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Horizontal cell connections with short-wavelength-sensitive cones in macaque monkey retina

Published online by Cambridge University Press:  02 June 2009

Ann K. Goodchild
Affiliation:
Department of Physiology F13, University of Sydney, Sydney, N.S.W. 2006, Australia
Tricia L. Chan
Affiliation:
Department of Physiology F13, University of Sydney, Sydney, N.S.W. 2006, Australia
Ulrike Grünert
Affiliation:
Department of Physiology F13, University of Sydney, Sydney, N.S.W. 2006, Australia

Abstract

This study describes the connectivity between horizontal cells and short-wavelength-sensitive (SWS) cones in macaque monkey retina. H1 and H2 horizontal cells were either labelled with the carbocyanine dye, Dil, or injected intracellularly with Neurobiotin. The retinas were then processed with an antiserum against human SWS cone pigment, which usually stained the entire SWS cone. In these double-labelled retinas, the pattern of connectivity of H1 (n = 91) and H2 (n = 7) cells with SWS cones has been determined. About 85% of the H1 cells examined do not contact SWS cones. The dendritic terminal knobs of five H1 cells that do contact SWS cones were counted. They have, at most, 3% of their dendritic terminal knobs at SWS cones. All H2 cells examined make contact with SWS cones. The dendritic terminal knobs of one H2 cell were counted; about 11% of the dendritic terminal knobs are at the SWS cone. We conclude that horizontal cells in macaque monkey retina show specific patterns of connectivity to SWS cones.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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References

Ahnelt, P., Keri, C. & Kolb, H. (1990). Identification of pedicles of putative blue-sensitive cones in the human retina. Journal of Comparative Neurology 293, 3953.CrossRefGoogle ScholarPubMed
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, 387405.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, 406427.CrossRefGoogle ScholarPubMed
Balthazart, J., Dupiereux, V., Aste, N., Vigletti-Panzica, C., Barrese, M. & Panzica, G.C. (1994). Afferent and efferent connections of the sexually dimorphic medial preoptic nucleus of the male quail revealed by in vitro transport of Dil. Cell and Tissue Research 276, 455475.CrossRefGoogle Scholar
Bloomfield, S.A., Xin, D.Y. & Persky, S.E. (1995). A comparison of receptive field and tracer coupling size of horizontal cells in the rabbit retina. Visual Neuroscience 12, 985999.Google Scholar
Boycott, B.B. (1988). Horizontal cells of mammalian retinae. Neuroscience Research (Suppl.) 8, S97–S111.Google ScholarPubMed
Boycott, B.B. & Dowling, J. (1969). Organisation of primate retina: Light microscopy. Philosophical Transactions of the Royal Society B (London) 255, 109176.Google Scholar
Boycott, B.B. & Hopkins, J.M. (1991). Cone bipolar cells and cone synapses in the primate retina. Visual Neuroscience 7, 4960.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, 345379.Google Scholar
Boycott, B.B. & Kolb, H. (1973). The horizontal cells of the rhesus monkey retina. Journal of Comparative Neurology 148, 115140.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1991). Morphological classification of bipolar cells of the primate retina. European Journal of Neuroscience 3, 10691088.CrossRefGoogle ScholarPubMed
Chan, T.L. & Grünert, U. (1996). Horizontal cell connections with the short wavelength sensitive cones in the common marmoset, Callithrix jacchus. Proceedings of the Australian Neuroscience Society 7, 46.Google Scholar
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 stained with anti-blue opsin. Journal of Comparative Neurology 312, 610624.Google Scholar
Dacey, D.M. (1993). Morphology of a small-field bistratified ganglion cell type in the macaque and human retina. Visual Neuroscience 10, 10811098.CrossRefGoogle ScholarPubMed
Dacey, D.M. & Brace, S. (1992). A coupled network for parasol but not midget ganglion cells in the primate retina. Visual Neuroscience 9, 279290.CrossRefGoogle Scholar
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.Google Scholar
Dacey, D.M., Lee, B.B., Stafford, D.K., Pokorny, J. & Smith, V.C. (1996). Horizontal cells of the primate retina: Cone specificity without spectral opponency. Science 271, 656659.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Raviola, E. (1982). Horizontal cells in the retina of the rabbit. Journal of Neuroscience 10, 14861493.CrossRefGoogle Scholar
Dacheux, R.F. & Raviola, E. (1990). Physiology of (H1) horizontal cells in the primate retina. Proceedings of the Royal Society B (London) 239, 213230.Google Scholar
De Monasterio, P.M., McCrane, E.P., Newlander, J.K. & Schein, S.J. (1985). Density profile of blue-sensitive cones along the horizontal meridian of macaque retina. Investigative Ophthalmology and Visual Science 26, 289302.Google Scholar
Dogiel, A.S. (1891). Über die nervösen Elemente in der Retina des Menschen. Archiv für Mikroskopische Anatomie 38, 317344.CrossRefGoogle Scholar
Famiglietti, E.V. (1990). A new type of wide-field horizontal cell, presumably linked to blue cones, in rabbit retina. Brain Research 535, 174179.Google Scholar
Gallego, A. (1985). Advances in horizontal cell terminology since Cajal. In Neurocircuitry of the Retina, ed. Gallego, A. & Gouras, P., pp. 122140. New York: Elsevier Science Publishing Co., Inc.Google Scholar
Gallego, A. (1986). Comparative studies on horizontal cells and a note on microglial cells. Progress in Retinal Research 5, 165206.CrossRefGoogle Scholar
Goodchild, A.K., Chan, T.L. & Grünert, U. (1995). Anatomical identification of short wavelength sensitive (S) cone input to H1 and H2 horizontal cells in macaque monkey retina. Society for Neuroscience Abstracts 21, 1645.Google Scholar
Harlow, E. & Lane, D. (1988) Antibodies: A laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.Google Scholar
Jacobs, G.H. (1993). The distribution and nature of colour vision among the mammals. Biological Reviews 68, 413471.CrossRefGoogle ScholarPubMed
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, 261283.Google ScholarPubMed
Kolb, H. (1991). Anatomical pathways for color vision in the human retina. Visual Neuroscience 7, 6174.CrossRefGoogle ScholarPubMed
Kolb, H., Fernandez, E., Schouten, J., Ahnelt, P., Linberg, K.A. & Fisher, S.K. (1994). Are there three types of horizontal cell in the human retina? Journal of Comparative Neurology 343, 370386.CrossRefGoogle ScholarPubMed
Kolb, H., Linberg, K.A. & Fisher, S.K. (1992). Neurons of the human retina: A Golgi study. Journal of Comparative Neurology 318, 147187.CrossRefGoogle ScholarPubMed
Kolb, H., Mariani, A. & Gallego, A. (1980). A second type of horizontal cell in the monkey retina. Journal of Comparative Neurology 189, 3144.Google ScholarPubMed
Kuyama, N. & Marshak, D.W. (1992). Bipolar cells specific for blue cones in the macaque retina. Journal of Neuroscience 12, 12331252.Google Scholar
Marc, R.E. & Sperling, H.G. (1977). Chromatic organization of primate cones. Science 196, 454456.Google Scholar
Mariani, A.P. (1984 a). The neuronal organization of the outer plexiform layer of the primate retina. International Review of Cytology 86, 285320.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1984 b). Bipolar cells in monkey retina selective for cones likely to be blue-sensitive. Nature 308, 184186.CrossRefGoogle ScholarPubMed
Müller, B. & Peichl, L. (1993). Horizontal cells in the cone-dominated tree shrew retina: Morphology, photoreceptor contacts, and topographical distribution. Journal of Neuroscience 13, 36283646.Google Scholar
Nelson, R. (1977). Cat cones have rod input: A comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. Journal of Comparative Neurology 172, 109136.CrossRefGoogle ScholarPubMed
Peichl, L. & González-Soriano, J. (1994). Morphological types of horizontal cell in rodent retinae: A comparison of rat, mouse, gerbil, and guinea pig. Visual Neuroscience 11, 501517.CrossRefGoogle ScholarPubMed
Raviola, R.F. & Gilula, N.B. (1975). Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. Journal of Cell Biology 65, 192222.CrossRefGoogle ScholarPubMed
Sandell, J.H. & Masland, R.H. (1988). Photoconversion of some fluorescent markers to a diaminobenzidine product. Journal of Histochemistry and Cytochemistry 36, 555559.CrossRefGoogle ScholarPubMed
Sandmann, D., Boycott, B.B. & Peichl, L. (1996). Blue cone horizontal cells in the retinae of horses and other Equidae. Journal of Neuroscience 16, 33813396.Google Scholar
Silveira, L.C.L., Yamada, E.S. & Picano-Diniz, C.W. (1989). Displaced horizontal cells and biplexiform horizontal cells in the mammalian retina. Visual Neuroscience 3, 483488.CrossRefGoogle ScholarPubMed
Szél, A., Diamantstein, T. & Röhlich, P. (1988). Identification of the blue-sensitive cones in the mammalian retina by anti-visual pigment antibody. Journal of Comparative Neurology 273, 593602.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1991). Many diverse types of retinal neurones show tracer coupling when injected with biocytin or neurobiotin. Neuroscience Letters 125, 187190.CrossRefGoogle ScholarPubMed
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, 217223.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, 93101.Google ScholarPubMed
Wang, Y., Macke, J.P., Merbs, S.L., Zack, D.J., Klaunberg, B., Bennet, J., Gearhart, J. & Nathans, J. (1992). A locus control region adjacent to the human red and green visual pigment genes. Neuron 9, 429440.CrossRefGoogle 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, 421435.CrossRefGoogle ScholarPubMed
Wässle, H., Grünert, U., Martin, P.R. & Boycott, B.B. (1994). Immunocytochemical characterization and spatial distribution of midget bipolar cells in the macaque monkey retina. Vision Research 34, 561579.CrossRefGoogle ScholarPubMed
Wikler, K.C. & Rakic, P. (1990). Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates. Journal of Neuroscience 10, 33903401.Google Scholar
Yang, G. & Masland, R.H. (1994). Receptive fields and dendritic structure of directionally selective ganglion cells. Journal of Neuroscience 14, 52675280.CrossRefGoogle Scholar