Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-11T04:34:47.728Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  02 June 2009

Heath D. Wilder ,
Ulrike Grünert ,
Barry B. Lee  and
Paul R. Martin
Heath D. Wilder
Affiliation:
Department of Physiology F13, University of Sydney, NSW 2006, Australia
Ulrike Grünert
Affiliation:
Department of Physiology F13, University of Sydney, NSW 2006, Australia Department of Neuroanatomy, Max-Planck-Institute for Brain Research, Deutschordenstrasse 46, D-60528 Frankfurt am Main, Germany
Barry B. Lee
Affiliation:
Department of Neurobiology, Max-Planck-Institute for Biophysical Chemistry, D-37077 Göttingen, Germany
Paul R. Martin
Affiliation:
Department of Physiology F13, University of Sydney, NSW 2006, Australia
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

PrimateFoveaVisionDichromatTrichromat
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 2 , March 1996 , pp. 335 - 352
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Azzopardi, P. & Cowey, A. (1993). Preferential representation of the fovea in the primary visual cortex. Nature 361, 719–721.CrossRefGoogle ScholarPubMed
Blakemore, C. & Vital-Durand, F. (1986). Organization and postnatal development of the monkey's lateral geniculate nucleus. Journal of Physiology 380, 453–491.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, 109–176.Google Scholar
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, 6187–6191.CrossRefGoogle Scholar
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, 1–17.CrossRefGoogle ScholarPubMed
Cowey, A. & Ellis, C.M. (1967). Visual acuity of rhesus and squirrel monkeys. Journal of Comparative Physiology and Psychology 64, 80–84.CrossRefGoogle ScholarPubMed
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. 23–52. San Diego, California: Academic Press.CrossRefGoogle Scholar
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, 22–45.CrossRefGoogle ScholarPubMed
Crook, J.M., Lange-Malecki, B., Lee, B.B. & Valberg, A. (1988). Visual resolution of macaque retinal ganglion cells. Journal of Physiology 396, 205–224.CrossRefGoogle ScholarPubMed
Crooks, J. & Kolb, H. (1992). Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina. Journal of Comparative Neurology 315, 287–302.CrossRefGoogle ScholarPubMed
Curcio, C.A. & Allen, K.A. (1990). Topography of ganglion cells in human retina. Journal of Comparative Neurology 300, 5–25.CrossRefGoogle ScholarPubMed
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, 610–624.CrossRefGoogle Scholar
Curcio, C.A., Sloan, K.R., Kalina, R.E. & Hendrickson, A.E. (1990). Human photoreceptor topography. Journal of Comparative Neurology 292, 497–523.CrossRefGoogle ScholarPubMed
Dacey, D.M. (1993 a). Morphology of a small-field bistratified ganglion cell type in the macaque and human retina. Visual Neuroscience 10, 1081–1098.CrossRefGoogle ScholarPubMed
Dacey, D.M. (1993 b). The mosaic of midget ganglion cells in the human retina. Journal of Neuroscience 13, 5334–5355.CrossRefGoogle ScholarPubMed
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, 731–735.CrossRefGoogle ScholarPubMed
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, 9666–9670.CrossRefGoogle ScholarPubMed
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, 483–494.CrossRefGoogle ScholarPubMed
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, 1278–1281.CrossRefGoogle ScholarPubMed
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. Journal of Physiology 357, 241–265.CrossRefGoogle ScholarPubMed
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, 890–902.CrossRefGoogle ScholarPubMed
Drasdo, N. & Fowler, C.W. (1974). Non-linear projection of the retinal image in a wide-angle schematic eye. British Journal of Ophthalmology 58, 709–714.CrossRefGoogle ScholarPubMed
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, 445–455.CrossRefGoogle Scholar
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, 157–168.CrossRefGoogle Scholar
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).3.0.CO;2-H>CrossRefGoogle Scholar
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, 1–14.CrossRefGoogle Scholar
Grünert, U. & Martin, P.R. (1991). Rod bipolar cells in the macaque monkey retina: Immunoreactivity and connectivity. Journal of Neuroscience 11, 2742–2758.CrossRefGoogle ScholarPubMed
Grünert, U. & Wässle, H. (1990). GABA-like immunoreactivity in the macaque monkey retina: A light and electron microscopic study. Journal of Comparative Neurology 297, 509–524.CrossRefGoogle ScholarPubMed
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.Google Scholar
Hirsch, J. & Curcio, C. (1989). The spatial resolution capacity of human foveal retina. Vision Research 29, 1095–1101.CrossRefGoogle ScholarPubMed
Hsu, S.M., Raine, L. & Fanger, H. (1981). Use of avidin-biotin peroxidase complex (ABC) in immunoperoxidase techniques. Journal of Histochemistry and Cytochemistry 29, 577–580.CrossRefGoogle ScholarPubMed
Jacobs, D.S. & Blakemore, C. (1988). Faċtors limiting the postnatal development of visual acuity in the monkey. Vision Research 28, 947–958.CrossRefGoogle ScholarPubMed
Jacobs, G.H. (1983). Within-species variations in visual capacity among squirrel monkeys (Saimiri sciurcus): Sensitivity differences. Vision Research 23, 239–248.CrossRefGoogle ScholarPubMed
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, 2545–2549.CrossRefGoogle Scholar
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. 273–336.New York: Pergamon.Google Scholar
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, 177–184.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
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, 19–25.CrossRefGoogle ScholarPubMed
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, 2617–2628.CrossRefGoogle ScholarPubMed
Krebs, W. & Krebs, I.P. (1989). Quantitative morphology of the central fovea of the primate retina. American Journal of Anatomy 184, 225–236.CrossRefGoogle ScholarPubMed
Krubitzer, L.A. & Kaas, J.H. (1990). Cortical connections of MT in four species of primates: Areal, modular and retinotopic patterns. Visual Neuroscience 5, 165–204.CrossRefGoogle ScholarPubMed
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, 1001–1009.CrossRefGoogle ScholarPubMed
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, 367–376.CrossRefGoogle ScholarPubMed
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, 170–189.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in the Old World monkey: Morphology and central projections. Science 213, 1139–1142.CrossRefGoogle ScholarPubMed
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, 325–332.CrossRefGoogle Scholar
Martin, P.R. & GrÜNert, U. (1992). Spatial density and immunoreactivity of bipolar cells in the macaque monkey retina. Journal of Comparative Neurology 323, 269–287.CrossRefGoogle ScholarPubMed
Missotten, L. (1974). Estimation of the ratio of cones to neurons in the fovea of the human retina. Investigative Ophthalmology and Visual Science 13, 1045–1049.Google ScholarPubMed
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, 373–399.Google Scholar
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, 1205–1225.CrossRefGoogle Scholar
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, 165–183.CrossRefGoogle ScholarPubMed
Perry, V.H. & Cowey, A. (1984). Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience 12, 1125–1137.CrossRefGoogle Scholar
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, 1795–1810.CrossRefGoogle ScholarPubMed
Perry, V.H. & Cowey, A. (1988). The lengths of the fibers of Henle in the retina of macaque monkeys: Implications for vision. Neuroscience 25, 225–236.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: University of Chicago Press.Google Scholar
Rodieck, R.W. (1988). The primate retina. In Comparative Primate Biology, Volume4: Neurosciences, ed. Steklis, H.D. & Erwin, J., pp. 203–278. New York: Alan R. Liss.Google Scholar
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. 83–93. London: Plenum.CrossRefGoogle Scholar
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, 46–64.CrossRefGoogle ScholarPubMed
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, 289–303.CrossRefGoogle Scholar
Rohen, J.W. & Castenholz, A. (1967). Über die Zentralisation der Retina bei Primaten. Folia Primatalogia 5, 92–147.CrossRefGoogle Scholar
Rose, R.D. & Rohrlich, D. (1988). Counting sectioned cells via mathematical reconstruction. Journal of Comparative Neurology 272, 617.Google 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). The mapping of retinal and geniculate neurons onto striate cortex of macaque. Journal of Neuroscience 7, 996–1009.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Malpeli, J.G. (1977). Properties and tectal projections of monkey retinal ganglion cells. Journal of Neurophysiology 40, 428–445.CrossRefGoogle ScholarPubMed
Shapley, R. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neurosciences 9, 229–235.CrossRefGoogle Scholar
Silveira, L.C.L. & Perry, V.H. (1991). The topography of magnocellular projecting ganglion cells (M-ganglion cells) in the primate retina. Neuroscience 40, 217–237.CrossRefGoogle ScholarPubMed
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, 887–897.CrossRefGoogle ScholarPubMed
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, 1471–1483.CrossRefGoogle Scholar
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, 191–221.CrossRefGoogle Scholar
Snyder, A.W. & Miller, W.H. (1977). Photoreceptor diameter and spacing for highest resolving power. Journal of the Optical Society of America A 67, 696–698.CrossRefGoogle ScholarPubMed
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. 339–359. Amsterdam: Elsevier.Google Scholar
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, 559–572.CrossRefGoogle ScholarPubMed
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, 551–563.CrossRefGoogle ScholarPubMed
Sterio, D.C. (1984). The unbiased estimation of number and sizes of arbitrary particles using the disector. Journal of Microscopy 134, 127–136.CrossRefGoogle ScholarPubMed
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, 205–223.CrossRefGoogle ScholarPubMed
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, 902–904.CrossRefGoogle ScholarPubMed
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, 867–878.CrossRefGoogle Scholar
Troilo, D., Howland, H.C. & Judge, S.J. (1993). Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus). Vision Research 33, 1301–1310.CrossRefGoogle ScholarPubMed
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, 1726–1734.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, ed. Osborne, N. & Chader, J., pp. 49–100. Pergamon.Google Scholar
Wässle, H. & Chun, M.H. (1989). GABA-like immunoreactivity in the cat retina: Light microscopy. Journal of Comparative Neurology 279, 43–54.CrossRefGoogle ScholarPubMed
Wässle, H., Chun, M.H. & Müller, F. (1987). Amacrine cells in the ganglion cell layer of the cat retina. Journal of Comparative Neurology 265, 391–408.CrossRefGoogle ScholarPubMed
Wässle, H., GrÜNert, U., RÖHrenbeck, J. & Boycott, B.B. (1989). Cortical magnification factor and the ganglion cell density of the primate retina. Nature 341, 643–646.CrossRefGoogle ScholarPubMed
Wässle, H., GrÜNert, U., RÖHrenbeck, J. & Boycott, B.B. (1990). Retinal ganglion cell density and cortical magnification factor in the primate. Vision Research 30, 1897–1911.CrossRefGoogle ScholarPubMed
Wikler, K.C. & Rakic, P. (1990). Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates. Journal of Neuroscience 10, 3390–3401.CrossRefGoogle ScholarPubMed
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, 499–508.CrossRefGoogle ScholarPubMed
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, 159–177.CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed