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Depletion of retinal dopamine does not affect the ERG b-wave increment threshold function in goldfish in vivo

Published online by Cambridge University Press:  02 June 2009

Zheng-Shi Lin  and
Stephen Yazulla
Zheng-Shi Lin
Affiliation:
Department of Neurobiology and Behavior, University at Stony Brook, Stony Brook
Stephen Yazulla
Affiliation:
Department of Neurobiology and Behavior, University at Stony Brook, Stony Brook
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Abstract

Increment threshold functions of the electroretinogram (ERG) b–wave were obtained from goldfish using an in vivo preparation to study intraretinal mechanisms underlying the increase in perceived brightness induced by depletion of retinal dopamine by 6–hydroxydopamine (6–OHDA). Goldfish received unilateral intraocular injections of 6–OHDA plus pargyline on successive days. Depletion of retinal dopamine was confirmed by the absence of tyrosine-hydroxylase immunoreactivity at 2 to 3 weeks postinjection as compared to sham-injected eyes from the same fish. There was no difference among normal, sham-injected or 6–OHDA-injected eyes with regard to ERG waveform, intensity-response functions or increment threshold functions. Dopamine-depleted eyes showed a Purkinje shift, that is, a transition from rod-to-cone dominated vision with increasing levels of adaptation. We conclude (1) dopamine-depleted eyes are capable of photopic vision; and (2) the ERG b–wave is not diagnostic for luminosity coding at photopic backgrounds. We also predict that (1) dopamine is not required for the transition from scotopic to photopic vision in goldfish; (2) the ERG b–wave in goldfish is influenced by chromatic interactions; (3) horizontal cell spinules, though correlated with photopic mechanisms in the fish retina, are not necessary for the transition from scotopic to photopic vision; and (4) the OFF pathway, not the ON pathway, is involved in the action of dopamine on luminosity coding in the retina.

Keywords

GoldfishERGIncrement thresholdLight adaptationDopamine
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 4 , July 1994 , pp. 695 - 702
Copyright
Copyright © Cambridge University Press 1994

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References

Beudet, L., Browman, H.I. & Hawryshyn, C.W. (1993). Optic nerve responses and retinal structure in rainbow trout of different sizes. Vision Research 33, 1739–1746.CrossRefGoogle Scholar
Buelow, N.F., Kelly, M.E. & Barlow, R.B. Jr. (1992). Dopamine: A circadian modulator of rod-cone dominance in quail? Investigative Ophthalmology and Visual Science (Suppl.) 33, 1406.Google Scholar
Burkhardt, D.A. (1968). Cone action spectra: Evidence from the goldfish electroretinogram. Vision Research 8, 839–854.CrossRefGoogle ScholarPubMed
Citron, M., Erinoff, L., Rickman, D.W. & Brecha, N.C. (1985). Modification of electroretinograms in dopamine-depleted retinas. Brain Research 345, 186–191.CrossRefGoogle ScholarPubMed
DeMarco, P.J. Jr. & Powers, M.K. (1991). Spectral sensitivity of ON and OFF responses from the optic nerve of goldfish. Visual Neuro science 6, 207–218.CrossRefGoogle 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, 200–204.CrossRefGoogle ScholarPubMed
Djamgoz, M.B.A. & Wagner, H.-J. (1992). Invited review: Localization and function of dopamine in the adult vertebrate retina. Neurochemistry International 20, 139–191.CrossRefGoogle Scholar
Dowling, J.E. & Eknger, 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
Falzett, M., Nussdorf, J.D. & Powers, M.K. (1988). Responsivity and absolute sensitivity of retinal ganglion cells in goldfish of different sizes when measured under “psychophysical” conditions. Vision Research 28, 233–239.CrossRefGoogle ScholarPubMed
Gurevich, L. & Slaughter, M.M. (1993). Comparison of the wave forms of the On bipolar neuron and the b–wave of the electroretinogram. Vision Research 33, 2431–2435.CrossRefGoogle Scholar
Gutierrez, C.O. & Spiguel, R.D. (1973). Oscillatory potentials of the cat retina: Effects of adrenergic drugs. Life Sciences 13, 991–999.Google ScholarPubMed
Hempel, F.G. (1972). Modification of the rabbit electroretinogram by reserpine. Ophthalmic Research 4, 65–75.CrossRefGoogle Scholar
Kaneko, A. & Tachibana, M. (1981). Retinal bipolar cells with double color-opponent receptive fields. Nature 293, 220–222.CrossRefGoogle Scholar
Kaneko, A. & Tachibana, M. (1983). Double color-opponent receptive fields of carp bipolar cells. Vision Research 23, 381–388.CrossRefGoogle ScholarPubMed
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 Tissue Research 260, 123–130.CrossRefGoogle Scholar
Kline, R.P., Ripps, H. & Dowling, J.E. (1978). Generation of b–wave currents in the skate retina. Proceedings of the National Academy of Sciences of the U.S.A. 75, 5727–5731.CrossRefGoogle ScholarPubMed
Knapp, A.G. & Dowling, J.E. (1987). Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature 325, 437–438.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, 417–428.CrossRefGoogle ScholarPubMed
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, 788–794.CrossRefGoogle Scholar
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
Lin, Z.S. & Yazulla, S. (1994). Depletion of retinal dopamine increases brightness perception in goldfish. Visual Neuroscience 11, 683–693.CrossRefGoogle ScholarPubMed
Maguire, G.W. & Smith, E.L. III. (1985). Cat retinal ganglion cell receptive-field alterations after 6–hydroxydopamine induced dopaminergic amacrine cell lesions. Journal of Neurophysiology 53, 1431–1443.CrossRefGoogle ScholarPubMed
Malchow, R.P. & Yazulla, S. (1986). Separation and light adaptation of rod and cone signals in the retina of the goldfish. Vision Research 26, 1655–1666.CrossRefGoogle ScholarPubMed
Malchow, R.P. & Yazulla, S. (1988). Light adaptation of rod and cone luminosity horizontal cells of the retina of the goldfish. Brain Research 443, 222–230.CrossRefGoogle ScholarPubMed
Malmpors, T. (1963). Evidence of adrenergic neurons with synaptic terminals in the retina of rats demonstrated with fluorescence and electron microscopy. Acta Physiologica Scandinavia 58, 99–100.CrossRefGoogle Scholar
Miller, R.F. & Dowling, J.E. (1970). Intracellular responses of the Müller (glial) cells of the mudpuppy retina: Their relation to the b–wave of the electroretinogram. Journal of Neurophysiology 33, 323–341.CrossRefGoogle Scholar
Mills, S.L. & Sperling, H.G. (1990). Red/green opponency in the rhesus macaque ERG spectral sensitivity is reduced by bicuculline. Visual Neuroscience 5, 217–221.CrossRefGoogle ScholarPubMed
Mora-Ferrer, C. & Neumeyer, C. (1993). Reduced red-green discrimination in goldfish after application of dopamine antagonists. Investigative Ophthalmology and Visual Science (Suppl.) 34, 752.Google Scholar
Müller, F., Wässle, H. & Voigt, T. (1988). Pharmacological modulation of rod pathway in the cat retina. Journal of Neurophysiology 59, 1657–1672.CrossRefGoogle ScholarPubMed
Naka, K.I. & Rushton, W.A.H. (1966). An attempt to analyse colour reception by electrophysiology. Journal of Physiology 185, 556–586.CrossRefGoogle ScholarPubMed
Naarendorp, F., Hitchcock, P.F. & Sieving, P.A. (1993). Dopaminergic modulation of rod pathway signals does not affect the scotopic ERG of cat at dark-adapted threshold. Journal of Neurophysiology 70, 1681–1691.CrossRefGoogle Scholar
Negishi, K., Teranishi, T. & Kato, S. (1982). New dopaminergic and indoleamine-accumulating cells in the growth zone of goldfish retinas after neurotoxic destruction. Science 216, 747–749.CrossRefGoogle ScholarPubMed
Negishi, K., Teranishi, T. & Kato, K. (1990). The dopamine system of the teleost fish retina. Progress in Retinal Research 9, 1–48.CrossRefGoogle Scholar
Nussdorf, J.D. & Powers, M.K. (1988). Spectral sensitivity of the electroretinogram b–wave in dark-adapted goldfish. Visual Neuroscience 1, 159–168.CrossRefGoogle ScholarPubMed
Ogden, T.E. (1973). The oscillatory wave of the primate electroretinogram. Vision Research 13, 1059–1074.CrossRefGoogle Scholar
Pfeiffer, W. (1964). Equilibrium orientation in fish. In International Review of General Experimental Zoology; Vol. 1, ed. Felts, W.J.L. & Harris, R.J., pp. 77–111. New York: Academic Press.Google Scholar
Powers, M.K. (1978). Light-adapted spectral sensitivity of the goldfish: A reflex measure. Vision Research 18, 1131–1136.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, 1436–1438.CrossRefGoogle Scholar
Sillman, A.J., Ito, H. & Tomtta, T. (1969). Studies on the mass receptor potential of the isolated frog retina. I. General properties of the response. Vision Research 9, 1435–1442.CrossRefGoogle ScholarPubMed
Silver, P.H. (1974). Photopic spectral sensitivity of the neon tetra (Paracheirodon innesi (Meyers)) found by the use of a dorsal light reaction. Vision Research 14, 329–334.CrossRefGoogle Scholar
Sperling, H.G. & Mills, S.L. (1987). ERG and behavioral analysis of spectral sensitivity in normal and blue-blind rhesus monkeys. In Color Vision Deficiencies, VIII, ed. Verriest, G., pp. 365–374. Dordrecht, Netherlands: Nihoff/Junk Publishers.Google Scholar
Stockton, R.A. & Slaughter, M.M. (1989). B–wave of the electroretinogram: A reflection of ON bipolar cell activity. Journal of General Physiology 93, 101–122.CrossRefGoogle ScholarPubMed
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 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
Wachtmeister, L. & Dowling, J.E. (1978). The oscillatory potentials of the mudpuppy retina. Investigative Ophthalmology and Visual Science 17, 1176–1188.Google ScholarPubMed
Wagner, H.-J. (1980). Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedicles of fish retinas. Journal of Neurocytology 9, 573–590.CrossRefGoogle ScholarPubMed
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, 345–352.CrossRefGoogle ScholarPubMed
Wagner, H.-J., Luo, B.-G., Ariano, M.A., Sibley, D.R. & Stell, W.K. (1993). Localization of D2 dopamine receptors in vertebrate retinae with anti-peptide antibodies. Journal of Comparative Neurology 331, 469–481.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
Weiler, R., Kohler, K., Kirsch, M. & Wagner, H.-J. (1988). Glutamate and dopamine modulate synaptic plasticity in horizontal cell dendrites of fish retina. Neuroscience Letters 87, 205–209.CrossRefGoogle ScholarPubMed
Weiler, R., Kohler, K. & Janssen, U. (1991). Protein kinase C mediates transient spinule-type neurite outgrowth in the retina during light adaptation. Proceedings of the National Academy of Sciences of the U.S.A. 88, 3603–3607.CrossRefGoogle ScholarPubMed
Weiler, R. & Wagner, H.J. (1984). Light-dependent changes of cone horizontal cell interactions in carp retina. Brain Research 298, 1–9.CrossRefGoogle ScholarPubMed
Wheeler, T.G. (1979). Retinal ON and OFF responses convey different chromatic information to the CNS. Brain Research 160, 145–149.CrossRefGoogle ScholarPubMed
Witkovsky, P. (1967). A comparison of ganglion cell and S-potential response properties in carp retina. Journal of Neurophysiology 30, 546–561.CrossRefGoogle ScholarPubMed
Witkovsky, P. (1968). The effect of chromatic adaptation on color sensitivity of the carp electroretinogram. Vision Research 8, 823–838.CrossRefGoogle ScholarPubMed
Witkovsky, P., Dudek, F.E. & Ripps, H. (1975). Slow PIII component of the carp electroretinogram. Journal of General Physiology 65, 119–134.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, 864–881.CrossRefGoogle Scholar
Witkovsky, P. & Dearry, A. (1992). Functional roles of dopamine in the vertebrate retina. Progress in Retinal Research 11, 113–147.Google 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
Yang, H.L., Shou, T.T., Li, C.Y., Cheng, W.U. & Chai, M.C. (1978). Changes in retinal sensitivity of silver carp during light adaptation. Acta Biochimica Biophysica Sinica 10, 15–26.Google Scholar
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 carrier mediated release of GABA from retinal horizontal cells. Brain Research 233, 211–215.CrossRefGoogle ScholarPubMed
Yazulla, S. & Zucker, C.L. (1988). Synaptic organization of dopaminergic interplexiform cells in the goldfish retina. Visual Neuroscience 1, 13–30.CrossRefGoogle ScholarPubMed
Yonemura, D. & Hatta, M. (1966). Studies of the minor components of the frog's electroretinogram. Japanese Journal of Physiology 16, 11–22.Google Scholar