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Volume transmission of dopamine may modulate light-adaptive plasticity of horizontal cell dendrites in the recovery phase following dopamine depletion in goldfish retina

Published online by Cambridge University Press:  02 June 2009

Stephen Yazulla
Affiliation:
Department of Neurobiology and Behavior, SUNY, Stony Brook
Keith M. Studholme
Affiliation:
Department of Neurobiology and Behavior, SUNY, Stony Brook

Abstract

We investigated the recovery of light-adaptive spinule formation following dopamine depletion with intraocular injection of 6-hydroxydopamine (6-OHDA) and subsequent neogeneration of dopamine interplexiform cells (DA-IPC) at the marginal zone. DA-IPCs were gone by 2 weeks postinjection and appeared at the marginal zone by 6 weeks postinjection, at which time DA-IPC neurites grew toward the central retina, reaching within 0.5 mm of the central retina by 1 year. Retinas from day time, light-adapted fish at 2 weeks, 4 weeks, 3 months, and 1 year postinjection with 6-OHDA were processed for pre-embedding tyrosine hydroxylase immunoreactivity (TOH-IR) and compared to sham-injected and control retinas at the electron-microscopical (EM) level. Only 6-OHDA fish that tilted markedly toward the injected eye were used for these experiments. The tilt mimics the dorsal light reaction, indicating a 2–2.5 log unit increase in the photopic sensitivity of the 6-OHDA eye. Spinule formation was reduced by about 60% in the 2- and 4-week 6-OHDA retinas, but returned to control levels throughout the entire retina of 3-month and 1 year 6-OHDA retinas even though the central region of these retinas contained no detectable TOH-IR. Intraocular injection with 10 μM SCH 23390 (a Dl antagonist) reduced light-adaptive spinule formation by 50% both in control eyes as well as those eyes that were 3 months post 6-OHDA injected. The full return of spinule formation with only partial reinnervation of the retina with DA-IPC processes and their subsequent inhibition by SCH 23390 indicates that dopamine diffused large distances within the retina to regulate this synaptic plasticity (i.e. displayed volume transmission). Also, since all 6-OHDA injected fish displayed an increased photopic sensitivity in the injected eye when sacrificed, we suggest that horizontal cell spinules are not required for photopic luminosity coding in the outer retina.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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References

Ali, M.A. (1975). Retinomotor responses. In Vision in Fishes, ed. Ali, M.A., pp. 313355. New York: Plenum Press.Google Scholar
Baldridge, W.H., Ball, A.K. & Miller, R.G. (1989). Gap junction particle density of horizontal cells in goldfish retinas lesioned with 6-OHDA. Journal of Comparative Neurology 287, 238246.Google Scholar
Baldridge, W.H., Tomasic, S. & Ball, A.K. (1993). Effects of norepinephrine on [3H]dopamine release and horizontal cell receptive-field size in the goldfish retina. Brain Research 626, 210218.Google Scholar
Baldridge, W.H. & Ball, A.K. (1991). Background illumination reduces horizontal cell receptive-field size in both normal and 6-hydroxydo-pamine-lesioned goldfish retinas. Visual Neuroscience 7, 441450.CrossRefGoogle ScholarPubMed
Baldridge, W.H. & Ball, A.K. (1993). A new type of interplexiform cell in the goldfish retina is PNMT-immunoreactive. Neuroreport 4, 10151018.Google Scholar
Ball, A.K., Baldridge, W.H. & Fernback, T.C. (1993). Neuromodulation of pigment movement in the RPE of normal and 6-OHDA-lesioned goldfish retinas. Visual Neuroscience 10, 529540.CrossRefGoogle ScholarPubMed
Behrens, U.D., Douglas, R.H. & Wagner, H.-J. (1993). Gonado-tropin-releasing hormone, a neuropeptide of efferent projections to the teleost retina induces light-adaptive spinule formation on horizontal cell dendrites in dark-adapted preparations kept in vitro. Neuroscience Letters 164, 5962.Google Scholar
Bjelke, B., Stromberg, I., O'Connor, W.T., Andbjer, B., Agnati, L.F. & Fuxe, K. (1994). Evidence for volume transmission in the dopamine denervated neostriatum of the rat after a unilateral nigral 6-OHDA microinjection. Studies with systemic D-amphetamine treatment. Brain Research 662, 1124.Google Scholar
Djamgoz, M.B.A., Downing, J.E.G., Kirsch, M., Prince, D.J. & Wagner, H.-J. (1988). Plasticity of cone horizontal cell functioning in cyprinid fish retina: Effects of background illumination of moderate intensity. Journal of Neurocytology 17, 701710.Google Scholar
Djamgoz, M.B.A., Kirsch, M. & Wagner, H.-J. (1989). Haloperidol suppresses light-induced spinule formation and biphasic responses of horizontal cells in fish (roach) retina. Neuroscience Letters 107, 200204.Google Scholar
Djamgoz, M.B.A. & Wagner, H.-J. (1992). Invited review: Localization and function of dopamine in the adult vertebrate retina. Neuro-chemistry International 20, 139191.Google Scholar
Dong, C.-J. & McReynolds, J.S. (1991). The relationship between light, dopamine release and horizontal cell coupling in the mudpuppy retina. Journal of Physiology (London) 440, 291309.Google Scholar
Douglas, R.H., Wagner, H.-J., Zaunreiter, M., Behrens, U.D. & Djamgoz, M.B.A. (1992). The effect of dopamine depletion on light-evoked and circadian retinomotor movements in the teleost retina. Visual Neuroscience 9, 335343.Google 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 (London) 201, 726.Google Scholar
Eldred, W.D., Zucker, C., Karten, H.J. & Yazulla, S. (1983). Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. Journal of Histochemistry and Cytochemistry 31, 285292.CrossRefGoogle ScholarPubMed
Fuxe, K. & Agnati, L.F. (1991). Volume Transmission in the Brain, Novel Mechanisms for Neural Transmission. Advances In Neuroscience. Vol. I. New York: Raven Press.Google Scholar
Holst, E.V. (1935). Über den lichtrükenreflex bei fischen. Pubblicazioni delta Stazione Zoologica di Napoli 15, 143158.Google 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.Google Scholar
Kirsch, M., Wagner, H.-J. & Djamgoz, 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, 401412.CrossRefGoogle ScholarPubMed
Kohler, K., Kolbinger, W., Kurz-Isler, G. & Weiler, R. (1990). Endogenous dopamine and cyclic events in the fish retina, II: Correlation of retinomotor movement, spinule formation, and connexon density of gap junctions with dopamine activity during light/dark cycles. Visual Neuroscience 5, 417428.Google Scholar
Kohler, K. & Weiler, R. (1990). Dopaminergic modulation of transient neurite outgrowth from horizontal cells of the fish retina is not mediated by cAMP. European Journal of Neuroscience 2, 788794.Google Scholar
Lin, Z.S. (1993). Effects of dopamine depletion on the retina and visual behavior of goldfish. Ph.D. Thesis, State University of New York, Stony Brook.Google Scholar
Lin, Z.S. & Yazulla, S. (1994a). Depletion of retinal dopamine increases brightness perception in goldfish. Visual Neuroscience 11, 683693.CrossRefGoogle ScholarPubMed
Lin, Z.S. & Yazulla, S. (1994b). Depletion of retinal dopamine does not affect the ERG-b wave increment threshold function in goldfish in vivo. Visual Neuroscience 11, 695702.CrossRefGoogle ScholarPubMed
Maguire, G. & Werblin, F. (1994). Dopamine enhances a glutamategated ionic current in OFF bipolar cells of the tiger salamander retina. Journal of Neuroscience 14, 60946101.Google Scholar
Mora-Ferrer, C. & Neumeyer, C. (1994). Dopamine depletion and wavelength discrimination in goldfish. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1363.Google Scholar
Negishi, K., Teranishi, T. & Kato, S. (1982 a). Neurotoxic destruction of dopaminergic cells in the carp retina revealed by a histofluorescence study. Acta Histochemistry Cytochemistry 15, 768778.Google Scholar
Negishi, K., Teranishi, T. & Kato, S. (1982 b). New dopaminergic and indoleamine-accumulating cells in the growth zone of goldfish retinas after neurotoxic destruction. Science 216, 747749.CrossRefGoogle ScholarPubMed
Negishi, K., Teranishi, T., Kato, S. & Nakamura, Y. (1987). Paradoxical induction of dopaminergic cells following intravitreal injection of high doses of 6-hydroxydopamine in juvenile carp retina. Developmental Brain Research 33, 6779.CrossRefGoogle Scholar
Negishi, K., Teranishi, T. & Kato, K. (1990). The dopamine system of the teleost fish retina. Progress in Retinal Research 9, 148.Google Scholar
Pfeiffer, W. (1964). Equilibrium orientation in fish. In International Review of General Experimental Zoology, Vol.I, ed. Felts, W.J.L. & Harrison, R.J., pp. 77111. New York: Academic Press.Google Scholar
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1984). Decrease of gap junction permeability induced by dopamine and cyclic adenosine 3′,5′-monophosphate in the horizontal cells of turtle retina. Journal of Neuroscience 4, 24772488.CrossRefGoogle ScholarPubMed
Raynauld, J.-P., Laviolette, J.R. & Wagner, H.-J. (1979). Goldfish retina: A correlate between cone activity and morphology of the horizontal cell in cone pedicles. Science 204, 14361438.Google Scholar
Schutte, M. & Witkovsky, P. (1991). Dopaminergic interplexiform cells and centrifugal fibres in the Xenopus retina. Journal of Neurocytology 20, 195207.Google Scholar
Stell, W.K. (1967). The structure and relationships of horizontal cells and photoreceptor-bipolar synaptic complexes in goldfish retina. American Journal of Anatomy 120, 401424.Google Scholar
Umino, O. & Dowling, J.E. (1991). Dopamine release from interplexiform cells in the retina: Effects of GnRH, FMRFamide, bicuculline, and enkephalin on horizontal cell activity. Journal of Neuroscience 11, 30343046.Google Scholar
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, 503518.Google Scholar
Wagner, H.-J. (1980). Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedicles of fish retinas. Journal of Neurocytology 9, 573590.Google Scholar
Wagner, H.-J., Behrens, U.D., Zaunreiter, M. & Douglas, R.H. (1992). The circadian component of spinule dynamics in teleost retinal horizontal cells is dependent on the dopaminergic system. Visual Neuroscience 9, 345352.Google Scholar
Wagner, H.-J. & Behrens, U.D. (1993). Microanatomy of the dopaminergic system in the rainbow trout retina. Vision Research 33, 13451358.Google Scholar
Wagner, H.-J. & Wulle, I. (1992). Contacts of dopaminergic interplexiform cells in the outer retina of the blue acara. Visual Neuroscience 9, 325333.Google Scholar
Watt, C.B., Yang, S., 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, 114126.Google Scholar
Weiler, R. & Wagner, H.-J. (1984). Light-dependent change of cone-horizontal cell interactions in carp retina. Brain Research 298, 19.Google Scholar
Witkovsky, P., Eldred, W. & Karten, H.J. (1984). Catecholamine-and indoleamine-containing neurons in the turtle retina. Journal of Comparative Neurology 228, 217225.CrossRefGoogle ScholarPubMed
Witkovsky, P., Stone, S. & Tranchina, D. (1989). Photoreceptor to horizontal cell synaptic transfer in the Xenopus retina: Modulation by dopamine ligands and a circuit model for interactions of rod and cone inputs. Journal of Neurophysiology 62, 864881.Google Scholar
Witkovsky, P. & Dearry, A. (1992). Functional roles of dopamine in the vertebrate retina. Progress in Retinal Research 11, 113147.Google Scholar
Yazulla, S. & Lin, Z.-S. (1995). Differential effects of dopamine depletion on the distribution of 3H-SCH23390 and 3H-spiperone binding sites in the goldfish retina. Vision Research (in press).Google Scholar
Yazulla, S. & Zucker, C.L. (1988). Synaptic organization of dopaminergic interplexiform cells in the goldfish retina. Visual Neuro-science 1, 1330.CrossRefGoogle ScholarPubMed