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The organization of dopaminergic neurons in vertebrate retinas

Published online by Cambridge University Press:  02 June 2009

Paul Witkovsky  and
Michael Schütte
Paul Witkovsky
Affiliation:
Department of Ophthalmology, New York University Medical Center, New York Department of Physiology and Biophysics, New YorkUniversity Medical Center, New York
Michael Schütte
Affiliation:
Department of Ophthalmology, New York University Medical Center, New York
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Abstract

A survey of the shapes of dopaminergic (DA) neurons in the retinas of representative vertebrates reveals that they are divisible into three groups. In teleosts and Cebus monkey, DA cells are interplexiform (IPC) neurons with an ascending process that ramifies to create an extensive arbor in the outer plexiform layer (OPL). All other vertebrates studied, including several primate species, have either DA amacrine cells or IPCs with an ascending process that either does not branch within the OPL or does so to a very limited degree. DA neurons of non-teleosts exhibit a dense plexus of fine caliber fibers which extends in the distal most sublamina of the inner plexiform layer (IPL). Teleosts lack this plexus. In all vertebrates, DA cells are distributed more or less evenly and at a low density (10–60 cells/mm2) over the retinal surface. Dendritic fields of adjacent DA neurons overlap. Most of the membrane area of the DA cell is contained within the plexus of fine fibers, which we postulate to be the major source of dopamine release. Thus, dopamine release can be modeled as occurring uniformly from a thin sheet located either in the OPL (teleosts) or in the distal IPL (most other vertebrates) or both (Cebus monkey). Assuming that net lateral spread of dopamine is zero, the fall of dopamine concentration with distance at right angles to the sheet (i.e. in the scleral-vitreal axis) will be exponential. The factors that influence the rate of fall – diffusion in extracellular space, uptake, and transport – are not yet quantified for dopamine, hence the dopamine concentration around its target cells cannot yet be assessed. This point is important in relation to the thresholds for activation of D1 and D2 dopamine receptors that are found on a variety of retinal cells.

Keywords

RetinaDopamineTyrosine hydroxylase
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 1-2 , August 1991 , pp. 113 - 124
Copyright
Copyright © Cambridge University Press 1991

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References

Adolph, A., Dowling, J.E. & Ehinger, B. (1980). Monoaminergic neurons of the mudpuppy Retina. Cell and Tissue Research 210, 269–282.CrossRefGoogle ScholarPubMed
Besharse, J.C., Iuvone, P.M. & Pierce, M.E. (1988). Regulation of rhythmic photoreceptor metabolism: a role for post-receptoral neurons. In Progress in Retinal Research, Vol. 7, ed. Chader, G. & Osborne, N.N., pp. 21–61. New York: Pergamon Press.Google Scholar
Boatright, J.H., Hoel, M.J. & Iuvone, P.M. (1989). Stimulation of endogenous dopamine release and metabolism in amphibian retina by light- and K+-evoked depolarization. Brain Research 482, 164–168.CrossRefGoogle ScholarPubMed
Brecha, N. (1983). Retinal neurotransmitters: histochemical and biochemical studies. In Chemical Neuroanatomy, ed. Emson, P.C., pp. 85–129. New York: Raven Press.Google Scholar
Brecha, N.C., Oyster, C.W. & Takahashi, E.S. (1984). Identification and characterization of tyrosine hydroxylase-immunoreactive amacrine cells. Investigative Ophthalmology and Visual Science 25, 66–70.Google ScholarPubMed
Chang, G.D. & Ramirez, V.D. (1989). Studies of the in vivo Catabolism of exogenous dopamine as infused through a push-pull cannula implanted in the rat caudate nucleus. Brain Research 481, 265–273.Google ScholarPubMed
Cohen, A.I. & Blazynski, C. (1990). Dopamine and its agonists reduce a light-sensitive pool of cyclic AMP in mouse photoreceptors. Visual Neuroscience 4, 43–52.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1986). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas, I: Induction of cone contraction is mediated by D2 receptors. Journal of Neurochemistry 46, 1006–1021.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1988). Stimulation of distinct D2 dopaminergic and Á2-adrenergic receptors induces light-adaptive pigment dispersion in teleost retinal pigment epithelium. Journal of Neurochemistry 51, 1516–1523.CrossRefGoogle Scholar
De Vries, S.H. & Schwartz, E.A. (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. Journal of Physiology 414, 351–375.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). The Retina: An Approachable +Part of the Brain. Cambridge: Harvard University Press.Google Scholar
Dowling, J.E. & Ehinger, B. (1975). Synaptic organization of the amine-containing interplexiform cells of the goldfish and Cebus monkey retina. Science 188, 270–273.CrossRefGoogle Scholar
Dowling, J.E. & Ehinger, B. (1978). The interplexiform cell system, I: Synapses of the dopaminergic neurons of the goldfish retina. Proceedings of the royal society B (London) 201, 7–26.Google Scholar
Dowling, J.E., Ehinger, B. & Floren, I. (1980). Fluorescence and electron-microscopical observations on the amine-accumulating neurons of the Cebus monkey retina. Journal of Comparative Neurology 192, 665–685.CrossRefGoogle ScholarPubMed
Ehinger, B. (1982). Neurotransmitter systems in the retina. Retina 2, 305–321.CrossRefGoogle ScholarPubMed
Ehinger, B. & Falck, B. (1969). Adrenergic retinal neurons of some New World monkeys. Zeitschrift für Zellforschung 100, 364–375.CrossRefGoogle ScholarPubMed
Ehinger, B., Falck, B. & Laties, A.M. (1969). Adrenergic neurons in teleost retina. Zeitschrift für Zellforschung 97, 285–297.CrossRefGoogle ScholarPubMed
Engbretson, G.A. & Battelle, B.-A. (1987). Serotonin and dopamine in the retina of a lizard. Journal of Comparative Neurology 257, 140–147.CrossRefGoogle ScholarPubMed
Falck, B., Hillarp, N.-A., Thieme, G. & Torp, A. (1962). Fluorescence of catecholamines and related compounds condensed with formaldehyde. Journal of Histochemistry and Cytochemstry 10, 348–354.CrossRefGoogle Scholar
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.CrossRefGoogle Scholar
Frederick, J.M., Rayborn, M.E., Laties, A.M., Lam, D.M.K. & Hollyfield, J.G. (1982). Dopaminergic neurons in human retina. Journal of Comparative Neurology 210, 65–79.CrossRefGoogle ScholarPubMed
Furness, J.B., Costa, M. & Wilson, A.L. (1977). Water-stable fluorophores, produced by reaction with aldehyde solutions, for the histochemical localization of catechol and indoleamines. Histochemistry 52, 159–170.CrossRefGoogle Scholar
Gallego, A. (1971). Horizontal and amacrine cells in the mammal's retina. Vision Research (Suppl.) 3, 33–50.CrossRefGoogle Scholar
Gerschenfeld, H.M., Neyton, J., Piccolino, M. & Witkovsky, P. (1982). L-Horizontal cells of the turtle: network organization and coupling modulation. In Biomedical Research (Suppl.), ed. Kaneko, A., Tsukahara, N. & Uchnizono, K., pp. 21–32. Tokyo, Japan: Biomedical Research Federation.Google Scholar
HeddenW.L., Jr. W.L., Jr., & Dowling, J.E. (1978). The interplexiform cell system, II: Effects of dopamine on goldfish retinal neurones. Proceedings of the Royal Society B (London) 201, 27–51.Google Scholar
Hokoc, J.N. & Mariani, A.P. (1988). Synapses from bipolar cells onto dopaminergic amacrine cells in cat and rabbit retinas. Brain Research 461, 17–26.CrossRefGoogle Scholar
Holmgren, I. (1982). Synaptic organization of the dopaminergic neurons in the retina of the Cynomolgus monkey. Investigative ophthalmology and Visual Science 22, 8–24.Google ScholarPubMed
Holmgren-Taylor, I. (1982). Ultrastructure and synapses of the [3H]-dopamine-accumulating neurons in the retina of the rabbit. Experimental Eye Research 35, 555–572.CrossRefGoogle ScholarPubMed
Jonsson, G. (1980). Chemical neurotoxins as denervation tools in neurobiology. Annual Review of Neuroscience 3, 169–187.CrossRefGoogle ScholarPubMed
Kebabian, J. & Calne, D. (1979). Multiple receptors for dopamine. Nature 277, 93–96.CrossRefGoogle ScholarPubMed
Kirsch, M. & Wagner, H.-J. (1989). Release pattern of endogenous dopamine in teleost retinae during light adaptation and pharmacological stimulation. Vision Research 29, 147–154.CrossRefGoogle ScholarPubMed
Kolb, H., Cline, C., Wang, H.H. & Brecha, N. (1987). Distribution and morphology of dopaminergic amacrine cells in the retina of the turtle (Pseudemys scripta elegans). Journal of Neurocytology 16, 577–588.CrossRefGoogle ScholarPubMed
Kolb, H., Cuenca, N., Wang, H.H. & Dekorver, L. (1990). The synaptic organization of the dopaminergic amacrine cell in the cat retina. Journal of Neurocytology 19, 343–366.CrossRefGoogle ScholarPubMed
Kolb, H. & Wang, H.H. (1985). The distribution of photoreceptors, dopaminergic amacrine cells, and ganglion cells in the retina of the North American opossum (Didelphis virginiana). Vision Research 25, 1207–1221.CrossRefGoogle ScholarPubMed
Lasater, E.M. & Dowling, J.E. (1985). Dopamine decreases conductance of the electrical junctions between cultured retinal horizontal cells. Proceedings of the National Academy of Sciences of the U.S.A. 82, 3025–3029.CrossRefGoogle ScholarPubMed
Level, V., Gobert, A. & Guibert, B. (1989). Direct observation of dopamine compartmentation in striatal nerve terminal by “in vivo” measurement of the specific activity of released dopamine. Brain Research 499, 205–213.CrossRefGoogle Scholar
Makino-Tasaka, M., Suzuki, T., Nagai, K. & Miyata, S. (1985). Spatial distribution of visual pigment and dopamine in the bullfrog retina. Experimental Eye Research 40, 767–778.CrossRefGoogle ScholarPubMed
Makman, M.H. & Dvorkin, B. (1986). Binding Sites for [3H-SCH] 23390 in retina: properties and possible relationship to dopamine D1 receptors mediating stimulation of adenylate cyclase. Molecular Brain Research 1, 261–270.CrossRefGoogle Scholar
Makman, M.H., Dvorkin, B., Horowitz, S.G. & Thal, L.J. (1980). Properties of dopamine agonist and antagonist binding sites in mammalian retina. Brain Research 194, 403–418.CrossRefGoogle ScholarPubMed
Mariani, A.P. & Hokoc, J.N. (1988). Two types of tyrosine hydroxylase-immunoreactive amacrine cell in the rhesus monkey retina. Journal of Comparative Neurology 276, 81–91.CrossRefGoogle ScholarPubMed
Mariani, A.P., Kolb, H. & Nelson, R. (1984). Dopamine-containing amacrine cells of rhesus monkey retina parallel rods in spatial distribution. Brain Research 322, 1–7.CrossRefGoogle ScholarPubMed
McGonigle, P., Wax, M.B. & Molinoff, P.B. (1988). Characterization of binding sites for [3H]-spiroperidol in human retina. Investigative Ophthalmology and Visual Science 29, 687–694.Google ScholarPubMed
Naka, K.-I. & Sakai, H. (1985). Functional morphology of the outer plexiform layer. In Neurocircuitry of the Retina, ed. Gallego, A. & Gouras, P., pp. 141–151. New York: Elsevier.Google Scholar
Negishi, K., Kato, S. & Teranishi, T. (1982). Dopaminergic cells of the river lamprey retina revealed by a histofluorecence study. Acta of Histochemistry and Cytochemistry 15, 757–767.CrossRefGoogle Scholar
Negishi, K., Teranishi, T., Hidaka, S., Hilda, E. & Naka, K.-I. (1983). Regional difference in density of monamine-accumulating cells of carp and catfish retinas. Journal of Neuroscience Research 9, 211–222.CrossRefGoogle ScholarPubMed
Negishi, K., Teranishi, T. & Kato, S. (1990). In Progress in Retinal Research, eds. Osborne, N. & Chader, J., pp. 2–48. New York: Pergamon Press.Google Scholar
Nguyen-Legros, J., Botteri, C., Phuc, L.H., Vigny, A. & Gay, M. (1984). Morphology of primate's dopaminergic amacrine cells as revealed by TH-like immunoreactivity on retinal flatmounts. Brain Research 295, 145–153.CrossRefGoogle Scholar
Nguyen-Legros, J., Versaux-Botter, C., Vigny, A. & Raoux, N. (1985). Tyrosine hydroxylase immunohistochemistry fails to demonstrate dopaminergic interplexiform cells in the turtle retina. Brain Research 339, 323–328.CrossRefGoogle ScholarPubMed
Nicholson, C. & Hounsgaard, J. (1983). Diffusion in the slice microenvironment and implications for physiological studies. Federation Proceedings 42, 2865–2868.Google ScholarPubMed
Nicholson, C., Phillips, J.M. & Gardner-Medwin, A.R. (1979). Diffusion from an iontophoretic point source in the brain: role of tortuosity and volume fraction. Brain Research 169, 580–584.CrossRefGoogle ScholarPubMed
Oyster, C.W., Takahasi, E.S., Cilluffo, M. & Brecha, N.M. (1985). Morphology and distribution of tyrosine hydroxylase-like immunoreactive neurons in the cat retina. Proceedings of the National Academy of Sciences of the U.S.A. 82, 6335–6339.CrossRefGoogle ScholarPubMed
Piccolino, M., Demontis, G., Witkovsky, P., Strettoi, E., Cappagli, G.C., Porceddu, M.L., Demontis, M.G., Pepitoni, S., Biggio, G., Meller, E. & Bohmaker, K. (1989). Involvement of D1 and D2 dopamine receptors in the control of horizontal cell electrical coupling in the turtle retina. European Journal of Neuroscience 1, 247–257.CrossRefGoogle ScholarPubMed
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1984). Decrease of gap-junction permeability induced by dopamine and cyclic adenosine 3′:5′-monophosphate in horizontal cells of turtle retina. Journal of Neuroscience 4, 2477–2488.CrossRefGoogle ScholarPubMed
Pollard, J. & Eldred, W.D. (1990). Synaptic analysis of amacrine cells in the turtle retina which contain tyrosine hydroxylase. Journal of Neurocytology 19, 53–66.CrossRefGoogle ScholarPubMed
Porceddu, M.L., DeMontis, G., Mele, S., Ongini, E. & Biggio, G. (1987). D1 dopamine receptors in the rat retina: effect of dark adaptation and chronic blockade by SCH 23390. Brain Research 424, 264–271.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1985). A combined Golgi and autoradiographic study of [3H]-glycine-accumulating amacrine cells in the cat retina. Journal of Comparative Neurology 233, 473–480.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1987). Visualization of endogenous glycine in cat retina: an immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 1189–1197.CrossRefGoogle ScholarPubMed
Redburn, D.A., Clement-Cormier, Y. & Lam, D.M.K. (1980). Dopamine receptors in the goldfish retina: [3H]-spiroperidol and [3H]-domperidone binding; and dopamine-stimulated adenylate cyclase activity. Life Sciences 27, 23–31.CrossRefGoogle ScholarPubMed
Rice, M.E. & Nicholson, C. (1987). Interstitial ascorbate in turtle brain is modulated by release and extracellular volume change. Journal of Neurochemistry 49, 1096–1104.CrossRefGoogle ScholarPubMed
Sandell, J.H. & Masland, R.H. (1986). A system of indoleamine-accumulating neurons in the rabbit retina. Journal of Neuroscience 6, 3331–3347.CrossRefGoogle ScholarPubMed
Savy, C., Yelnik, J., Martin-Martinelli, E., Karpouzas, I. & Nguyen-Legros, J. (1989). Distribution and spatial geometry of dopamine interplexiform cells in the rat retina; I: Developing retina. Journal of Comparative Neurology 289, 99–110.CrossRefGoogle ScholarPubMed
Schütte, M. (1991). [125]-SCH 23982, a new tool for rapid visualization of dopaminergic neurons in lower vertebrate retinas. Neuroscience Letters 121, 29–33.CrossRefGoogle Scholar
Schütte, M. & Witkovsky, P. (1990). Dopaminergic interplexiform cells and centrifugal fibers in the Xenopus retina. Journal of Neurocytology 20, 195–207.CrossRefGoogle Scholar
Smiley, J.F. & Basinger, S.F. (1988). Somatostatin-like immunoreactivity and glycine high-affinity uptake colocalize to an interplexiform cell of the Xenopus laevis retina. Journal of Comparative Neurology 274, 608–618.CrossRefGoogle Scholar
Smiley, J.F. & Yazulla, S. (1990). Characterization of glycinergic contacts in the outer plexiform layer of the Xenopus laevis retina using antibodies to glycine, GABA, and glycine receptors Journal of Comparative Neurology 299, 375–388.CrossRefGoogle ScholarPubMed
Stone, S. & Witkovsky, P. (1984). The actions of γ-aminobutyric acid, glycine, and their antagonists upon horizontal cells of the Xenopus retina. Journal of Physiology 353, 249–264.CrossRefGoogle ScholarPubMed
Stoof, J.C. (1988/1989). Localization and pharmacology of some dopamine receptor complexes in the striatum and the pituitary gland: synaptic and sonsynaptic communication. Acta Morphol. Neerl, Scand. 26, 115–130.Google ScholarPubMed
Tachibana, M. & Kaneko, A. (1984). γ-aminobutyric acid acts at axonterminals of turtle photoreceptors: difference in sensitivity among cell types. Proceedings of the National Academy of Sciences of the U.S.A. 81, 7961–7964.CrossRefGoogle Scholar
Tauchi, M., Madigan, N.K. & Masland, R.M. (1990). Shapes and distributions of the catecholamine-accumulating neurons in the rabbit retina. Journal of Comparative Neurology 293, 178–189.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1983). Dopamine modulates Spotential amplitude and dye coupling between external horizontal cells in carp retina. Nature 301, 243–246.CrossRefGoogle ScholarPubMed
Törk, I. & Stone, J. (1979). Morphology of catecholamine containing amacrine cells in the cat's retina, as seen in retinal wholemounts. Brain Research 169, 261–273.CrossRefGoogle Scholar
Tornqvist, K., Yang, X.-L. & Dowling, J.E. (1988). Modulation of cone horizontal cell activity in the teleost fish retina, III: Effects of prolonged darkness and dopamine on electrical coupling between horizontal cells. Journal of Neuroscience 8, 2259–2268.CrossRefGoogle ScholarPubMed
Van Buskirk, R. & Dowling, J.E. (1981). Isolated horizontal cells from carp retina demonstrate dopamine-dependent accumulation of cyclic AMP. Proceedings of the National Academy of Sciences of the U.S.A. 78, 7825–7829.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Research 9, 49–100.CrossRefGoogle Scholar
Versaux-Botteri, C., Nguyen-Legros, J., Vigny, A. & Raoux, N. (1984). Morphology, density, and distribution of tyrosine hydroxylase-like immunoreactive cells in the retina of mice. Brain Research 301, 192–197.CrossRefGoogle ScholarPubMed
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of All amacrine cells in mammalian retina. Journal of Neuroscience 7, 4115–4128.CrossRefGoogle ScholarPubMed
Wagner, H.-J. & Wulle, I. (1990). Dopaminergic interplexiform cells contact photoreceptor terminals in catfish retina. Cell and Tissue Research 261, 359–365.CrossRefGoogle Scholar
Wässle, H., & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society B (London) 200, 441–461.Google Scholar
Watt, C.B., Yang, S.Z., Lam, D.M.K. & Wu, S.M. (1988). Localization of tyrosine-hydroxylase-like-immunoreactive amacrine cells in the larval tiger salamander retina. Journal of Comparative Neurology 272, 114–126.CrossRefGoogle ScholarPubMed
Weiler, R. & Schütte, M. (1985). Morphological and pharmacological analysis of putative serotonergic bipolar and amacrine cells in the retina of a turtle (Pseudemys scripta elegans). Cell and Tissue Research 241, 373–382.CrossRefGoogle ScholarPubMed
Witkovsky, P., Alones, V. & Piccolino, M. (1987). Morphological changes induced in turtle retinal neurons by exposure to 6-hyroxydopamine and 5,6-dihydroxytryptamine. Journal of Neurocylology 16, 55–67.Google Scholar
Witskovsky, P., Eldred, W. & Karten, H.J. (1984). Catecholamine- and indoleamine-containing neurons in the turtle retina. Journal of Comparative Neurology 228, 217–225.CrossRefGoogle Scholar
Witkovsky, P. & Shi, X.-P. (1990). Slow light and dark adaptation of horizontal cells in the Xenopus retina: a role for endogenous dopamine. Visual Neuroscience 5, 405–413.CrossRefGoogle ScholarPubMed
Witkovsky, P., Stone, S. & Besharse, J.C. (1988). Dopamine modifies the balance of rod and cone inputs to horizontal cells of the Xenopus retina. Brain Research 449, 332–336.CrossRefGoogle ScholarPubMed
Wulle, I. & Schnitzer, J. (1989). Distribution and morphology of tyrosine hydroxylase-immunoreactive neurons in the developing mouse retina. Developmental Brain Research 48, 59–72.CrossRefGoogle ScholarPubMed
Yamada, M. & Saito, T. (1988). Effects of dopamine on bipolar cells in the carp retina. Biomedical Research (Suppl.) 9, 125–130.Google Scholar
Yazulla, S. & Kleinschmidt, J. (1983). Carrier-mediated release of GABA from retinal horizontal cells. Brain Research 263, 63–75.CrossRefGoogle ScholarPubMed
Yazulla, S. & Zucker, C.L. (1988). Synaptic organization of dopaminergic interplexiform cells in the goldfish retina. Visual Neuroscience 1, 13–29.CrossRefGoogle ScholarPubMed