Physiology (London) 240, 177–199.Google Scholar
Gouras, P. (1968). Identification of cone mechanisms in monkey ganglion cells. Journal of Physiology (London) 199, 533–547.Google Scholar
Gouras, P. (1971). The function of the midget system in primate color vision. Vision Research (Suppl.) 3, 397–410.CrossRefGoogle Scholar
Gouras, P. (1984). Color vision. Progress in Retinal Research 3, 227–261.CrossRefGoogle Scholar
Gouras, P. (1990). Pre-cortical physiology of colour vision. In Vision and Visual Dysfunction, Vol. 6: Perception of Colour, ed. Gouras, P., England: Macmillan Press, Ltd., pp. 163–178.Google Scholar
Gouras, P. & Zrenner, E. (1982). The neural organization of primate color vision. In Color Research and Application, Vol. 7, John Wiley & Sons Inc. pp. 205–298.Google Scholar
Gouras, P. & Evers, H. (1989). Neural systems detecting spectral contrast independently of affective energy contrast: where and how does colour vision begin. In Seeing Contour and Color, ed. Kulikowski, H., Oxford: Pergamon Press. pp. 41–59.Google Scholar
Grassmann, H.G. (1853). Theory of compound colors. Annalen der Physik und Chemie 89, 69–84.CrossRefGoogle Scholar
Hartline, H.K. (1940). The receptive fields of optic nerve fibers. American Journal of Physiology 130, 690–699.CrossRefGoogle Scholar
Helmholtz, H. (1896). Handbuch der Physiologischen Optik, 2nd edition. Liepzig: Voss.Google Scholar
Hendrickson, A.E., Koontz, M.L., Pourcho, R.G., Sarthy, P.V. & Goebel, D.J. (1988). Localization of glycine-containing neurons in Macaca monkey retina. The Journal of Comparative Neurology 273, 473–487.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1960). Receptive fields of optic nerve fibres in the spider monkey. Journal of Physiology (London) 154, 572–580.Google Scholar
Jacobs, G.H. (1981). Comparative Color Vision. New York: Academic Press.Google Scholar
Kaneko, A. (1973). Receptive-field organization of bipolar and amacrine cells in the goldfish retina. Journal of Physiology (London) 213, 95–105.Google Scholar
Kolb, H. (1970). Organization of the outer plexiform layer of the primate retina: electron microscopy of Golgi-impregnated cells. Philosophical Transactions of the Royal Society B (London) 258, 261–283.Google Scholar
Kolb, H. (1984). Cone pathways in the mammalian retina. In Molecular and Cellular Basis of Visual Acuity, ed. Hilfer, S.R. & Sheffield, J.B., pp. 56–78. New York: Springer Verlag.Google Scholar
Kolb, H., Ahnelt, P.F., Linberg, K.A. & Keri, C. (1989). Chromatic connectivity of the three horizontal cell types in the human retina. Investigative Ophthalmology and Visual Science (Suppl.) 30, 348.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
Kolb, H. & Dekorver, L. (1991). Midget ganglion cells of the parafovea of the human retina: a study by electron microscopy and serial-section reconstructions. Journal of Comparative Neurology 303, 617–636.CrossRefGoogle ScholarPubMed
Kolb, H., Linberg, K.A. & Fisher, S.K. (1986). A Golgi study of ganglion cells in the human retina. Investigative Ophthalmology and Visual Science (Suppl.) 27, 203.Google Scholar
Kolb, H., Mariani, A. & Gallego, A. (1980). A second type of horizontal cell in the monkey retina. Journal of Comparative Neurology 189, 31–44.Google ScholarPubMed
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 37–68.CrossRefGoogle ScholarPubMed
Lee, B.B., Martin, P.R. & Valberg, A. (1989). Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker. Journal of Physiology (London) 414, 223–244.Google Scholar
Leeper, H.F. (1978). Horizontal cells of the turtle retina, II: Analysis of interconnections between photoreceptor cells and horizontal cells by light microscopy. Journal of Comparative Neurology 182, 795–810.CrossRefGoogle ScholarPubMed
Linberg, K.A., Fisher, S.K. & Kolb, H. (1986). A Golgi study of amacrine cells in the human retina. Investigative Ophthalmology and Visual Science (Suppl.) 27, 203.Google Scholar
Linberg, K.A., Fisher, S.K. & Kolb, H. (1987). Are there three types of horizontal cell in the human retina? Investigative Ophthalmology and Visual Science (Suppl.) 28, 262.Google Scholar
Mach, E. (1866). Ueber den physiologischen effect raumlich vertheilter lichtreize, II: Sitzber. Akad. Wiss. Wein (Mathnat Kl) Abt. 254, 131–144.Google Scholar
Malpeli, J.G. & Schiller, P.H. (1978). Lack of blue OFF-center cells in the visual system of the monkey. Brain Research 141, 385–389.CrossRefGoogle ScholarPubMed
Marc, R.E. & Sperling, H.G. (1977). Chromatic organization of primate cones. Science 196, 454–456.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1981). A diffuse, invaginating cone bipolar cell in primate retina. Journal of Comparative Neurology 197, 661–671.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1983). Giant bistratified bipolar cells in the monkey retina. Anatomical Record 206, 215–220.CrossRefGoogle Scholar
Mariani, A.P. (1984a). The neuronal organization of the outer plexiform layer in the primate retina. International Review of Cytology 86, 285–320.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1984b). Bipolar cells in monkey retina selective for cones likely to be blue-sensitive. Nature 308, 184–186.CrossRefGoogle ScholarPubMed
Marks, W.B., Dobelle, W.H. & Macnichol, E.F.J. (1964). Visual pigments of single primate cones. Science 43, 1181–1183.CrossRefGoogle Scholar
Marshak, D.W., Aldrich, L.B., Del Valle, J. & Yamada, T. (1990). Localization of immunoreactive cholecystokinin precursor to amacrine cells and bipolar cells of the macaque monkey retina. Journal of Neuroscience 10, 3045–3055.CrossRefGoogle ScholarPubMed
Massey, S.C. & Miller, R.F. (1988). Olutamate receptors of ganglion cells in the rabbit retina: evidence for glutamate as a bipolar cell transmitter. Journal of Physiology (London) 405, 635–655.Google Scholar
Maxwell, J.C. (1855). Experiments on colour, perceived by the eye, with remarks on colour blindness. Edinburgh Transactions 21, 275–297.CrossRefGoogle Scholar
Naka, K.I. (1976). Neuronal circuitry in the catfish retina. Investigative Ophthalmology 15, 926–935.Google Scholar
Nelson, R., Famiglietti, E.V. & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for ON-center and OFF-center ganglion cells in the cat retina. Journal of Neurophysiology 41, 427–483.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 1183–1195.CrossRefGoogle ScholarPubMed
Perry, V.H. & Silveira, L.C.L. (1990). Distribution of magnocellular projecting ganglion cells in the primate retina. Proceedings of the International Society for Eye Research 6, 234.Google Scholar
Polyak, S.L. (1941). The Retina. Chicago, Illinois: University of Chicago Press.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1987). Visualization of endogenous glycine in cat retina: an immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 1189–1197.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1988). The primate retina. Comparative Primate Biology (Neurosciences) 4, 203–278.Google Scholar
Rodieck, R.W., Binmoeller, K.F. & Dineen, J.T. (1985). Parasol and midget ganglion cells of the human retina. Journal of Comparative Neurology 233, 115–132.CrossRefGoogle ScholarPubMed
Röhrenbeck, J., Wässle, H. & Boycott, B.B. (1989). Horizontal cells in the monkey retina: immunocytochemical staining with antibodies against calcium-binding proteins. European Journal of Neuro–science 1, 407–420.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
Schiller, P.H. (1984). The connections of the retinal On and Off pathways to the lateral geniculate nucleus of the monkey. Vision Research 24, 933–942.CrossRefGoogle Scholar
Scholes, J.H. (1975). Colour receptors, and their synaptic connexions in the retina of a cyprinid fish. Philosophical Transactions of the Royal Society B (London) 270, 61–118.Google Scholar
Shapley, R. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neuroscience 9, 229–235.CrossRefGoogle Scholar
Spekreuse, H. & Norton, A.L. (1970). The dynamic characteristics of color-coded S potentials. Journal of General Physiology 56, 1–15.CrossRefGoogle Scholar
Sperling, H.G. (1986). Spectral sensitivity, intense spectral light studies, and the color receptor mosaic of primates. Vision Research 16, 647–657.Google Scholar
Stell, W.K. & Lightfoot, D.O. (1975). Color-specific interconnections of cones and horizontal cells in the retina of the goldfish. Journal of Comparative Neurology 159, 473–501.CrossRefGoogle ScholarPubMed
Stell, W.K., Lightfoot, D.O., Wheeler, T.G. & Leeper, H.F. (1975). Goldfish retina: functional polarization of cone horizontal cell dendrites and synapses. Science 190, 989–990.CrossRefGoogle ScholarPubMed
Svaetichin, G. & Macnichol, E.F.J. (1958). Retinal mechanisms for chromatic and achromatic vision. Annals of the New York Academy of Sciences 74, 385–404.CrossRefGoogle Scholar
Szel, A., Diamanstein, T. & Rohlich, P. (1988). Indentification of blue-sensitive cones in the mammalian retina by antivisual pigment antibody. Journal of Comparative Neurology 273, 593–602.CrossRefGoogle Scholar
Wassle, H., Grunert, U., Röhrenbeck, J. & Boycott, B.B. (1989a). Cortical magnification factor and the ganglion cell density of the pri-mate retina. Nature 341, 643–646.CrossRefGoogle ScholarPubMed
Wässle, H., Boycott, B.B. & Röhrenbeck, J. (1989b). Horizontal cells in the monkey retina: cone connections and dendritic network. European Journal of Neuroscience 1, 421–435.CrossRefGoogle ScholarPubMed
Wässle, H., Schäfer-Trenkler, L. & Voigt, T. (1986). Analysis of glycinergic inhibitory pathway in the cat retina. Journal of Neuro–science, 6, 594–604.Google ScholarPubMed
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. Journal of Comparative Neurology 289, 434–454.CrossRefGoogle ScholarPubMed
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy (Necturus maculosus), II: Intracellular recording. Journal of Neurophysiology 32, 339–355.CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiology 29, 1115–1156.CrossRefGoogle ScholarPubMed
Williams, D.R., Macleod, D.I.A. & Hayhoe, M. (1981a). Foveal tritanopia. Vision Research 21, 1341–1356.CrossRefGoogle ScholarPubMed
Williams, D.R., Macleod, D.I.A. & Hayhoe, M. (1981b). Punctate sensitivity of the blue-sensitive mechanisms. Vision Research 21, 1357–1375.CrossRefGoogle Scholar
Young, T. (1802). On the theory of light and colours. Philosophical Transactions of the Royal Society (London) 92, 20–71.Google Scholar