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Synaptic organization of dopaminergic interplexiform cells in the goldfish retina

Published online by Cambridge University Press:  02 June 2009

Stephen Yazulla  and
Charles L. Zucker
Stephen Yazulla
Affiliation:
Department of Neurobiology and Behavior, State University of New York, Stony Brook
Charles L. Zucker
Affiliation:
Department of Neurobiology and Behavior, State University of New York, Stony Brook
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Abstract

The synaptic organization of dopaminergic interplexiform cells (DA-IPC) in the goldfish retina was studied by a combined double-label electron-microscopical (EM) immunocytochemical/autoradiographical study. DA-IPCs were labeled with antisera against tyrosine hydroxylase. The possibility of synaptic contact with GABAergic amacrine cells in the proximal inner plexiform layer (IPL) was studied by using 3H-GABA uptake. Most synaptic input and output from DA-IPC processes involved amacrine cell processes. In addition, synaptic interactions were observed between DA-IPC processes and bipolar cell terminals, other DA-IPC processes, very small dendrites in the IPL, ganglion cell and optic fiber layers (OFL), and cell bodies in the ganglion cell layer (GCL). Input and output synapses with GABAergic amacrine processes also were observed. Two-thirds of the DA-IPC boutons in the proximal IPL were involved in “junctional appositions,” that is, the junctions appeared to be specialized but they were different than classical chemical synapses. The synaptic organization of DA-IPCs in the goldfish IPL appears to be far more complex than previously thought. Although earlier studies have attempted to explain the action of dopamine in terms of interaction only with amacrine cells, the present study shows that effects involving bipolar cells, other DA-IPCs, unidentified processes and cell bodies in the GCL and OFL must be considered as well.

Keywords

GoldfishRetinaDopamineSynapsesImmunocytochemistry
Type
Research Articles
Information
Visual Neuroscience , Volume 1 , Issue 1 , January 1988 , pp. 13 - 29
Copyright
Copyright © Cambridge University Press 1988

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References

Ayoub, G.S. & Lam, D.M.K. (1984). The release of γ-aminobutyric acid from horizontal cells of the goldfish (Carassius auratus) retina. Journal of Physiology 355, 191–214.CrossRefGoogle ScholarPubMed
Ball, A.K. & Brandon, C. (1986). Localization of 3H-GABA, 3H-muscimol, and 3H-glycine uptake in goldfish retinas stained for glutamate decarboxylase. Journal of Neuroscience 6, 1221–1227.CrossRefGoogle ScholarPubMed
Ball, A.K. & St. Denis, J. (1986). Displaced GABAergic amacrine cells in the ganglion cell layer of the goldfish retina. Investigative Ophthalmology and Visual Science (Suppl.) 27, 332.Google Scholar
Beaudet, A. & Descarries, L. (1978). The monoamine innervation of rat cerebral cortex: synaptic and nonsynaptic terminals. Neuroscience 3, 851–860.CrossRefGoogle ScholarPubMed
Cohen, J. & Dowling, J.E. (1983). The role of the retinal interplexiform cell: effects of 6-hydroxydopamine on the spatial properties of carp horizontal cells. Brain Research 264, 307–310.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1986 a). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas. 1. Induction of contraction is mediated by D-2 receptors. Journal of Neurochemistry 46, 1006–1021.CrossRefGoogle Scholar
Dearry, A. & Burnside, B. (1986 b). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas. II. Modulation by gamma-aminobutyric acid and serotonin. Journal of Neurochemistry 46, 1022–1031.CrossRefGoogle ScholarPubMed
Dismukes, K. (1977). New look at the aminergic nervous system. Nature 269, 557–558.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 201, 7–26.Google Scholar
Dowling, J.E., Ehinger, B. & Hedden, W.L. (1976). The interplexiform cell: a new type of retinal neuron. Investigative Ophthalmology 15, 916–926.Google Scholar
Dowling, J.E., Ehinger, B. & Floren, I. (1980). Fluorescence and electron microscopical observations of the amine-accumulating neurons of the Cebus monkey retina. Journal of Comparative Neurology 192, 665–685.CrossRefGoogle ScholarPubMed
Ehinger, B., Falck, B. & Larties, A.M. (1969). Adrenergic neurons in teleost retina. Zeitschrift für Zellforschung und Mikroskopische Anatomie 97, 285–297.CrossRefGoogle ScholarPubMed
Eldred, W.D., Zucker, C, Karten, H.J. & Yazulla, S. (1983). Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. Journal Histochemistry and Cytochemistry 31, 285–292.CrossRefGoogle ScholarPubMed
Hayashi, T. (1980). Histochemical localization of dopamine and acetylcholinesterase activity in the carp retina. Acta Histochemica Cytochemica 13, 330–342.CrossRefGoogle Scholar
Hedden, W.L. & Dowling, J.E. (1978). The interplexiform cell system. II. Effects of dopamine on goldfish retinal neurons. Proceedings of the Royal Society B 201, 27–55.Google Scholar
Hokoc, J.N. & Mariani, A.P. (1987). Tyrosine hydroxylase immunoreactivity in the rhesus monkey retina reveals synapses from bipolar cells to dopaminergic amacrine cells. Journal of Neuroscience 7, 2785–2793.CrossRefGoogle ScholarPubMed
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
Ishida, A.T., Stell, W.K. & Lightfoot, D.O. (1980). Rod and cone inputs to bipolar cells in goldfish retina. Journal of Comparative Neurology 191, 315–335.CrossRefGoogle ScholarPubMed
Joh, T.H., Geghman, C. & Reis, D. (1973). Immunocytochemical demonstration of increased accumulation of tyrosine hydroxylase protein in sympathetic ganglia and adrenal medulla elicited by reserpine. Proceedings of the National Academy of Sciences of the U.S.A. 70, 2767.CrossRefGoogle Scholar
Mangel, S.C. & Dowling, J.E. (1985). Responsiveness and receptive field size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science 229, 1107–1109.CrossRefGoogle ScholarPubMed
Marc, R.E. (1982). Spatial organization of neurochemically classified interneurons of the goldfish retina. I. Local patterns. Vision Research 22, 589–608.CrossRefGoogle ScholarPubMed
Marc, R.E., Stell, W.K., Bok, D. & Lam, D.M.K. (1978). GABAergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221–246.CrossRefGoogle ScholarPubMed
Negishi, K. (1981). Density of retinal catecholamine-accumulating cells in different sized goldfish. Experimental Eye Research 33, 223–232.CrossRefGoogle ScholarPubMed
Negishi, K. & Drujan, B.D. (1978). Effects of catecholamines on the horizontal cell membrane potential in the fish retina. Sensory Processes 2, 388–395.Google ScholarPubMed
Negishi, K. & Druian, B.D. (1979 a). Reciprocal changes in center and surrounding S potentials of fish retina in response to dopamine. Neurochemical Research 4, 313–318.CrossRefGoogle ScholarPubMed
Negishi, K. & Drujan, B.D. (1979 b). Similarities in effects of acetylcholine and dopamine on horizontal cells in the fish retina. Journal of Neuroscience Research 4, 335–349.CrossRefGoogle ScholarPubMed
Negishi, K., Drujan, B.D. & Laufer, M. (1980). Spatial distribution of catecholaminergic cells in the fish retina. Journal of Neuroscience Research 5, 621–635.CrossRefGoogle ScholarPubMed
Negishi, K., Teranishi, T. & Kato, S. (1983). A GABA antagonist, bicuculline, exerts its uncoupling action on external horizontal cells through dopamine cells in carp retina. Neuroscience Letters 37, 261–266.CrossRefGoogle ScholarPubMed
O'Brien, D.R. & Dowling, J.E. (1985). Dopaminergic regulation of GABA release from the intact goldfish retina. Brain Research 360, 41–50.CrossRefGoogle ScholarPubMed
O'Connor, P., Dorison, S.J., Watling, K.J. & Dowling, J.E. (1986). Factors affecting release of 3H-dopamine from perfused carp retina. Journal of Neuroscience 6, 1857–1865.CrossRefGoogle ScholarPubMed
O'Conner, P., Zucker, C.L. & Dowling, J.E. (1987). Regulation of dopamine release from interplexiform cell processes in the outer plexiform layer of carp retina. Journal of Neurochemistry 49, 916–920.CrossRefGoogle Scholar
Saito, T. & Kujiraoka, T. (1982). Physiological and morphological identification of two types of on-center bipolar cells in the carp retina. Journal of Comparative Neurology 205, 161–170.CrossRefGoogle ScholarPubMed
Sarthy, P.V. & Lam, D.M.K. (1979). The uptake and release of [3H]dopamine in the goldfish retina. Journal of Neurochemistry 32, 1269–1277.CrossRefGoogle ScholarPubMed
Stell, W.K. (1976). Functional polarization of horizontal cell dendrites in goldfish retina. Investigative Ophthalmology 15, 895–908.Google Scholar
Stell, W.K. (1985). Putative peptide transmitters, amacrine cell diversity and function in the inner plexiform layer. In Neurocircuitry of the Retina: A Cajal Memorial, ed. Gallego, A. & Gouras, P., pp. 171–187. Amsterdam, The Netherlands: Elsevier Press.Google Scholar
Stell, W.K., Ishida, A.T. & Lightfoot, D.O. (1977). Structural basis for on- and off-center responses in retinal bipolar cells. Science 198, 1269–1271.CrossRefGoogle ScholarPubMed
Stell, W.K., Walker, S.E., Chohan, K.S. & Ball, A.K. (1984). Goldfish nervus terminalis, a luteinizing hormone —releasing hormone and molluscan cardioexcitatory peptide immunoreactive olfactoretinal pathway. Proceedings of the National Academy of Sciences of the U.S.A. 82, 940–944.CrossRefGoogle Scholar
Teranishi, T., Negishi, K. & Kato, S. (1983). Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature 301, 243–246.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1984). Regulatory effect of dopamine on spatial properties of horizontal cells in carp retina. Journal of Neuroscience 4, 1271–1280.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
Witkovsky, P. & Dowling, J.E. (1969). Synaptic relationships in the plexiform layers of the carp retina. Zeitschrift für Zellforschung und Mikroskopishe Anatomie 100, 60–82.CrossRefGoogle ScholarPubMed
Yamada, T., Marshak, D., Basinger, S., Walsh, J., Morley, J. & Stell, W.K. (1980). Somatostatin-like immunoreactivity in the retina. Proceedings of the National Academy of Sciences of the U.S.A. 77, 1691–1695.CrossRefGoogle ScholarPubMed
Yazulla, S. (1981). GABAergic synapses in the goldfish retina: an autoradiographic study of 3H-muscimol and 3H-GABA binding. Journal of Comparative Neurology 200, 83–93.CrossRefGoogle ScholarPubMed
Yazulla, S. (1985). Evoked efflux of 3H-GABA from goldfish retina in the dark. Brain Research 325, 171–180.CrossRefGoogle Scholar
Yazulla, S. & Kleinschmidt, J. (1982). Dopamine blocks carriermediated release of GABA from retinal horizontal cells. Brain Research 233, 211–215.CrossRefGoogle ScholarPubMed
Yazulla, S., Studholme, K.M. & Zucker, C.L. (1985). Synaptic organization of substance P-like immunoreactive amacrine cells in goldfish retina. Journal of Comparative Neurology 231, 232–238.CrossRefGoogle ScholarPubMed
Yazulla, S., Studholme, K. & Wu, J.-Y. (1986). Comparative distribution of 3H-GABA uptake and GAD immunoreactivity in goldfish retinal amacrine cells: a double-label analysis. Journal of Comparative Neurology 244, 149–162.CrossRefGoogle ScholarPubMed
Yazulla, S., Studholme, K.M. & Wu, J.-Y. (1987). GABAergic input to mb1 bipolar cells in the goldfish retina. Brain Research 411, 400–405.CrossRefGoogle ScholarPubMed
Zucker, C. & Yazulla, S. (1982). Localization of synaptic and nonsynaptic nicotinic-cholinergic receptors in the goldfish retina. Journal of Comparative Neurology 204, 188–195.CrossRefGoogle ScholarPubMed
Zucker, C.L. & Dowling, J.E. (1987). Centrifugal fibres on dopaminergic interplexiform cells in the teleost retina. Nature 330, 166–168.CrossRefGoogle ScholarPubMed