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The occurrence of dopaminergic interplexiform cells correlates with the presence of cones in the retinae of fish

Published online by Cambridge University Press:  02 June 2009

Eleonore Fröhlich ,
Koroku Negishi  and
Hans-Joachim Wagner
Eleonore Fröhlich
Affiliation:
Anatomisches Institut der Eberhard-Karls-Universität, österbergstr. 3, D-72074 Tübingen, Germany
Koroku Negishi
Affiliation:
Department of Anatomy, Nippon Medical School, Tokyo, Japan
Hans-Joachim Wagner
Affiliation:
Anatomisches Institut der Eberhard-Karls-Universität, österbergstr. 3, D-72074 Tübingen, Germany
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Abstract

Using light-microscopic immunocytochemistry against tyrosine hydroxylase, we have investigated the morphology of dopaminergic cells in 23 species of fishes representing various systematic classes and subclasses and which live in very different habitats. We have, for the first time, observed teleosts with dopaminergic amacrine cells. Thus, in both bony and cartilaginous fishes, dopaminergic cells are differentiated as interplexiform and amacrine cells. The differentiation of dopaminergic cells into amacrine or interplexiform cells in fishes correlates with the absence or presence of cones. In pure-rod retinae, they occur as amacrine cells, and in mixed rod/cone retinae, they occur as interplexiform cells. We conclude therefore that the differentiation of retinal dopaminergic cells in fish does not depend on the evolutionary or systematic classification of a given species. Rather, it is correlated with the occurrence of rods and/or cones, and thus linked more closely to the habitat. We argue that, in fish, the presence of cones and cone-specific horizontal cells may be responsible for inducing dopaminergic cells to differentiate as interplexiform cells. Possible functions of dopamine in all-rod retinae, which may not require adaptation, may include neuromodulation in the inner plexiform layer for the sensitization of the rod pathway, the shaping of biological rhythms, and the control of eye growth.

Keywords

DopamineAmacrine cellsInterplexiform cellsAll-rod retinaeDuplex retinaeFish retina
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 2 , March 1995 , pp. 359 - 369
Copyright
Copyright © Cambridge University Press 1995

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References

Besharse, J.C., Iuvone, P.M. & Pierce, M.E. (1988). Regulation of rhythmic photoreceptor metabolism: A role for post-receptoral neurons. Progress in Retinal Research 7, 21–61.CrossRefGoogle Scholar
Brunken, W.J., Witkovsky, P. & Karten, H.J. (1986). Retinal neurochemistry of three elasmobranch species: An immunohistochemical approach. Journal of Comparative Neurology 243, 1–12.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1986). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas: 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 (α2)-adrenergic receptors induces light-adaptive pigment dispersion in teleosts retinal pigment epithelium. Journal of Neurochemistry 51, 1516–1523.CrossRefGoogle Scholar
De Miouel, E. & Wagner, H.-J. (1990). Tyrosine hydroxylase immu-noreactive interplexiform cells in the lamprey retina. Neuroscience Letters 113, 151–155.CrossRefGoogle Scholar
Djamgoz, M.B.A. & Wagner, H.-J. (1992). Localization and function of dopamine in the adult vertebrate retina. Neurochemistry International 2, 139–191.CrossRefGoogle Scholar
Diamgoz, M.B.A., Wagner, H.-J. & Witkovsky, P. (1995). Photo-receptor-horizontal cell connectivity, synaptic transmission and neuromodulation. In Neurobiology and Clinical Aspects of the Outer Retina, ed. Diamgoz, M.B.A., Archer, S.N. & Vaileroa, S., London: Chapman and Hall (in press).CrossRefGoogle Scholar
Dowling, J.E. & Emincer, 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
Gallego, A. (1971). Cellules interplexiformes en la retina de gato. Archivos de la Sociedad espanola de oftalmologia Madrid 31, 299–304.Google Scholar
Gallego, A. (1985). Advances in horizontal cell terminology since Cajal. In Neurocircuitry of the Retina. A Cajal Memorial, ed. Gallego, A. & Gouras, P., pp. 122–140. New York, Amsterdam, Oxford: Elsevier.Google Scholar
Hampson, E., Vaney, D. & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. Journal of Neuroscience 12, 4911–4922.CrossRefGoogle ScholarPubMed
Hatakenata, S., Kiyama, H., Tohyama, M. & Miki, N. (1985). Immunohistochemical localization of chick retinal 24 kDa protein (visinin) in various vertebrate retina. Brain Research 331, 209–215.CrossRefGoogle Scholar
Kirsch, M., Wagner, H.-J. & Diamgoz, M.B.A. (1991). Dopamine and plasticity of horizontal cell function in the teleost retina: Regulation of a spectral mechanism through D1-receptors. Vision Research 31, 401–412.CrossRefGoogle ScholarPubMed
Knapp, A. & Dowling, J.E. (1987). Dopamine enhances excitatory amino acid-gated conductances in retinal horizontal cells. Nature 325, 437–439.CrossRefGoogle ScholarPubMed
Kretz, R., Ishida, A. & Stell, W.K. (1982). Ratfish retina-intracellular recordings and HRP injections in an isolated superfused all-rod retina. Vision Research 22, 857–861.CrossRefGoogle Scholar
Locket, A. (1977). Adaptations to the deep-sea environment. In Handbook of Sensory Physiology, Vol. VII/5: The Visual System of Vertebrates, ed. Crescitelli, F., pp. 67–192. Heidelberg: Springer Verlag.CrossRefGoogle Scholar
Munk, O. (1981). On the cones of the mesopelagic teleost Trachipterus trachypterus (Gmelin, 1789). Videnskabelige Meddelelser fra Dansk naturhistorisk Forening 143, 101–111.Google Scholar
Munk, O. (1965). Osmosudis lowei Guenther, 1887 a bathypelagic deep-sea fish with an almost pure-cone retina. Videnskabelige Meddelelser fra Dansk naturhistorisk Forenin 128, 341–355.Google Scholar
Munk, O. (1982). Cones in the eye of the deep-sea teleost Diretmus argenteus C. Vision Research 22, 179–181.CrossRefGoogle Scholar
Negishi, K., Kiyama, H., Kato, S., Teranishi, T., Hatakenata, S., Katayama, Y., Miki, N. & Tohyama, M. (1986). An immunohistochemical study on the river lamprey retina. Brain Research 362, 389–393.CrossRefGoogle Scholar
Negishi, K., Teranishi, T., Kuo, C.-H. & Miki, N. (1987). Two types of lamprey retina photoreceptors immunoreactive to rod-or conespecific antibodies. Vision Research 27, 1237–1241.CrossRefGoogle ScholarPubMed
Negishi, K., Kato, S. & Teranishi, T. (1989). The dopamine system in fish retina: Histochemical, pharmacological and neurochemical approaches. In Neurology and Neurobiology, Vol. 49: Extracellular and Intracellular Messengers in the Vertebrate Retina, ed. Redburn, D.A. & Pasantes-Morales, H., pp. 207–228. New York, Amsterdam, Oxford: Elsevier.Google Scholar
Nguyen-Legros, J. (1988). Morphology and distribution of catecho-lamine-neurons in mammalian retina. Progress in Retinal Research 7, 113–147.CrossRefGoogle Scholar
Qian, H., Malchow, R. & Ripps, H. (1993). Gap-junctional properties of electrically coupled skate horizontal cells in culture. Visual Neuroscience 10, 287–295.CrossRefGoogle ScholarPubMed
Rohrer, B., Spira, A. & Stell, W.K. (1993). Apomorphine blocks form deprivation myopia in chickens by a dopaminergic D2 receptor mechanism acting in retina or pigmented epithelium. Visual Neuroscience 10, 447–453.CrossRefGoogle ScholarPubMed
Stell, W.K. (1972). The structure and morphologic relations of rods and cones in the retina of the spiny dogfish, Squalus. Comparative Biochemistry and Physiology 42A, 141–151.CrossRefGoogle Scholar
Stell, W.K. & Lightfoot, D.O. (1975). Colour specific interconnections of cones and horizontal cell dendrites in the retina of the goldfish. Journal of Comparative Neurology 159, 473–502.CrossRefGoogle ScholarPubMed
Teranishi, T. & Negishi, K. (1983). Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature 301, 243–246.CrossRefGoogle ScholarPubMed
Toyoda, J.-I., Saito, T. & Kondo, H. (1978). Three types of horizontal cells in the stingray retina: Their morphology and physiology. Journal of Comparative Neurology 179, 569–580.CrossRefGoogle ScholarPubMed
Van Haesendonck, E., Marc, R.E. & Missotten, L. (1993). New aspects of dopaminergic interplexiform cell organization in the goldfish retina. Journal of Comparative Neurology 333, 503–518.CrossRefGoogle ScholarPubMed
Wagner, H.-J. & Behrens, U.D. (1993). Microanatomy of the dopaminergic system in the rainbow trout retina. Vision Research 33, 1345–1358.CrossRefGoogle ScholarPubMed
Wagner, H.-J. & Diamgoz, M.B.A. (1993). Spinules: A case for retinal synaptic plasticity. Trends in Neuroscience 16, 201–206.CrossRefGoogle ScholarPubMed
Wagner, H.-J., Wulle, I., Meerfeld, N. & Wewetzer, K. (1991). Characterization of a GABAergic population of interstitial amacrine cells in the teleost retina. Vision Research 31, 1489–1500.CrossRefGoogle ScholarPubMed
Wagner, H.-J., Luo, B., Ariano, M., Sibley, D. & Stell, W.K. (1993 a). Localization of D2 dopamine receptors in vertebrate retinae with anti-peptide antibodies. Journal of Comparative Neurology 331, 469–481.CrossRefGoogle ScholarPubMed
Wagner, H.-J., Kirsch, M. & Douglas, R.H. (1993 b). Light-dependent and endogenous circadian control of adaptation in teleost retinae. In Rhythms in Fishes, ed. Ali, M.A., pp. 255–291. New York: Plenum Press.Google Scholar
Weiler, R. & Wagner, H.-J. (1984). Light-dependent change of cone-horizontal cell interactions in carp retina. Brain Research 298, 1–9.CrossRefGoogle ScholarPubMed
Whitehead, P., Bauchot, M.-L., Hureau, J.-C., Nielson, J. & Tortonese, E. (1984). Fishes of the North-Eastern Atlantic and the Mediterranean, Vol. I. Paris, France: Unesco.Google Scholar
Whitehead, P., Bauchot, M.-L., Hureau, J.-C., Nielson, J. & Tortonese, E. (1986). Fishes of the North-Eastern Atlantic and the Mediterranean, Vol. II. Paris, France: Unesco.Google Scholar
Witkovsky, P. & Dearry, A. (1992). Functional roles of dopamine in the vertebrate retina. In Progress in Retinal Research, Vol. II, pp. 247–290. Oxford: Pergamon Press.Google Scholar
Yamagata, K., Goto, K., Kuo, C.-H., Kondo, H. & Miki, N. (1990). Visinin: A novel calcium binding protein expressed in retinal cone cells. Neuron 2, 469–476.CrossRefGoogle Scholar
Yasui, S., Yamada, M. & Djamgoz, M.B.A. (1990). Dopamine and 2-amino-4-phosphonobutyrate differentially modify spectral responses of H1 horizontal cells in carp retina. Experimental Brain Research 83, 79–84.CrossRefGoogle ScholarPubMed
Zucker, C.L. & Dowling, J.E. (1987). Centrifugal fibres synapse on dopaminergic interplexiform cells in the teleost retina. Nature 330, 166–168.CrossRefGoogle ScholarPubMed