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Topography of ganglion cells and photoreceptors in the retina of a New World monkey: The marmoset Callithrix jacchus

  • Heath D. Wilder (a1), Ulrike Grünert (a1) (a2), Barry B. Lee (a3) and Paul R. Martin (a1)

Abstract

We studied the anatomical substrates of spatial vision in a New World monkey, the marmoset Callithrix jacchus. This species has good visual acuity and a foveal specialization which is qualitatively similar to that of humans and other Old World primates.We measured the spatial density of retinal ganglion cells and photoreceptors, and calculated the relative numbers of these cell populations. We find that ganglion cells outnumber photoreceptors by between 2.4:1 and 4.2:1 in the fovea. The peak sampling density of ganglion cells is close to 550,000 cells/mm2. This value falls by almost 1000-fold between the fovea and peripheral retina; a value which approaches recent estimates of the centroperipheral ganglion cell gradient for human and macaque monkey retina and primary visual cortex. The marmoset shows a sex-linked polymorphism of color vision: all male and some female marmosets are dichromats. Six of the retinas used in the present study came from animals whose chromatic phenotype was identified in electrophysiological experiments and confirmed by polymerase chain reaction (PCR) amplification of cone opsin encoding genes. One animal was a trichromat and the others were dichromats. Antibodies against short wavelength-sensitive (SWS) cones labeled close to 8% of all cones near the fovea of onedichromat animal, consistent with electrophysiological evidence that the SWS system is present inall marmosets. The topography and spatial density of cone photoreceptors and ganglion cells was similar to that reported for macaque retina, and we found no obvious difference between dichromatic and trichromatic marmoset retinas. These results reinforce the view that the main determinate of primate foveal topography is the requirement for maximal spatial resolution.

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Azzopardi, P. & Cowey, A. (1993). Preferential representation of the fovea in the primary visual cortex. Nature 361, 719721.
Blakemore, C. & Vital-Durand, F. (1986). Organization and postnatal development of the monkey's lateral geniculate nucleus. Journal of Physiology 380, 453491.
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions of the Royal Society B (London) 255, 109176.
Brecha, N.C., Hohnson, D., Peichl, L. & WÄSsle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and γ-aminobutyrateimmunoreactivity. Proceedings of the National Academy of Sciences of the U.S.A. 85, 61876191.
Brysch, W., Brysch, I., Creutzfeldt, O.D., Schlingensiepen, R. & Schlingensiepen, K.H. (1990). The topology of the thalamocortical projections in the marmoset monkey (Callithrix jacchus). Experimental Brain Research 81, 117.
Cowey, A. & Ellis, C.M. (1967). Visual acuity of rhesus and squirrel monkeys. Journal of Comparative Physiology and Psychology 64, 8084.
Crawford, M.L.J., Andersen, R.A., Blake, R., Jacobs, G.H. & Neumeyer, C. (1990). Interspecies comparisons in the understanding of human visual perception. In Visual Perception: The Neurological Foundations, ed. Spillmann, L. & Werner, J.S., pp. 2352. San Diego, California: Academic Press.
Creutzfeldt, O.D., Kastner, S., Pei, X. & Valberg, A. (1991). The neurophysiological correlates of colour and brightness contrast in lateral geniculate neurons. II. Adaptation and surround effects. Experimental Brain Research 87, 2245.
Crook, J.M., Lange-Malecki, B., Lee, B.B. & Valberg, A. (1988). Visual resolution of macaque retinal ganglion cells. Journal of Physiology 396, 205224.
Crooks, J. & Kolb, H. (1992). Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina. Journal of Comparative Neurology 315, 287302.
Curcio, C.A. & Allen, K.A. (1990). Topography of ganglion cells in human retina. Journal of Comparative Neurology 300, 525.
Curcio, C.A., Allen, K.A., Sloan, K.R., Lerea, C.L., Hurley, J.B., Klock, I.B. & Milam, A.H. (1991). Distribution and morphology of human cone photoreceptors strained with anti-blue opsin. Journal of Comparative Neurology 312, 610624.
Curcio, C.A., Sloan, K.R., Kalina, R.E. & Hendrickson, A.E. (1990). Human photoreceptor topography. Journal of Comparative Neurology 292, 497523.
Dacey, D.M. (1993 a). Morphology of a small-field bistratified ganglion cell type in the macaque and human retina. Visual Neuroscience 10, 10811098.
Dacey, D.M. (1993 b). The mosaic of midget ganglion cells in the human retina. Journal of Neuroscience 13, 53345355.
Dacey, D.M. & Lee, B.B. (1994). The ‘blue-on’ opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731735.
Dacey, D.M. & Petersen, M.R. (1992). Dendritic field size and morphology of midget and parasol ganglion cells of the human retina. Proceedings of the National Academy of Sciences of the U.S.A. 89, 96669670.
Davanger, S., Ottersen, O.P. & Storm-Mathisen, J. (1991). Glutamate, GABA, and glycine in the human retina: An immunocytochemical investigation. Journal of Comparative Neurology 311, 483494.
Demonasterio, F.M., Schein, S.J. & McCrane, E.P. (1981). Staining of blue-sensitive cones of the macaque retina by a fluorescent dye. Science 213, 12781281.
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. Journal of Physiology 357, 241265.
Dow, B.M., Vautin, R.G. & Bauer, R. (1985). The mapping of visual space onto foveal striate cortex in the macaque monkey. Journal of Neuroscience 5, 890902.
Drasdo, N. & Fowler, C.W. (1974). Non-linear projection of the retinal image in a wide-angle schematic eye. British Journal of Ophthalmology 58, 709714.
Freed, M.A., Smith, R.G. & Sterling, P. (1987). Rod bipolar cell array in the cat retina: Pattern of input from rods and GABA-accumulating cells. Journal of Comparative Neurology 266, 445455.
Fritchy, J.M. & Garey, L.J. (1986). Postnatal development of quantitative morphological parameters in the lateral geniculate nucleus of the marmoset monkey. Brain Research 395, 157168.
Ghosh, K.K., Goodchild, A.K., Sefton, A.E. & Martin, P.R. (1996). The morphology of retinal ganglion cells in the New World marmoset monkey Callithrix jacchus. Journal of Comparative Neurology (in press).
Grünert, U., Greferath, U., Boycott, B.B. & Wässle, H. (1993). Parasol (Pa) ganglion cells of the primate fovea: Immunocytochemical staining with antibodies against GABAA-receptors. Vision Research 33, 114.
Grünert, U. & Martin, P.R. (1991). Rod bipolar cells in the macaque monkey retina: Immunoreactivity and connectivity. Journal of Neuroscience 11, 27422758.
Grünert, U. & Wässle, H. (1990). GABA-like immunoreactivity in the macaque monkey retina: A light and electron microscopic study. Journal of Comparative Neurology 297, 509524.
Halasz, P. & Martin, P.R. (1984). A microcomputer based system for semi-automatic analysis of histological sections. Proceedings of the Royal Microscopical Society 19, 312.
Hirsch, J. & Curcio, C. (1989). The spatial resolution capacity of human foveal retina. Vision Research 29, 10951101.
Hsu, S.M., Raine, L. & Fanger, H. (1981). Use of avidin-biotin peroxidase complex (ABC) in immunoperoxidase techniques. Journal of Histochemistry and Cytochemistry 29, 577580.
Jacobs, D.S. & Blakemore, C. (1988). Faċtors limiting the postnatal development of visual acuity in the monkey. Vision Research 28, 947958.
Jacobs, G.H. (1983). Within-species variations in visual capacity among squirrel monkeys (Saimiri sciurcus): Sensitivity differences. Vision Research 23, 239248.
Jacobs, G.H. & Neitz, J. (1987). Inheritance of colour vision in a New World monkey (Saimiri sciureus). Proceedings of the National Academy of Sciences of the U.S.A. 84, 25452549.
Kaplan, E., Lee, B.B. & Shapley, R.M. (1989). New views of primate retinal function. In Progress in Retinal Research, ed. Osborne, N. & Chader, J., pp. 273336.New York: Pergamon.
Kolb, H., Boycott, B.B. & Dowling, J.E. (1969). 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. (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, 617636.
Koontz, M.A., Hendrickson, A.E. & Ryan, M.K. (1989). GABA-immunoreactive synaptic plexus in the nerve fiber layer of primate retina. Visual Neuroscience 2, 1925.
Koontz, M.A., Hendrickson, L.E., Brace, S.T. & Hendrickson, A.E. (1993). Immunocytochemical localization of GABA and glycine in amacrine and displaced amacrine cells of macaque monkey retina. Vision Research 33, 26172628.
Krebs, W. & Krebs, I.P. (1989). Quantitative morphology of the central fovea of the primate retina. American Journal of Anatomy 184, 225236.
Krubitzer, L.A. & Kaas, J.H. (1990). Cortical connections of MT in four species of primates: Areal, modular and retinotopic patterns. Visual Neuroscience 5, 165204.
Lee, B.B., Wehrhahn, C., Westheimer, G. & Kremers, J. (1993). Macaque ganglion cell responses to stimuli that elicit hyperacuity in man: Detection of small displacements. Journal of Neuroscience 13, 10011009.
Lerea, C.L., Bunt-Milam, A.H. & Hurley, J.B. (1989). α transducin is present in blue-, green-, and red-sensitive cone photoreceptors in the human retina. Neuron 3, 367376.
Leventhal, A.G., Ault, S.J., Vitek, D.J. & Shou, T. (1989). Extrinsic determinants of retinal ganglion cell development in primates. Journal of Comparative Neurology 286, 170189.
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in the Old World monkey: Morphology and central projections. Science 213, 11391142.
Lynch, J.J., Eskin, T.A. & Merigan, W.H. (1989). Selective degeneration of the parvocellular-projecting retinal ganglion cells in a New World monkey, Saimiri sciureus. Brain Research 499, 325332.
Martin, P.R. & GrÜNert, U. (1992). Spatial density and immunoreactivity of bipolar cells in the macaque monkey retina. Journal of Comparative Neurology 323, 269287.
Missotten, L. (1974). Estimation of the ratio of cones to neurons in the fovea of the human retina. Investigative Ophthalmology and Visual Science 13, 10451049.
Mollon, J.D., Bowmaker, J.K. & Jacobs, G.H. (1984). Variations of colour vision in a New World primate can be explained by a polymorphism of retinal photopigments. Proceedings of the Royal Society B 222, 373399.
Ordy, J.M. & Samorajski, T. (1968). Visual acuity and ERG-CFF in relation to the morphologic organization of the retina among diurnal and nocturnal primates. Vision Research 8, 12051225.
Packer, O., Hendrickson, A.E. & Curcio, C.A. (1989). Photoreceptor topography of the retina in the adult pigtail macaque (Macaca nemestrina). Journal of Comparative Neurology 288, 165183.
Perry, V.H. & Cowey, A. (1984). Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience 12, 11251137.
Perry, V.H. & Cowey, A. (1985). The ganglion cell and cone distributions in the monkey's retina: Implications for central magnification factors. Vision Research 25, 17951810.
Perry, V.H. & Cowey, A. (1988). The lengths of the fibers of Henle in the retina of macaque monkeys: Implications for vision. Neuroscience 25, 225236.
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: University of Chicago Press.
Rodieck, R.W. (1988). The primate retina. In Comparative Primate Biology, Volume4: Neurosciences, ed. Steklis, H.D. & Erwin, J., pp. 203278. New York: Alan R. Liss.
Rodieck, R.W. (1991). Which cells code for color? In From Pigments to Perception: Advances in Understanding Visual Processes, ed. Valberg, A. & Lee, B.B., pp. 8393. London: Plenum.
Rodieck, R.W. & Marshak, D.W. (1992). Spatial density and distribution of choline acetyltransferase immunoreactive cells in human, macaque and baboon retinas. Journal of Comparative Neurology 321, 4664.
Rodieck, R.W. & Watanabe, M. (1993). Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae of the lateral geniculate nucleus. Journal of Comparative Neurology 338, 289303.
Rohen, J.W. & Castenholz, A. (1967). Über die Zentralisation der Retina bei Primaten. Folia Primatalogia 5, 92147.
Rose, R.D. & Rohrlich, D. (1988). Counting sectioned cells via mathematical reconstruction. Journal of Comparative Neurology 272, 617.
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). The mapping of retinal and geniculate neurons onto striate cortex of macaque. Journal of Neuroscience 7, 9961009.
Schiller, P.H. & Malpeli, J.G. (1977). Properties and tectal projections of monkey retinal ganglion cells. Journal of Neurophysiology 40, 428445.
Shapley, R. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neurosciences 9, 229235.
Silveira, L.C.L. & Perry, V.H. (1991). The topography of magnocellular projecting ganglion cells (M-ganglion cells) in the primate retina. Neuroscience 40, 217237.
Silveira, L.C.L., Perry, V.H. & Yamada, E.S. (1993). The retinal ganglion cell distribution and the representation of the visual field in area 17 of the owl monkey, Aotus trivirgatus. Visual Neuroscience 10, 887897.
Silveira, L.C.L., Picanço-Diniz, C.W., Sampaio, L.F.S. & Oswaldocruz, E. (1989). Retinal ganglion cell distribution in the cebus monkey: A comparison with the cortical magnification factors. Vision Research 11, 14711483.
Smith, V.C., Lee, B.B., Pokorny, J., Martin, P.R. & Valberg, A. (1992). Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights. Journal of Physiology 458, 191221.
Snyder, A.W. & Miller, W.H. (1977). Photoreceptor diameter and spacing for highest resolving power. Journal of the Optical Society of America A 67, 696698.
Somogyi, P. (1988). Immunocytochemical demonstration of GABA in physiologically characterized, HRP-filled neurons and their postsynaptic targets. In Molecular Neuroanatomy, ed. Van Leeuwen, F.W., Bujis, R.M., Pool, C.W. & Pach, O., pp. 339359. Amsterdam: Elsevier.
Spatz, W.B. (1977). Topographically organized reciprocal connections between areas 17 and MT (visual area of the superior temporal sulcus) in the marmoset Callithrix jacchus. Experimental Brain Research 27, 559572.
Spatz, W.B. (1978). The retino-geniculo-cortical pathway in Callithrix I. Intraspecific variations in the lamination pattern of the lateral geniculate nucleus. Experimental Brain Research 33, 551563.
Sterio, D.C. (1984). The unbiased estimation of number and sizes of arbitrary particles using the disector. Journal of Microscopy 134, 127136.
Stone, J. & Johnstone, E. (1981). The topography of primate retina: A study of the human, bushbaby, and New- and Old-World monkeys. Journal of Comparative Neurology 196, 205223.
Tootell, R.B.H., Silverman, M.S., Switkes, E. & De Valois, R.L. (1982). Deoxyglucose analysis of retinotopic organization in primate striate cortex. Science 218, 902904.
Tovée, M.J., Bowmaker, J.K. & Mollon, J.D. (1992). The relationship between cone pigments and behavioural sensitivity in a New World monkey. (Callithrix jacchus jacchus). Vision Research 32, 867878.
Troilo, D., Howland, H.C. & Judge, S.J. (1993). Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus). Vision Research 33, 13011310.
Valberg, A., Seim, T., Lee, B.B. & Tryti, J. (1986). Reconstruction of equidistant colour space from responses of visual neurones of macaques. Journal of the Optical Society of America A 3, 17261734.
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, ed. Osborne, N. & Chader, J., pp. 49100. Pergamon.
Wässle, H. & Chun, M.H. (1989). GABA-like immunoreactivity in the cat retina: Light microscopy. Journal of Comparative Neurology 279, 4354.
Wässle, H., Chun, M.H. & Müller, F. (1987). Amacrine cells in the ganglion cell layer of the cat retina. Journal of Comparative Neurology 265, 391408.
Wässle, H., GrÜNert, U., RÖHrenbeck, J. & Boycott, B.B. (1989). Cortical magnification factor and the ganglion cell density of the primate retina. Nature 341, 643646.
Wässle, H., GrÜNert, U., RÖHrenbeck, J. & Boycott, B.B. (1990). Retinal ganglion cell density and cortical magnification factor in the primate. Vision Research 30, 18971911.
Wikler, K.C. & Rakic, P. (1990). Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates. Journal of Neuroscience 10, 33903401.
Wikler, K.C., Williams, R.W. & Rakic, P. (1990). Photoreceptor mosaic: Number and distribution of rods and cones in the rhesus monkey retina. Journal of Comparative Neurology 297, 499508.
Wong, R.O.L. & Hughes, A. (1987). The morphology, number, and distribution of a large population of confirmed displaced amacrine cells in the adult cat retina. Journal of Comparative Neurology 255, 159177.
Yeh, T., Lee, B.B., Kremers, J., Cowing, J.A., Hunt, D.M., Martin, P.R. & Troy, J. (1995). Visual responses in the lateral geniculate nucleus of dichromatic and trichromatic marmosets (Callithrix jacchus). Journal of Neuroscience (in press).

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Topography of ganglion cells and photoreceptors in the retina of a New World monkey: The marmoset Callithrix jacchus

  • Heath D. Wilder (a1), Ulrike Grünert (a1) (a2), Barry B. Lee (a3) and Paul R. Martin (a1)

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