Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-19T23:00:18.945Z Has data issue: false hasContentIssue false

Cone bipolar cells and cone synapses in the primate retina

Published online by Cambridge University Press:  02 June 2009

B. B. Boycott
Affiliation:
Department of Anatomy, United Medical and Dental Schools of Guy's and St. Thomas's Hospitals (Guy's Campus), London Se1 9Rt, UK
J. M. Hopkins
Affiliation:
Department of Anatomy, United Medical and Dental Schools of Guy's and St. Thomas's Hospitals (Guy's Campus), London Se1 9Rt, UK

Abstract

Primate retinal bipolar cells synapsing with two adjacent cones (2C bipolars) are further described. Their synaptic contacts are either as the central (invaginating) component of the cone triads or as basal (flat) contacts on the membrane of the cone pedicle base. Correspondingly, their axons end either in the b (inner) half or in the a (outer) half of the inner plexiform layer. The shape and size of the axon terminals of 2C bipolars are indistinguishable from those of adjacent midget bipolars. Therefore 2C bipolars, like midget bipolars, probably synapse with midget ganglion cells. Two C bipolars have not been identified as connected to foveal cones. But they are not restricted to the retinal periphery, as has previously been supposed, since they occur, mixed with midget (single cone) bipolars, throughout all parts of the retina from about 2.5 mm to atleast 10.0 mm from the fovea. It is likely that 2C bipolars are a variant of the midget bipolars; and that they contact some members of the same population of cones, instead of the midgets. This paper briefly reviews, and raises some new, problems concerning our current understanding of the synaptic connectivity patterns of the midget, 2C, and diffuse cone bipolar cells.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

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

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
Boycott, B.B. (1988). Horizontal cells of mammalian retinae. Neuro-science Research (Suppl.) 8, S97–S111.Google ScholarPubMed
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: light microscopy. Philosophical Transactions of the Royal Society B (London) 255, 109194.Google Scholar
Boycott, B.B. & Hopkins, J.M. (1981). Microglia in the retina of monkey and other mammals; its distinction from other types of glia and horizontal cells. Neuroscience 6, 679688.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 connections between bipolar cells and photoreceptors in the retina of the domestic cat. Journal of Comparative Neurology 148, 91114.CrossRefGoogle ScholarPubMed
Boycott, B.B., Peichl, L. & Wassle, H. (1978). Morphological types of horizontal cell in the retina of the domestic cat. Proceedings of the Royal Society B (London) 203, 229245.Google Scholar
Brandon, C. & Lam, D.M.-K. (1983). The ultrastructure of rod synaptic terminals: effects of dark adaptation. Journal of Comparative Neurology 217, 167175.CrossRefGoogle ScholarPubMed
Cragg, B.G. (1969). Structural changes in naive retinal synapses detectable within minutes of first exposure to daylight. Brain Research 15, 7996.CrossRefGoogle ScholarPubMed
Dacheux, R.F. (1982). Connections of the small bipolar cells with the photoreceptors in the turtle. An electron microscope study of Oolgiimpregnated, gold-toned retinas. Journal of Comparative Neurology 205, 5562.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331345.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1965). Foveal receptors of the monkey retina: fine structure. Science (Washington) 147, 5759.Google Scholar
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Massachusetts: Harvard University Press.Google Scholar
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: electron microscopy. Proceedings of the Royal Society B (London) 166, 80111.Google Scholar
Downing, J.E.G., Djamgoz, M.B.A. & Bowmaker, J.K. (1986). Photoreceptors of a cyprinid fish, the roach: morphological and spectral characteristics. Journal Comparative Physiology A 159, 859868.CrossRefGoogle Scholar
Greferath, U., Grünert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoactivity. Journal of Comparative Neurology 301, 433442.CrossRefGoogle Scholar
Kirsch, M., Djamgoz, M.B.A. & Wagner, H.-J. (1990). Correlation of spinule dynamics and plasticity of the horizontal cell spectral response in cyprinid fish retina: quantitative analysis. Cell and Tissue Research 260, 123130.CrossRefGoogle 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, 177184.Google Scholar
Kolb, H. (1970). Organization of the outer plexiform layer of the pri-mate retina: electron microscopy of Golgi-impregnated cells. Philosophical Transactions of the Royal Society B (London) 258, 261283.Google Scholar
Kolb, H. & Nelson, R. (1984). Neural architecture of the cat retina. In Progress in Retinal Research, Vol. 3, ed. Osborne, N. & Chader, G., pp. 2160. Oxford: Pergamon Press.Google Scholar
Lasansky, A. (1972). Cell junctions at the outer synaptic layer of the retina. Investigative Ophthalmology 11, 265274.Google ScholarPubMed
Mariani, A.P. (1981). A diffuse, invaginating cone bipolar cell in pri-mate retina. Journal of Comparative Neurology 197, 661671.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1984a). The neuronal organization of the outer plexi-form layer of the primate retina. International Review of Cytology 86, 285320.CrossRefGoogle Scholar
Mariani, A.P. (1984ft). Bipolar cells in monkey retina selective for the cones likely to be blue-sensitive. Nature (London) 308, 184186.Google 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(9), 30453055.CrossRefGoogle ScholarPubMed
Martin, P.R. & Grünert, U. (1991). Density of bipolar cells in the macaque monkey retina. In Advances in Understanding Visual Processes: Convergence of Neurophysiological and Psychophysical Evidence, ed. Valberg, A. & Lee, B.B., Pergamon: New York (in press).Google Scholar
Mccartney, M.D. & Dickson, D.H. (1985). Photoreceptor synaptic ribbons: Three-dimensional shape, orientation and diurnal (non) variation. Experimental Eye Research 41, 313321.CrossRefGoogle ScholarPubMed
Missotten, L., Appelmans, M. & Michiels, J. (1963). L'ultra-structure des synapses des cellules visuelles de la retiné humaine. Bulletins et Mémoires de la Société Francaise d'Ophtalmologie 76, 5982.Google Scholar
Missotten, L. (1965). The Ultrastructure of the Retina. Brussels: Arscia, Uitgaven N.V.Google Scholar
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 11831195.CrossRefGoogle ScholarPubMed
Ogden, T.E. (1974). The morphology of retinal neurons of the owl monkey, Aotes. Journal of Comparative Neurology 153, 399427.CrossRefGoogle ScholarPubMed
Ogden, T.E. (1975). The receptor mosaic of Aotes trivirgatus: distribution of rods and cones. Journal of Comparative Neurology 163, 193202.CrossRefGoogle Scholar
Polyak, S.L. (1941). The Retina. Chicago, Illinois: University of Chicago Press.Google Scholar
Raviola, E. & 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
Rodieck, R.W. (1988). The primate retina. In: Comparative Primate Biology, Vol. 4, Neurosciences, ed. Steklis, H.D. And Brown, J., pp. 203278. New York: Alan R. Liss, Inc.Google Scholar
Rolls, E.T. & Cowey, A. (1970). Topography of the retina and striate cortex and its relationship to visual acuity in rhesus monkeys and squirrel monkey. Experimental Brain Research 10, 298310.CrossRefGoogle Scholar
Saito, T. (1987). Physiological and morphological differences between ON- and OFF-Center bipolar cells in the vertebrate retina. Vision Research 27, 135142.CrossRefGoogle ScholarPubMed
Schaeffer, S.F. & Raviola, E. (1978). Membrane recycling in the cone cell endings of the turtle retina. Journal of Cell Biology 79, 802825.CrossRefGoogle ScholarPubMed
Scholes, J.H. (1975). Color receptors and their synaptic connections, in the retina of a cyprinid fish. Philosophical Transactions of the Royal Society B (London) 270, 61118.Google Scholar
Schwartz, E.A. (1987). Depolarization without calcium can release γ aminobutyric acid from a retinal neuron. Science (Washington) 238, 350355.Google Scholar
Spadaro, A., De Simone, I. & Puzzolo, D. (1978). Ultrastructural data and chronobiological patterns of the synaptic ribbons in the outer plexiform layer in the retina of albino rats. Acta Anatomica 102, 365373.CrossRefGoogle ScholarPubMed
Wagner, H.-J. (1990). Retinal structure of fishes. In The Visual System of Fish, ed. Douglas, R. & Djamgoz, M.B.A., pp. 109157. London: Chapman & Hall.CrossRefGoogle Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71(2).CrossRefGoogle ScholarPubMed
Wässle, H., Grünert, U., Röhrenbeck, J. & Boycott, B.B. (1991). Retinal ganglion cell density and cortical magnification factor in the primate. Vision Research 30, 18971911.CrossRefGoogle Scholar
Webb, S.V. & Kaas, J.H. (1976). The sizes and distribution of ganglion cells in the retina of the owl monkey (Aotus trivirgatus). Vision Re-search 16, 12471254.Google ScholarPubMed
West, R.W. & Dowling, J.E. (1975). Anatomical evidence for cone and rod-like receptors in the gray squirrel, ground squirrel, and prairie dog retinas. Journal of Comparative Neurology 159, 439460.CrossRefGoogle ScholarPubMed