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The morphology and distribution of horizontal cells in the retina of a New World monkey, the marmoset Callithrix jacchus: A comparison with macaque monkey

Published online by Cambridge University Press:  02 June 2009

Tricia L. Chan ,
Ann K. Goodchild  and
Paul R. Martin
Tricia L. Chan
Affiliation:
Department of Physiology and Institute for Biomedical Research, The University of Sydney, NSW 2006, Australia
Ann K. Goodchild
Affiliation:
Department of Physiology and Institute for Biomedical Research, The University of Sydney, NSW 2006, Australia
Paul R. Martin
Affiliation:
Department of Physiology and Institute for Biomedical Research, The University of Sydney, NSW 2006, Australia
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Abstract

The morphology and distribution of horizontal cells was studied in the retina of a New World monkey, the marmoset, Callithrix jacchus, and compared with that of the Old World macaque monkey. Horizontal cells in macaque and marmoset were either labelled with the carbocyanine dye, Dil, and then photoconverted, or were labelled by intracellular injection with Neurobiotin. The marmoset has two types of horizontal cell, H1 and H2, which have dendritic and axonal morphology similar to their counterparts in Old World monkeys and human. The dendritic-field size of both cell types increases with distance from the fovea. Both types make contact with the vast majority of the cones within their dendritic field. The dendrites of H1 cells in marmoset contact almost twice as many cones as H1 cells in macaque at an equivalent eccentricity. With increasing distance from the fovea, H1 cells make contact with more cones but have, on average, fewer terminal knobs inserted in each cone. The increase in dendritic-field area of H1 cells is balanced by a decrease in spatial density (from 4500 cells/mm2 at 25 deg eccentricity to 1000 cells/mm2 in far peripheral retina), so coverage of the retina remains fairly constant, between 5 and 8. Overall, the results show that the qualitative morphological properties, as well as quantitative population properties of horizontal cells, are common to both New World and Old World primates.

Keywords

Primate visionRetina circuitryPhotoreceptorsHorizontal cell morphologyNeurone mosaics

Information

Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 1 , January 1997 , pp. 125 - 140
Copyright
Copyright © Cambridge University Press 1997

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References

Ahnelt, P. & Kolb, H. (1994 a). Horizontal cells and cone photoreceptors in primate retina: A Golgi-light microscopic study of spectral connectivity. Journal of Comparative Neurology 343, 387–405.CrossRefGoogle ScholarPubMed
Ahnelt, P. & Kolb, H. (1994 b). Horizontal cells and cone photoreceptors in human retina: A Golgi-electron microscopic study of spectral connectivity. Journal of Comparative Neurology 343, 406–427.CrossRefGoogle ScholarPubMed
Bloomfield, S.A., Xin, D. & Persky, S.E. (1995). A comparison of receptive field and tracer coupling size of horizontal cells in the rabbit retina. Visual Neuroscience 12, 985–999.CrossRefGoogle ScholarPubMed
Bowmaker, J.K. (1991). Visual pigments and colour vision in primates. In From Pigments to Perception: Advances in Understanding Visual Processes, ed. Valsero, A. & Lee, B.B., pp. 1–9. New York: Plenum Press.Google Scholar
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
Boycott, B.B. & Kolb, H. (1973). The horizontal cells of the rhesus monkey retina. Journal of Comparative Neurology 148, 115–140.CrossRefGoogle ScholarPubMed
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) 229, 345–379.Google Scholar
Cajal, S.R. (1893). La Rétine des vertébrés. Cellule 9, 121–255.Google Scholar
Chan, T.L. & Grünert, U. (1996). Horizontal cell connections with short wavelength sensitive cones in the common marmoset Callithrix jacchus. Australian Neuroscience Society Abstracts 7, 46.Google Scholar
Chan, T.L., Goodchild, A.K. & Martin, P.R. (1995). Morphology and distribution of horizontal cells in Old and New World primate retina. Australian Neuroscience Society Abstracts 6, 204.Google Scholar
Dacey, D.M. & Brace, S. (1992). A coupled network for parasol but not midget ganglion cells in the primate retina. Visual Neuroscience 9, 279–290.Google Scholar
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.Google Scholar
Dacey, D.M., Lee, B.B., Stafford, O.K., Pokorny, J. & Smith, V.C. (1996). Horizontal cells of the primate retina: Cone specificity without spectral opponency. Science 271, 656–659.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Raviola, E. (1990). Physiology of H1 horizontal cells in the primate retina. Proceedings of the Royal Society B (London) 239, 213–230.Google Scholar
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.Google Scholar
Dick, A., Kaske, A. & Creutzfeldt, O.D. (1991). Topographical and topological organization of the thalamocortical projection to the striate and prestriate cortex in the marmoset (Callilhrix jacchus). Experimental Brain Research 84, 233–253.Google Scholar
Dogiel, A.S. (1891). Über die nervösen Elemente in der Retina des Menschen. Archiv für Mikroskopische Anatomie 38, 317–344.CrossRefGoogle Scholar
Dowling, J.E. (1987). The Retina: An Approachable Pan of the Brain. Cambridge, Massachusetts: The Belknapp Press of Harvard University Press.Google Scholar
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
Fritsches, K.A. & Rosa, M.G.P. (1996). Visuotopic organisation of striate cortex in the marmoset monkey (Callithrix jacchus). Journal of Comparative Neurology 372, 264–282.Google Scholar
Gallego, A. (1976). Comparative study of the horizontal cells in the vertebrate retina: Mammals and birds. In Neural Principles in Vision, ed. Zettler, F. & Weiler, R., pp. 22–62. Berlin: Springer.Google Scholar
Ghosh, K.K., Goodchild, A.K., Sefton, A.E. & Martin, P.R. (1996). The morphology of retinal ganglion cells in a New World monkey, the marmoset Callithrix jacchus. Journal of Comparative Neurology 366, 76–92.Google Scholar
Goodchild, A.K., Chan, T.L. & Grünert, U. (1996 a). Horizontal cell connections with short wavelength sensitive cones in macaque monkey retina. Visual Neuroscience 13, 833–845.Google Scholar
Goodchild, A.K., Ghosh, K.K. & Martin, P.R. (1996 b). Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat and the marmoset Callithrix jacchus. Journal of Comparative Neurology 366, 55–75.3.0.CO;2-J>CrossRefGoogle Scholar
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.Google Scholar
Harlow, E. & Lane, D. (1988). Antibodies: A Laboratory Manual. New York: Cold Spring Harbor Laboratory.Google Scholar
Jacobs, G.H. (1984). Within-species variations in visual capacity among squirrel monkeys (Saimiri sciureus): Colour vision. Vision Research 24, 1267–1277.Google Scholar
Jacobs, G.H. (1993). The distribution and nature of colour vision among the mammals. Biological Reviews 68, 413–471.Google Scholar
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
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., Fernandez, E., Schouten, J., Ahnelt, P., Linberg, K. & Fisher, S. (1994). Are there three types of horizontal cell in the human retina? Journal of Comparative Neurology 343, 370–386.Google Scholar
Kolb, H., Linberg, K.A. & Fisher, S.K. (1992). Neurons of the human retina: A Golgi study. Journal of Comparative Neurology 318, 147–187.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 Scholar
Mariani, A. (1984). The neuronal organization of the outer plexiform layer of the primate retina. International Review of Cytology 86, 285–320.Google Scholar
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 (London) 222, 373–399.Google Scholar
Ogden, T.E. (1974). The morphology of retinal neurons of the owl monkey, Aotes. Journal of Comparative Neurology 153, 399–428.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.Google 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.Google 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.Google 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, Volume 4: Neurosciences, ed. Steklis, H. D. & Erwin, J., pp. 203–278. New York: Alan R. Liss.Google Scholar
Sandell, J.H. & Masland, R.H. (1988). Photoconversion of some fluorescent markers to a diaminobenzidine product. Journal of Histochemistry and Cytochemistry 36, 555–559.Google Scholar
Sandmann, D., Boycott, B.B. & Peichl, L. (1996 a) Blue cone horizontal cells in the retinae of horses and other Equidae. Journal of Neuroscience 16, 3381–3396Google Scholar
Sandmann, D., Boycott, B.B. & Peichl, L. (1996 b) The horizontal cells of Artiodactyl retinae: A comparison with Cajal's descriptions. Visual Neuroscience 13, 735–746.Google Scholar
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.Google Scholar
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.Google Scholar
Travis, D.S., Bowmaker, J.K. & Mollon, J.D. (1988). Polymorphism of visual pigments in a callitrichid monkey. Vision Research 28, 481–490.Google 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.Google Scholar
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neuroscience Letters 125, 187–190.Google Scholar
Vaney, D.I. (1992). Photochromic intensification of diaminobenzidine reaction product in the presence of tetrazolium salts: Applications for intracellular labelling and immunohistochemistry. Journal of Neuroscience Methods 44, 217–223.Google Scholar
Vaney, D.I. (1993). The coupling pattern of axon-bearing horizontal cells in the mammalian retina. Proceedings of the Royal Society B (London) 252, 93–101.Google Scholar
Vardi, N., Kaufman, D.L. & Sterling, P. (1994). Horizontal cells in cat and monkey retina express different isoforms of glutamic acid decarboxylase. Visual Neuroscience 11, 135–142.Google Scholar
Wässle, H., Boycott, B.B. & Röhrenbeck, J. (1989). Horizontal cells in the monkey retina: Cone connections and dendritic network. European Journal of Neuroscience 1, 421–435.CrossRefGoogle ScholarPubMed
Wässle, H., Levick, W.R. & Cleland, B.G. (1975). The distribution of the alpha type of ganglion cells in the cat's retina. Journal of Comparative Neurology 159, 419–438.Google Scholar
Wässle, H., Peichl, L. & Boycott, B.B. (1978). Topography of horizontal cells in the retina of the domestic cat. Proceedings of the Royal Society B (London) 203, 269–291.Google 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
Wilder, H.D., Grünert, U., Lee, B.B. & Martin, P.R. (1996). Topography of ganglion cells and photoreceptors in the retina of a New World monkey: The marmoset Callithrix jacchus. Visual Neuroscience 13, 335–352.CrossRefGoogle ScholarPubMed
Yeh, T., Lee, B.B., Kremers, J., Cowing, J.A., Hunt, D.M., Martin, P.R. & Troy, J. (1996). Visual responses in the lateral geniculate nucleus of dichromatic and trichromatic marmosets (Callithrix jacchus). Journal of Neuroscience 15, 7892–7904.CrossRefGoogle Scholar