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Dopamine and retinal function

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Abstract

This review summarizes the experimental evidence in support of dopamine's role as a chemical messenger for light adaptation. Dopamine is released by a unique set of amacrine cells and activates D1 and D2 dopamine receptors distributed throughout the retina. Multiple dopamine-dependent physiological mechanisms result in an increased signal flow through cone circuits and a diminution of signal flow through rod circuits. Dopamine also has multiple trophic roles in retinal function related to circadian rhythmicity, cell survival and eye growth. In a reciprocal way, the health of the dopaminergic neurons depends on their receiving light-driven synaptic inputs. Dopamine neurons appear early in development, become functional in advance of the animal's onset of vision and begin to die in aging animals. Some diseases affecting photoreceptor function also diminish day/night differences in dopamine release and turnover. A reduction in retinal dopamine, as occurs in Parkinsonian patients, results in reduced visual contrast sensitivity

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References

  1. Witkovsky P, Dearry A. Functional roles of dopamine in the vertebrate retina. Prog Ret Res 1991; 11: 247–292.

    Google Scholar 

  2. Djamgoz MBA, Wagner H-J. Localization and function of dopamine in the adult retina. Neurochem.Int 1991; 20: 139–191.

    Google Scholar 

  3. Djamgoz MBA, Hankins MW, Hirano J, Archer SN. Neuro-biology of retinal dopamine in relation to degenerative states of the tissue. VisionRes.1987; 37: 3509–3929.

    Google Scholar 

  4. Nguyen-Legros J, Versaux-Botteri C, Vernier P. Dopamine receptor localizationinthe mammalianretina.Mol. Neuro-biol 1999; 19: 181–204.

    Google Scholar 

  5. Dacey DM. The dopaminergic amacrine cell. J Comp Neurol 1990; 301: 461–489.

    Google Scholar 

  6. Famiglietti EV, Kolb H. Structural basis for ON-and OFF-center responses in retinal cells. Science 1976; 194: 193–195.

    Google Scholar 

  7. Kolb H, Cuenca N, Wang H-H, Dekorver L. The synaptic or-ganization of the dopaminergic amacrine cell in the cat retina. J Neurocytol 1990; 19: 343–366.

    Google Scholar 

  8. Marshak DW. Synaptic inputs to dopaminergic neurons in mammalianretinas Prog BrainRes 2001; 131: 83–91.

    Google Scholar 

  9. Mariani AP. Giant bistrati ed bipolar cells in monkey retina. Anat Rec 1983; 206: 215–220.

    Google Scholar 

  10. Hokoc JN, Mariani AP. Tyrosine hydroxylase immunore-activity in the rhesus monkey retina reveals synapses from bipolar cells to dopaminergic amacrine cells. J Neurosci 1987; 7: 2785–2793.

    Google Scholar 

  11. Bloom eld SA, Dacheux R. Rod vision:pathways and pro-cessing inthe mammalianretina. Prog Ret Eye Res 2001; 20: 351–384.

    Google Scholar 

  12. Wässle H, Chun MH. Dopaminergic and indoleamine-accumulating amacrine cells express GABA-like immunore-activity inthe cat retina. J Neurosci 1988; 8: 3383–3394.

    Google Scholar 

  13. Wulle I, Wagner H-J. GABA and tyrosine hydroxylase im-munocytochemistry reveal different patterns of colocaliza-tion in retinal neurons of various vertebrates. J Comp Neur 1990; 296: 173–178.

    Google Scholar 

  14. Contini M, Raviola E. GABAergic synapses made by a ret-inal dopaminergic neuron. Proc Natl Acad Sci USA 2003; 100: 1358–1363.

    Google Scholar 

  15. Veruki ML, Wässle H. Immunohistochemical localization of dopamine D1 receptors in rat retina. Eur J Neurosci 1996; 8: 2286–2297.

    Google Scholar 

  16. Feigenspan A, Gustincich S, Bean BP, Raviola E. Spontan-eous activity of solitary dopaminergic cells of the retina. J Neurosci 1998; 18: 6776–6789.

    Google Scholar 

  17. Gustincich S, Feigenspan A, Wu DK, Koopman LJ, Raviola E. Control of dopamine release in the retina:a transgenic approach to neural networks. Neuron 1997; 18: 723–736.

    Google Scholar 

  18. Gabriel R, de Souza S, Ziff EB, Witkovsky P. Association of the AMPA-receptor related post-synaptic density proteins GRIP and ABP with subsets of glutamate-sensitive neurons inthe rat retina. J Comp Neur 2002; 449: 129–140.

    Google Scholar 

  19. Gustincich S, Feigenspan A, Sieghart W, Raviola E. Com-positionof the GABA Areceptors of retinal dopaminergic neurons. J Neurosci 1999; 19: 7812–7822.

    Google Scholar 

  20. Savy C, Moussa F, Durand J, Yelnik J, Simon A, Nguyen-Legros J. Distribution and spatial geometry of dopamine interplexiform cells in the retina. II External arborizations in the adult rat and monkey. J Comp Neur 1995; 355: 392–404.

    Google Scholar 

  21. Dowling JE, Ehinger B. Synaptic organization of the amine-containing interplexiform cells of the gold sh and Cebus monkey retina. Science 1975; 188: 270–273.

    Google Scholar 

  22. Ehinger B, Floren I. Quantitation of the uptake of indoleam-ines and dopamine in the rabbit retina. Exp Eye Res 1978; 26: 1–11.

    Google Scholar 

  23. Puopolo M, Hochstetler SE, Gustincich S, Wightman RM, Raviola E. Extrasynaptic release of dopamine in a retinal neuron:activity dependence and transmitter modulation. Neuron2001; 30: 211–225.

    Google Scholar 

  24. Gingrich JA, Caron M. Recent advances in the molecular biology of dopamine receptors. Annu Rev Neurosci 1993; 16: 299–321.

    Google Scholar 

  25. Seeman P, vanTol HHM. Dopamine receptor pharmacology. Trans Pharmacol Sci 1994; 15: 264–270.

    Google Scholar 

  26. Dearry A, Gingrich JA, Falardeau P, Fremeau RT, Bates MD, Caron MG. Molecular cloning and expression of the gene for a humanD1 dopamine receptor. Nature 1990; 347: 72–76.

    Google Scholar 

  27. Dearry A, Falardeau P, Shores C, Caron MG. D2 dopamine receptors in the human retina.Cloning of cDNA and local-izationof messenger RNA Cell Molec Neurobiol 1991; 11: 437–454.

    Google Scholar 

  28. Sokoloff P, Schwartz JC. Novel dopamine receptors half a decade later. Trends Pharmacol Sci 1995; 16: 406–408.

    Google Scholar 

  29. Ilani T, Fishburn CS, Levavi-Sivan B, Carmon S, Raveh L, Fuchs S. Coupling of dopamine receptors to g proteins: studies with chimeric D2/D3 dopamine receptors. Cell Mol Neurobiol 2002; 22: 47–56

    Google Scholar 

  30. Versaux-Botteri C, Gibert J-M, Nguyen-Legros J, Vernier P. Molecular identi cation of a dopamine D 1 b receptor in bovine retinal pigment epithelium. Neurosci Lett 1997; 237: 9–12.

    Google Scholar 

  31. Muresan Z, Besharse JC. D2-like dopamine receptors inam-phibian retina:localization with fluorescent ligands. J Comp Neur 1993; 331: 149–160.

    Google Scholar 

  32. Cohen AI, Todd RD, Harmon S, O 'Malley KL. Photore-ceptors of mouse retinas possess D4 receptors coupled to adenylate cyclase. Proc Natl Acad Sci 1992; 89: 12093–12097.

    Google Scholar 

  33. Nguyen-Legros J, Simon A, Caille I, Bloch B. Immunocyto-chemical localizationof dopamine D1 receptors inthe retina of mammals. Vis Neurosci 1997; 14: 545–551.

    Google Scholar 

  34. Veruki M. Dopaminergic neurons in the rat retina express dopamine D2/3 receptors. Eur J Neurosci 1997; 9: 1096–1100

    Google Scholar 

  35. Dubocovich ML, Weiner N. Pharmacological differences between the D-2 autoreceptor and D-1 dopamine receptor in rabbit retina. J Pharmacol Exp Ther 1985; 233: 747–754.

    Google Scholar 

  36. Biedermann B, Frohlich E, Grosche J, Wagner H-J, Reichen-bach A. Mammalian Muller (glial)cells express functional D2 dopamine receptors. Neuroreport 1995; 6: 609–612.

    Google Scholar 

  37. Wu DM, Kaamura H, Li Q, Puro DG. Dopamine activ-ates ATP-sensitive K+currents in rat retinal pericytes. Vis Neurosci 2001; 18: 935–940.

    Google Scholar 

  38. Bjelke B, Goldstein M, Tionner B, Andersson C, Sesack SR, Steinbusch HWM, Lew JY, He X, Watson S, Tengroth B, Fuxe K. Dopaminergic transmission in the rat retina:evid-ence for volume transmission. J Chem Neuroanat 1996; 12: 37–50.

    Google Scholar 

  39. Cooper JR, Bloom FE, Roth, RB. The Biochemical Basis of Neuropharmacology 5th ed.New York:1986;Oxford University Press

    Google Scholar 

  40. Nir I, Haque R, Iuvone PM. Diurnal metabolism of dopam-ine in dystrophic retinas of homozygous and heterozygous retinal degeneration slow (rds)mice. Brain Res 2000; 884: 13–22.

    Google Scholar 

  41. Witkovsky P, Nicholson C, Rice ME, Bohmaker K, Meller E. Extracellular dopamine concentration in the retina of the clawed frog,Xenopus laevis. Proc Natl Acad Sci 1993; 90: 5667–5671.

    Google Scholar 

  42. Doyle SE, McIvor WE, Menaker M. Circadian rhythmicity in dopamine content of mammalian retina:role of the photoreceptors. J Neurochem 2002; 83: 211–219.

    Google Scholar 

  43. Ko F, Seeman P, Sun WS, Kapur S. Dopamine D2 receptors internalize in their low-af nity state. Neuroreport 2002; 13: 1017–1020.

    Google Scholar 

  44. Nowak JZ, Sek B, Schorderet M. Dark-induced supersens-itivity of dopamine D-1 and D-2 receptors in rat retina. Neuroreport 1991; 2: 429–432.

    Google Scholar 

  45. Hadjiconstantinou M, Qu ZX, Neff NH. Differential changes of retina dopamine binding sites and adenylyl cyclase responses following 6-hydroxydopamine treatment 1991. Brain Res 538: 193–195.

    Google Scholar 

  46. Ding JM, Dong C, Weber ET, Faiman LE, Rea MA, Gillette MU. Resetting the biological clock:mediation of nocturnal circadian shifts by glutamate and NO. Science 1994; 266: 1713–1717.

    Google Scholar 

  47. Besharse JC, Iuvon e PM. Circadianclock inXenopus eye controlling retinal serotonin N-acetyltransferase. Nature 1983; 305: 133–135.

    Google Scholar 

  48. Cahill GM, Besharse JC. Circadian clock functions localized in xenopus retinal photoreceptors. Neuron 1993; 10: 573–577.

    Google Scholar 

  49. Cahill GM, Besharse JC. Rhythmic regulationof retin al melatonin:metabolic pathways,neurochemical mechanisms, and the ocular circadian clock. Cell Mol Neurobiol 1991; 11: 529–560.

    Google Scholar 

  50. Tosini G, Menaker M. Circadian rhythms in cultured mam-malian retina. Science 1996; 272: 419–421.

    Google Scholar 

  51. Doyle SE, McIvor W, Menaker M. Circadian rhythmicity in dopamine content of mammalian retina:role of the photore-ceptors. J Neurochem 2002; 83: 211–219.

    Google Scholar 

  52. Reppert SM, Weaver DR, Godson C. Melatoninreceptors step into the light:cloning and classi cation of subtypes. Trends Pharmacol Sci 1996; 17: 100–102.

    Google Scholar 

  53. Meyer P, Pache M, Loeffler KU, Brydon L, Jockers R, Flammer J, Wirz-Justice A, Savaskan E. MelatoninMT-1-receptor immunoreactivity inthe humaneye. Br J Ophthal 2002; 86: 1053–1057.

    Google Scholar 

  54. Marchiafava PL, Longoni B. Melatonin as an antioxidant in retinal photoreceptors. J Pineal Res 1999; 26: 184–189.

    Google Scholar 

  55. Dubocovich ML, Masana MI, Iacob S, Sauri DM. Melatonin receptor antagonists that differentiate between the human Mel1a and Mel1b recombinant subtypes are used to as-sess the pharmacological pro le of the rabbit retina ML1 presynaptic heteroreceptor.Naunyn. Schmiedebergs Arch Pharmacol 1997; 355: 365–375.

    Google Scholar 

  56. Fujieda H, Scher J, Hamadanizadeh SA, Wankiewicz E, Pang SF, Brown GM. Dopaminergic and GABAergic amacrine cells are direct targets of melatonin:immunocytochemical study of mt1 melatonin receptor in guinea pig retina. Vis Neurosci 2000; 17: 63–70.

    Google Scholar 

  57. Tosini G, Menaker M. The clock in the mouse retina: melatonin synthesis and photoreceptor degeneration. Brain Res 1998; 789: 221–228.

    Google Scholar 

  58. Andersen FE, Green CB. Symphony of rhythms inthe Xenopus laevis retina. Micr Res Tech 2000; 50: 360–372.

    Google Scholar 

  59. Tosini G, Fukuhara C. The mammalian retina as a clock. Cell Tiss Res 2002; 309: 119–126.

    Google Scholar 

  60. Namihira M, Honma S, Abe H, Masubuchi S, Ikeda M, Honma K-I. Circadian pattern,light responsiveness and localizationof rPer1 and rPer2 gene expressioninthe rat retina. Neuroreport 2001; 12: 471–475.

    Google Scholar 

  61. Kuhlman SJ, Quintero JE, McMahon DG.GFP. uorescence reports Period1 circadiangene regulationinthe mammalian biological clock Neuroreport.2000;. 11: 1–4.

    Google Scholar 

  62. Witkovsky P, Veisenberger E, LeSauter J, Yan L, Johnson M, Zhang D-Q, McMahon D, Silver R. Cellular locationand circadianrhythm of expressionof the biological clock gene Period 1 inthe mouse retina. J Neurosci 2003; 23: 7670–7676.

    Google Scholar 

  63. Soni BG, Philp AR, Foster RG, Knox BE. Novel retinal photoreceptors. Nature 1998; 394: 27–28.

    Google Scholar 

  64. Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD. A novel human opsin in the inner retina. J Neurosci 2000; 20: 600–605.

    Google Scholar 

  65. Hattar S, Liao W-W,T akao M, Berson DM, Yau K-W. Melanopsin-containing retinal ganglion cells:architecture, projections and intrinsic photosensitivity. Science 2002; 295: 1065–1070.

    Google Scholar 

  66. Foster RG, Provencio I, Hudson D, Fiske S, DeGrupo W, Menaker M. Circadianphotoreceptioninthe retinally degenerate mouse (rd/rd). J Comp Physiol A 1991; 169: 39–50.

    Google Scholar 

  67. Miyamoto Y, Sancar A. Vitamin B2-based blue-light photoreceptors inthe retinohypothalamic tract as the photoactive pigments for setting the circadian clock in mammals. Proc Natl Acad Sci USA 1998; 95: 6097–6102.

    Google Scholar 

  68. Reppert SM, Weaver DR. Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 2001; 63: 647–676.

    Google Scholar 

  69. Pugh EN, Lamb TD. Phototransductioninvertebrate rods and cones:molecular mechanisms of amplification,recovery and light adaptation.In:Stavenga DG, DeGrip WJ, Pugh EN,eds. Handbook of Biological Physics,Vol.3 Amsterdam: Elsevier,2000;183–255.

    Google Scholar 

  70. Shulman LM, Fox DA. Dopamine inhibits mammalian photoreceptor Na+,K+-ATPase activity via a selective effect onthe 3 isozyme. Proc Natl Acad Sci USA 1996; 93: 8034–8039.

    Google Scholar 

  71. Krizaj D, Gabriel R, Owen WG,Witkovsky P. Dopamine D2 receptor-mediated modulation of rod-cone coupling in the Xenopus retina. J Comp Neur 1998; 398: 529–538.

    Google Scholar 

  72. Stella SL, Thoreson WB. Differen tial modulationof rod and cone calcium currents in tiger salamander retina by D2 dopamine receptors and cAMP. Eur J Neurosci 1998; 15: 3537–3548.

    Google Scholar 

  73. Akopian A, Witkovsky P. D2 dopamine receptor-mediated inhibition of a hyperpolarization-activated current in rod photoreceptors. J Neurophysiol 1996; 67: 1828–1835.

    Google Scholar 

  74. Thoreson WB, Stella SL, Bryson EJ, Clements J, Witkovsky P. Interactionbetweencalcium and calcium-activated chloride channels diminishes rod output following stimulation of D2-like dopamine receptors in the salamander retina. Vis Neurosci 2002; 19: 235–247.

    Google Scholar 

  75. Schneeweis DM, Schnapf JL. Photovoltage of rods and cones in the macaque retina. Science 1995; 268: 1053–1056.

    Google Scholar 

  76. .DeVries SH, Schwartz EA. Modulationof anelectrical synapse between pairs of cat sh horizontal cells by dopamine and second messengers. J Physiol 1989; 414: 351–375.

    Google Scholar 

  77. McMahon DG, Brown DR. Modulationof gap-junction channel gating at zebrafish electrical synapses. J Neuro-physiol 1994; 72: 2257–2268.

    Google Scholar 

  78. Dermietzel R, Kremer M, Paputsoglu G, Stang A, Skerrett IM, Gomes D, Srinivas M, Janssen-Bienhold U, Weiler R, Nicholson BJ, Bruzzone R, Spray DC. Molecular and functional diversity of neural connexins in the retina. J Neurosci 2000; 20: 8331–8343.

    Google Scholar 

  79. He S, Weiler R, Vaney DI. Endogenous dopaminergic regulationof horizontal cell coupling inthe mammalian retina. J Comp Neur 2000; 428: 33–40.

    Google Scholar 

  80. Xin DY, Bloom eld SA. Dark-and light-induced changes incoupling between horizontal cells in mammalian retina. J Comp Neur 1999; 405: 75–87.

    Google Scholar 

  81. Lu C, McMahon DG. Modulation of hybrid bass retinal gap junctional channel gating by nitric oxide. J Physiol 1997; 499: 689–699.

    Google Scholar 

  82. Mills SL, Massey SC. Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 1995; 377: 734–737.

    Google Scholar 

  83. Weiler R, Pottek M, He S, Vaney DI. Modulation of couping between retinal horizontal cells by retinoic acid and endogenous dopamine. Brian Res Rev 2000; 32: 121–129.

    Google Scholar 

  84. Bugnon O, Schaad NC, Schorderet M. Nitric oxide modulates endogenous dopamine release in bovine retina. Neuroreport 1994; 5: 401–404.

    Google Scholar 

  85. Djamgoz MBA, Cunningham JR, Davenport SL, Neal MJ. Nitric oxide inhibits depolarization-induced release of endo-genous dopamine in the rabbit retina. Neurosci Lett 1995; 198: 33–36.

    Google Scholar 

  86. Eldred WD. Nitric oxide in the retina.Functional neuroanatomy of the nitric oxide system. In:Steinbusch HWM, De Vente J, Vincent SR, Eds. Handbook of Chemical Neuroanatomy 17.Amsterdam: Elsevier, 2000; 111–145.

    Google Scholar 

  87. Knapp AG, Dowling JE. Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature 1987; 325: 437–439.

    Google Scholar 

  88. Witkovsky P, Stone S, Besharse J. Dopamine modi es the balance of rod and cone inputs to horizontal cells of the Xenopus retina. Brain Res 1988; 449: 332–336.

    Google Scholar 

  89. Witkovsky P, Stone S, Tranchina D. Photoreceptor to ho-rizontal cell synaptic transfer in the Xenopus retina:modulation of by dopamine ligands and a circuit model for.37 interactions of rod and cone inputs. J Neurophysiol 1989; 62: 864–881.

    Google Scholar 

  90. Steinberg RH. Rod and cone contributions to S-potentials from the cat retina. Vision Res 1969; 9: 1319–1329.

    Google Scholar 

  91. Nelson R. Cat cones have rod input:a comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. J Comp Neur 1977; 172: 109–135.

    Google Scholar 

  92. Hankins MW, Ikeda H. The role of dopaminergic pathways at the outer plexiform layer of the mammalianretina. ClinVis Sci 1991; 6: 87–93.

    Google Scholar 

  93. Piccolino M, Neyton J, Gerschenfeld M. Decrease of gap junction permeability induced by dopamine and cyclic 3 ':5 '-monophosphate in horizontal cells of the turtle retina. J Neurosci 1984; 4: 2477–2488.

    Google Scholar 

  94. Maguire G, Werblin F. Dopamine enhances a glutamate-gated ionic current in OFF bipolar cells of the tiger salamander retina. J Neurosci 1994; 14: 6094–6101.

    Google Scholar 

  95. Dong C-J, Werblin FS. Dopamine modulation of GABA c receptor function in an isolated retinal neuron. J Neurophysiol 1994; 71: 1258–1260.

    Google Scholar 

  96. Wellis DP, Werblin FS. Dopamine modulates GABA c receptors mediating inhibition of calcium entry into and transmitter release from bipolar cell terminals in tiger salamander retina. J Neurosci 1995; 15: 4748–4761.

    Google Scholar 

  97. Pfeiffer-Linn CL, Lasater EM. Multiple second-messenger system modulation of voltage-activated calcium currents in teleost retinal horizontal cells. J Neurophysiol 1998; 80: 377–388.

    Google Scholar 

  98. Liu Y, Lasater EM. Calcium currents in turtle retinal ganglion cells.II dopamine modulation via a cyclic AMP-dependent mechanism. J Neurophysiol 1994; 71: 743–752.

    Google Scholar 

  99. Fan S-F, Yazulla S. Dopamine depletionwith 6-OHDA enhances dopamine D1 receptor modulation of potassium currents in retinal bipolar cells. Vis Neurosci 2001; 18: 327–337.

    Google Scholar 

  100. Fan S-F, Yazulla S. Modulationof voltage-dependent K+currents (I K (V) ) inretinal bipolar cells by ascorbate is mediated by dopamine D1 receptors. Vis Neurosci 1999; 16: 923–931.

    Google Scholar 

  101. Hare WA, Owen WG. Similar effects of carbachol and dopamine on neurons in the distal retina of the tiger salamander. Vis Neurosci 1995; 12: 443–455.

    Google Scholar 

  102. Hampson ECGM, Vaney DI, Weiler R. Dopaminergic modulationof gap junction permeability between a macrine cells in mammalian retina. J Neurosci 1992; 12: 4911–4922.

    Google Scholar 

  103. Deans MR, Volgyi B, Goodenough DA, Bloomfield SA, Paul DL. Connexin36 is essential for transmission of rodmediated visual signals in the mammalian retina. Neuron 2002; 36: 703–712.

    Google Scholar 

  104. Feigenspan A, Bormann J. Facilitation of GABAergic signaling in the retina by receptors stimulating adenylate cyclase. Proc Natl Acad Sci USA 1994; 91: 10893–10897.

    Google Scholar 

  105. Masland RH, Mills JW, Hayden SA. Acetylcholine synthesizing amacrine cells:identification and selective staining by using radioautography and fluorescent markers. Proc Roy Soc London B 1984; 223: 79–100.

    Google Scholar 

  106. Yeh HH, Battelle BA, Puro DG. Dopamine regulates synaptic transmission mediated by cholinergic neurons of the rat retina. Neuroscience 1984; 13: 901–909.

    Google Scholar 

  107. Hensler JG, Dubocovich ML. D1-Dopamine receptor activationmediates [3H ]acetylcholine release from rabbit retina. BrainRes 1986; 398: 407–412.

    Google Scholar 

  108. Hensler JG, Cotterell DJ, Dubocovich ML. Pharmacological and biochemical characterization of the D-1 dopamine receptor mediating acetylcholine release in rabbit retina. J Pharmacol Exp Ther 1987; 243: 857–867.

    Google Scholar 

  109. Kuffler SW. Discharge patterns and functional organization of mammalian retina. J Neurophysiol 1953; 16: 37–68.

    Google Scholar 

  110. Rodieck RW. The First Steps in Seeing. Sunderland, MA: Sinauer Assoc. Inc. 1998.

    Google Scholar 

  111. Naka K-I, Witkovsky P. Dogfish ganglion cell discharge resulting from extrinsic polarization of the horizontal cells. J Physiol 1972; 223: 449–460.

    Google Scholar 

  112. Mangel SC. Analysis of the horizontal cell contribution to the receptive eld surround of ganglion cells in the rabbit retina. J Physiol 1991; 442: 211–234.

    Google Scholar 

  113. Barlow HB, Fitzhugh R, Kuffler SW. Change of organization in the receptive fields of the cat 's retina during dark adaptation. J Physiol 1957; 137: 338–354.

    Google Scholar 

  114. Müller F, Wässle H, Voigt T. Pharmacological modulationof the rod pathway in the cat retina. J Neurophysiol 1988; 59: 1657–1672.

    Google Scholar 

  115. Bolz J, Their P, Voigt T, Wässle H. Action and localization of glycine and taurine in the cat retina. J Physiol 1985; 362: 395–413.

    Google Scholar 

  116. Jensen RJ, Daw NW. Effects of dopamine antagonists on receptive elds of brisk cells and directionally selective cells in the rabbit retina. J Neurosci 1984; 4: 2972–2985.

    Google Scholar 

  117. Jensen R. Effects of dopamine and its agonists and antagonists on the receptive field properties of ganglion cells in the rabbit retina. Neuroscience 1986; 17: 837–855.

    Google Scholar 

  118. Daw NW, Brunken WJ, Jensen R. The function of monoamines in the retina. In:Weiler R, Osborne NN, eds. Neurobiology of the Inner Retina,NATO ASI Ser.1989;363–374.

  119. Jensen R. Mechanism and site of action of a dopamine D1 antagonist in the rabbit retina. Vis Neurosci 1989; 3: 573–585.

    Google Scholar 

  120. Jensen R. Involvement of glycinergic neurons in the diminished surround activity of ganglion cells in the dark-adapted rabbit retina. Vis Neurosci 1991; 6: 43–53.

    Google Scholar 

  121. Holder GE. Pattern electroretinography (PERG) and an integrated approach to visual pathway diagnosis. Prog Ret Eye Res 1991; 20: 531–561.

    Google Scholar 

  122. Naarendorp F, Hitchcock PF, Sieving PA. Dopaminergic modulation of rod pathway signals does not affect the scotopic ERG of cat at dark-adapted threshold. J Neuro-physiol 1993; 70: 1681–1691.

    Google Scholar 

  123. Olivier P, Jolicoeur FB, Lafond B, Drumheller AT, Brunette JR. Effects of retinal dopamine depletion on the rabbit electroretinogram. Doc.Ophthalmol 1987; 66: 359–371.

    Google Scholar 

  124. Malmfors T, Sachs C. Degeneration of adrenergic nerves produced by 6-hydroxydopamine. Eur.J Pharmacol 1968; 3: 89–92.

    Google Scholar 

  125. Sieving PA, Frishman LJ, Steinberg RH. Scotopic threshold response of proximal retina in cat. J Neurophysiol 1986; 56: 1949–1061.

    Google Scholar 

  126. Frishman LJ, Steinberg RH. Light evoked increases in [K+]oinproximal portionof dark-adapted cat retina. J Neurophysiol 1989; 621: 1233–1243.

    Google Scholar 

  127. Volgyi B, Xin D, Bloomfield SA. Feedback inhibitionin the inner plexiform layer underlies the surround-mediated responses of AII amacrine cells in the mammalian retina. J Physiol 2002; 539: 603–614.

    Google Scholar 

  128. Menger N, Wässle H. Morphological and physiological properties of the A17 amacrine cell of the rat retina. Vis Neurosci 2000; 17: 769–780.

    Google Scholar 

  129. Naarendorp F, Sieving PA. The scotopic threshold response of the cat ERG is suppressed selectively by GABA and glycine 1991 Vision Res 31: 1–15.

    Google Scholar 

  130. Tian N, Slaughter MM. Correlationof dynamic responses in the ON bipolar neuron and the b-wave of the electroretinogram. VisionRes 1995; 35: 1359–1364.

    Google Scholar 

  131. Skandries W, Wässle H. Dopamine and serotonin in cat retina:electroretinography and histology. Exp Brain Res 1988; 71: 231–240.

    Google Scholar 

  132. Schneider T, Zrenner E. Effects of D-1 and D-2 dopamine antagonists on ERG and optic nerve response of the cat. Exp Eye Res 1991; 52: 425–430.

    Google Scholar 

  133. Tornqvist K, Yang X-L, Dowling JE. Modulation of cone horizontal cell activity in the teleost sh retina.III.Effects of prolonged darkness and dopamine on electrical coupling betweenhorizontal cells. J Neurosci 1988; 8: 2279–2288.

    Google Scholar 

  134. Dearry A, Burnside B. Dopamine induces light-adaptive retinomotor movements in teleost photoreceptors and retinal pigment epithelium. In:Bodis-Wollner I, Alan R Liss, ed. Dopaminergic Mechanisms in Vision. New York: 1988; 109–135.

  135. Weiler R, Baldridge WH, Mangel SC, Dowling JE. Modulation of endogenous dopamine release in the fish retina by light and prolonged darkness. Vis Neurosci 1997; 14: 351–366.

    Google Scholar 

  136. Umino O, Lee Y, Dowling JE. Effects of light stimuli on the release of dopamine from interplexiform cells in the white perch retina. Vis Neurosci 1991; 7: 451–458.

    Google Scholar 

  137. Wang Y, Mangel SC. A circadian clock regulates rod and cone input to fish retinal cone horizontal cells. Proc Natl Acad Sci USA 1996; 93: 4655–4660.

    Google Scholar 

  138. Ribelayga C, Wang Y, Mangel SC. Dopamine mediates circadian clock regulation of rod and cone input to fish retinal horizontal cells. J Physiol 2002; 544: 801–816.

    Google Scholar 

  139. Li L, Dowling JE. Effects of dopamine depletion on visual sensitivity of zebra fish. J Neurosci 2000; 20: 1893–1903.

    Google Scholar 

  140. Witkovsky P, Schuette M. The organization of dopaminergic neurons in vertebrate retinas. Vis Neurosci 1991; 7: 113–124.

    Google Scholar 

  141. Kumer SC, Vrana KE. Intricate regulation of tyrosine hydroxylase activity and gene expression. J Neurochem 1996; 67: 443–462.

    Google Scholar 

  142. Haycock JW. Multiple signaling pathways in bovine chromaffin cells regulate tyrosine hydroxylase phosphorylation bat Ser 19, Ser 31, and Ser 40. Neurochem Res 1993; 18: 15–26.

    Google Scholar 

  143. Iuvone PM, Galli CL, Garrison-Gund CK, Neff NH. Light stimulates tyrosine hydroxylase activity and dopamine synthesis in retinal amacrine neurons. Science 1978; 202: 901–902.

    Google Scholar 

  144. Iuvone PM, Rauch AL, Marshburn PB, Glass DB, Neff NH. Activation of retinal tyrosine hydroxylase in vitro by cyclic AMP-dependent protein kinase:characterization and comparisonto activation in vivo by photic stimulation. J Neurochem 1982; 39: 1632–1640.

    Google Scholar 

  145. Boelen MK, Wellard J, Dowton M, Morgan IG. Endogenous dopamine inhibits the release of enkephalin-like immunoreactivity from amacrine cells of the chicken retina in the light. BrainRes 1994; 645: 240–246.

    Google Scholar 

  146. Johnson J, Wu V, Wong H, Walsh JH, Brecha NC. Somatostatinreceptor subtype 2A expressioninthe rat retina. Neuroscience 1999; 94: 675–683.

    Google Scholar 

  147. Akopian A, Johnson J, Gabriel R, Brecha N, Witkovsky P. Somatostatinmodulates voltage-gated K +and Ca 2+currents in rod and cone photoreceptors of the salamander retina. J Neurosci 2000; 20: 929–936.

    Google Scholar 

  148. Witkovsky P, Gabriel R, Haycock J, Meller E. Influence of light and neural circuitry on tyrosine hydroxylase phosphorylation in the rat retina. J Chem Neuroanat 2000; 19: 105–116.

    Google Scholar 

  149. Boelen MK, Boelen MG, Marshak DW. Light stimulated release of dopamine from the primate retina is blocked by 1–2-amino-4-phosphonobutyric acid (APB). Vis Neurosci 1998; 15: 97–103.

    Google Scholar 

  150. Critz SD, Marc RE. Glutamate antagonists that block hyperpolarizing bipolar cells increase the release of dopamine from turtle retina. Vis Neurosci 1992; 9: 271–278.

    Google Scholar 

  151. Nir I, Haque R, Iuvone PM. Diurnal metabolism of dopamine in dystrophic retinas of homozygous and heterozygous retinal degeneration slow (rds)mice. Brain Res 2000; 884: 13–22.

    Google Scholar 

  152. Nir I, Iuvone PM. Alterations in light-evoked dopamine metabolism in dystrophic retinas of mutant rds mice. Brain Res 1994; 649: 85–94.

    Google Scholar 

  153. Nir I, Haque R, Iuvone PM. Regulation of cAMP by light and dopamine receptors is dysfunctional in photoreceptors of dystrophic retinal degeneration slow (rds)mice. Exp Eye Res 2001; 73: 265–272.

    Google Scholar 

  154. Nir IU, Harrison JM, Haque R, Low MJ, Grandy DK, Rubin-stein M, Iuvone PM. Dysfunctional light-evoked regulation of cAMP in photoreceptors and abnormal retinal adaptation in mice lacking dopamine D4 receptors. J Neurosci 2002; 22: 2063–2073.

    Google Scholar 

  155. Cohen AI, Blazynski C. Dopamine and its agonists reduce a light-sensitive pool of cyclic AMP in mouse photoreceptors Vis Neurosci 1990; 4: 43–52.

    Google Scholar 

  156. Xu LX, Tanaka Y, Bonderenko VA, Matsuura I, Matsumoto H, Yamazaki A, Hayashi F. Phosphorylation of the gamma subunit of the retinal photoreceptor cGMP phosphodiesterase by the cAMP-dependent protein kinase and its effect on the gamma subunit interaction with other proteins. Biochemistry 1998; 37: 6205–6213.

    Google Scholar 

  157. Hankins M, Ikeda H. Early abnormalities of retinal dopamine pathways in rats with hereditary retinal dystrophy. Doc Ophthalmol 1994; 86: 325–334.

    Google Scholar 

  158. Steinberg RH, Linsenmeier RA, Griff ER. Retinal pigment epithelial cell contributions to the electroretinogram and electrooculogram Prog Ret Res 1985; 4: 33–66.

    Google Scholar 

  159. Dawis SM, Niemeyer G. Dopamine in fluences the light peak in the perfused mammalian eye. Invest Ophthalmol Vis Sci 1986; 27: 330–335.

    Google Scholar 

  160. Gallemore RP, Steinberg RH. Effects of dopamine on the chick retinal pigment epithelium. Invest Ophthalmol Vis Sci 1990:31: 67–80.

    Google Scholar 

  161. Nao-i N, Gallemore RP, Steinberg RH. Effects of cAMP and IBMX on the chick retinal pigment epithelium. Invest Ophthalmol Vis Sci 1990; 31: 68–80.

    Google Scholar 

  162. Rudolf G, Wioland N, Allart I. Is dopamine involved in the generationof the light peak inthe intact chickeneye? Vision Res 1991; 11: 1841–1849.

    Google Scholar 

  163. Iuvone PM, Tigges M, Fernandes A, Tigges J. Dopamine synthesis and metabolism in rhesus monkey retina:development, aging, and the effects of monocular visual deprivation. Vis Neurosci 1989; 2: 465–471.

    Google Scholar 

  164. Stone RA, Lin T, Laties AM, Iuvone PM. Retinal dopamine and form-deprivation myopia. Proc Natl Acad Sci USA 1989; 86: 704–706.

    Google Scholar 

  165. Rohrer B, Iuvone PM, Stell WK. Stimulation of dopaminergic amacrine cells by stroboscopic illumination or broblast growth factor (bFGF,FGF-2)injections:possible roles in preventionof form-deprivationmyopia inthe chick. Brain Res 1995; 686: 169–181.

    Google Scholar 

  166. Iuvone PM, Tigges M, Stone RA, Lambert S, Laties AM. Effects of apomorphine, a dopamine receptor agonist, on ocular refractionand axial elongation in a primate model of myopia. Invest Ophthalmol Vis Sci 1991; 32: 1674–1677.

    Google Scholar 

  167. Rohrer B, Spira AW, Stell WK. Apomorphine blocks form deprivation myopia in chickens by a dopamine D2-receptor mechanism acting in retina or pigmented epithelium. Vis Neurosci 1993; 10: 447–453.

    Google Scholar 

  168. Seko Y, Tanaka Y, Tokoro T. Apomorphine inhibits the growth-stimulating effect of retinal pigment epithelium on scleral cells invitro. Cell Biochem Funct 1997; 15: 191–196.

    Google Scholar 

  169. Li XX, Schaeffel F, Kohler K, Zrenner E. Dose-dependent effects of 6-hydroxydopamine on deprivation myopia, electroretinograms, and dopaminergic amacrine cells in chickens. Vis Neurosci 1992; 9: 483–492.

    Google Scholar 

  170. Schaeffel F, Bartmann M, Hagel G, Zrenner E. Studies on the role of the retinal dopamine/melatonin system in experimental refractive errors in chickens. Vision Res 1995; 35: 1247–1264.

    Google Scholar 

  171. Seko Y, Shimizu M, Tokoro T. Retinoic acid increases in the retina of the chick with form deprivation myopia. Ophthalmol Res 1998; 30: 361–367.

    Google Scholar 

  172. Bitzer M, Feldmaemper M, Schaeffel F. Visually induced changes in components of the retinoic acid system in fundal layers of the chick. Exp Eye Res 2000; 70: 97–106.

    Google Scholar 

  173. Mertz JR, Wallman J. Choroidal retinoic acid synthesis:a possible mediator between refractive error and compensatory eye growth. Exp Eye Res 2000; 70: 519–527.

    Google Scholar 

  174. Fischer AJ, McGuire JJ, Schaeffel F, Stell WK. Light-and focus-dependent expression of the transcription factor ZENK inthe chick retina. Nat Neurosci 1999; 2: 706–712.

    Google Scholar 

  175. Rohrer B, Tao J, Stell WK. Basic broblast growth factor, its high-and low-affinity receptors,and their relationship to form-deprivation myopia in the chick. Neuroscience 1997; 79: 775–787.

    Google Scholar 

  176. Harnois C, di Paolo T. Decreased dopamine in the retinas of patients with Parkinson 's disease. Invest Ophthalmol Vis Sci 1990; 31: 2473–2475.

    Google Scholar 

  177. Nguyen-Legros J, Harnois C, DiPaolo T, Simon A. The retinal dopamine system in Parkinson 's disease. Clin Vis Sci 1993; 8: 1–12.

    Google Scholar 

  178. Maffei L, Fiorentini A. Electroretinographic responses to alternating gratings before and after section of the optic nerve. Science 1981; 211: 953–955.

    Google Scholar 

  179. Peppe A, Stanzione P, Pierantozzi M, Semprini R, Bassi A, Santilli AM, Formisano R, Piccolino M, Bernardi G. Does pattern electroretinogram spatial tuning alteration in Parkinson 's disease depend on motor disturbances or retinal dopaminergic loss? Electroencephalogr Clin Neurophysiol 1998; 106: 374–382.

    Google Scholar 

  180. Stanzione P, Pierantozzi M, Semprini R, Tagliati M, Traversa R, Peppe A, Pierelli F, Bernardi G. Increasing doses of L-sulpiride reveal dose and spatial frequency dependent effects of D2 selective blockade in the human electroretinogram. Vis Res 1995; 35: 2659–2664.

    Google Scholar 

  181. Akamine T, Nishimura Y, Ito K, Uji Y, Yamamoto T. Effects of haloperidol on K+ currents inacutely isolated rat retinal ganglion cells. Invest Ophthal Vis Sci 2002; 43: 1257–1261.

    Google Scholar 

  182. Stanzione P, Bodis-Wollner I, Pierantozzi M, Semprini R, Tagliati M, Peppe A, Bernardi G. A mixed D1 and D2 antagonist does not replay pattern electroretinogram alterations observed with a selective D2 antagonist in normal humans: relationship with Parkinson 's disease pattern electroretinogram alterations. Clin Neurophysiol 1999; 220: 82–85.

    Google Scholar 

  183. Guenther E, Wilsch V, Zrenner E. Inhibitory action of haloperidol, spiperone and SCH23390 on calcium currents in rat retinal ganglion cells. Neuroreport 1994; 5: 1363–1376.

    Google Scholar 

  184. Ghilardi MF, Bodis-Wollner I, Onofrj M, Marx MS, Glover AA. Spatial frequency-dependent abnormalities of the pattern electroretinogram and visual evoked potentials in a parkinsonian monkey model. Brain 1988; 111: 131–149.

    Google Scholar 

  185. Sarthy PV, Rayborn ME, Hollyfield JG, Lam DMK. The emergence, localization and maturation of neurotransmitter systems during development of the retina in Xenopus laevis. III.Dopamine. J Comp Neur 1981; 195: 595–602.

    Google Scholar 

  186. Witkovsky P, Gallin E, Hollyfield JG, Ripps H, Bridges CDB. Photoreceptor thresholds and visual pigment levels in normal and Vitamin-A deprived Xenopus tadpoles. J Neurophysiol 1976; 39: 1272–1287.

    Google Scholar 

  187. Chung SH, Stirling RV, Gaze RM. The structural and functional development of the retina in larval Xenopus. J Embryol Exp Morphol 1975; 33: 915–940.

    Google Scholar 

  188. Evans JA, Battelle B-A. Histogenesis of dopamine containing neurons in the rat retina. Exp Eye Res 1987; 44: 407–414.

    Google Scholar 

  189. Wulle I, Schnitzer J. Distribution and morphology of tyrosine hydroxylase-immunoreactive neurons in the developing mouse retina. Dev Brain Res 1989; 48: 59–72.

    Google Scholar 

  190. Versaux-Botteri C, Verney C, Zecevic N, Nguyen-Legros J.Early appearance of tyrosine hydroxylase immunoreactivity in the retina of human embryos. Dev Brain Res 1992; 69: 283–287.

    Google Scholar 

  191. Soares HC, de Melo Reis RA, De Mello FG, Ventura ALM, Kurtenbach E. Differential expression of D1A and D1B dopamine receptor mRNAs in the developing avian retina.J Neurochem 2000; 75: 1071–1075.

    Google Scholar 

  192. Guimaraes MZP, Hokoc JN, Duvoisin R, Reis RAM, Garcia de Mello F. Dopaminergic retinal cell differentiation in culture:modulationby for skolin and dopamine. Eur J Neurosci 2001; 13: 1931–1937.

    Google Scholar 

  193. Morgan WW, Kamp CW. Postnatal development of the light response of the dopaminergic neurons in the rat retina. J Neurochem 1982; 39: 283–285.

    Google Scholar 

  194. Sharma RK. Development and survival of tyrosine hydroxylase containing neurons in RCS rat retinae. Curr Eye Res 2001; 23: 256–262.

    Google Scholar 

  195. Ogilvie JM, Speck JD. Dopamine has a critical role in photoreceptor degeneration in the rd mouse. Neurobiol Dis 2002; 20: 33–40.

    Google Scholar 

  196. Roufail E, Rees S. Ageing has a differential effect on nitric oxide synthase-containing and catecholaminergic amacrine cells inthe humanand rat retina. J Comp Neur 1997; 389: 329–347.

    Google Scholar 

  197. Goettl VM, Wemlinger TA, Fong TG, Neff NH, Hadjiconstantinou M. Retinal cholinergic and dopaminergic deficits of aged rats are improved following treatment with GM1 ganglioside. Brain Res 2000; 877: 1–6.

    Google Scholar 

  198. Cellerino A, Kohler K. Brain-derived neurotrophic factor/neurotrophin-4 receptor TrkB is localized on ganglion cells and dopaminergic amacrine cells in the vertebrate retina. J Comp Neurol 1997; 386: 149–160.

    Google Scholar 

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Witkovsky, P. Dopamine and retinal function. Doc Ophthalmol 108, 17–39 (2004). https://doi.org/10.1023/B:DOOP.0000019487.88486.0a

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