Push-Pull Model of Dopamine’s Action in the Retina

  • Iván Bódis-Wollner
  • Areti Tzelepi
Part of the Topics in Biomedical Engineering International Book Series book series (TOBE)


Although our knowledge of the interactive connections in the mammalian retina has greatly expanded over the last 20 years, the exact wiring and functional role of this complex network has not yet been elucidated. Ganglion cells receive input from the vertical pathways (photoreceptors — bipolar cells — ganglion cells) and lateral pathways (photoreceptors — horizontal cells — bipolar cells — amacrine cells) of retinal interneurons (Werblin and Dowling, 1969). Contrary to the ganglion cell responses which can be recorded from the optic nerve, the three classes of retinal interneurons (horizontal, amacrine and bipolar cells) are not easily accessible and recordings are further limited by their small size, especially in higher vertebrates. Together with photoreceptors and the ganglion cells, they make up the complex network of the mammalian retina. Ganglion cells have a characteristic center-surround antagonistic organization in their receptive fields (Kuffler, 1953; Rodieck and Stone, 1966; Enroth-Cugell and Robson, 1966) (Fig. 5.1). It has been shown, however, that bipolar neurons of the primate, which precede ganglion cells in the vertical pathway, also have surrounds (Dacey et al, 2000).


Spatial Frequency Ganglion Cell Receptive Field Bipolar Cell Amacrine Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Barlow, H.B., and Hill, R.M., 1963, Selective sensitivity to direction of movement in ganglion cells of the rabbit retina, Science. 139: 412–414.CrossRefGoogle Scholar
  2. Baylor, D.A., Fuortes, M.G.F., and O’Bryan, P.M., 1971, Receptive fields of the cones in the retina of the turtle, J. Physiol. (Lond.) 214: 265–294.Google Scholar
  3. Bodis-Wollner, I., 1972, Visual acuity and contrast sensitivity in patients with cerebral lesions, Science. 178: 769–771.CrossRefGoogle Scholar
  4. Bodis-Wollner, I., and Camisa, J.M., 1980, Conrast sensitivity in clinical diagnosis, in: Neuro-opthalmology, Lessell, S., Van Dalen, J.T.W., eds., Elsevier Science, Amsterdam, pp. 373–401.Google Scholar
  5. Bodis-Wollner, I., Marx, M., and Ghilardi, M.F., 1989, Systematic Haloperidol administration increases the amplitude of the light and dark adapted flash ERG in the monkey, Clin. Vis. Sci. 4: 19–26.Google Scholar
  6. Bodis-Wollner, I., 1990, Visual deficits related to dopamine deficiency in experimental animals and Parkinson’s disease patients. Trends Neurosci. 13: 296–302.CrossRefGoogle Scholar
  7. Bodis-Wollner, I., Tagliati, M., Peppe, A., and Antal, A., 1993, Visual and visual perceptual disorders in neurodegenerative diseases, Bailliere’s Clinical Neurology. 2: 461–490.Google Scholar
  8. Midis Wollner, I., 1996, Electrophysiological assessment of retinal dopaminergic deficiency, Fund. Neurosci. 46: 35–41.Google Scholar
  9. Bodis -Wollner, I., and Tzelepi, A., 1998, The push-pull action of dopamine on spatial tuning of the monkey retina: the effects of dopaminergic deficiency and selective D1 and D2 receptor ligands on the pattern electroretinogram, Vis. Res. 38: 1479–1487.CrossRefGoogle Scholar
  10. Boycott, B.B., and Wassle, H., 1974, The morphological types of ganglion cells of the domestic cat’s retina, J. Physiol. (Lond.) 240: 397–419.Google Scholar
  11. Boycott, B.B., and Wassle, H., 1991, Morphological classification of bipolar cells of the primate retina, Eur. J. Neurosci. 3: 1069–1088.CrossRefGoogle Scholar
  12. Burns, R.S., Chiuech, C.C., Markey, S., Ebert, M.H., Jacobowitz, D.M., and Kopin, J., 1983, A primate model of Parkinson’s disease: selective destruction of substantia nigra pars compacta dopaminergic neurons by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine, Proc. Natl. Acad. Sci. USA 80: 4546–4550.CrossRefGoogle Scholar
  13. Cleland, B.G., and Levick, W.R., 1974, Properties of rarely encountered types of ganglion cells in the cat’s retina, J. Physiot(Lond.) 240: 457–492.Google Scholar
  14. Cohen, J.L., and Dowling, J.E., 1983, The role of the retinal interplexiform cell: effects of 6- hydroxydopamine on the spatial properties of carp horizontal cells, Brain Res. 264: 307–310.CrossRefGoogle Scholar
  15. Dacey, D., Packer, O., Diller, L., Brainard, D., Peterson, B., and Lee, B., 2000, Center surround receptive field structure of cone bipolar cells in the primate retina, Vis. Res. 40: 1801–1811.CrossRefGoogle Scholar
  16. Dacey, D.M., 1993, The mosaic of midget ganglion cells in the human retina. J. Neurosci. 13: 5334–5355.Google Scholar
  17. Davis, G.C., Williams A.C., Markey, S.P., Ebert, M.H., Caine, E.D., Reichert, C.M., and Kopin I.J., 1979, Chronic parkinsonisms secondary to intravenous injections of meperidine analogues, Psychiatry Res. 1: 249–254.CrossRefGoogle Scholar
  18. De Monasterio, F.M., and Gouras, P., 1975, Functional properties of ganglion cells of the rhesus monkey retina. J. Physiol. (Lond.) 251: 167–195.Google Scholar
  19. Djamgoz, M.B.A., and Kolb, H., 1993, Ultrastructural and functional connectivity of intracellularly stained neurons in the vertebrate retina: correlative analyses, Microsc. Res. Tech. 24: 43–66.CrossRefGoogle Scholar
  20. Enroth-Cugell, C., and Robson, J.G., 1966, The contrast sensitivity of retinal ganglion cells of the cat, J. Physiol.(Land) 187: 517–552.Google Scholar
  21. Fukuda, Y., Hsiao, C.F., Watanabe, M., and Ito, H., 1984, Morphological correlates of physiologically identified Y-, X-, and W-cells in cat retina. J. Neurophysiol. 52: 999–1013.Google Scholar
  22. Fukuda, Y., Hsiao, C.F., and Watanabe, M., 1985, Morphological correlates of Y, X and W type ganglion cells in the cat’s retina, Vis. Res. 25: 319–27.CrossRefGoogle Scholar
  23. Gerschenfeld, H.M., Neyton, J., Piccolino, M., and Witkovsky, P., 1982, L-horizontal cells of the turtle: network organization and coupling modulation, Biomed Res. 3: 21–32.Google Scholar
  24. Ghilardi, M.F., Bodis-Wollner, I., Onofrj, M.C., Marx, M.S., and Glover AA., 1988, Spatial frequency-dependent abnormalities of the pattern electroretinogram and visual evoked potentials in a Parkinsonian monkey model, Brain. 11: 131–184.CrossRefGoogle Scholar
  25. Ghilardi, M.F., Marx, M.X., Bôdis-Wollner, I., Camras, C.B., and Glover, A., 1989, The effect of intraocular 6-hydroxydopamine on retinal processing of primates, Ann. NeuroL 25: 359–364.Google Scholar
  26. Grzywacz, N.M., Merwine, D.K., and Amthor, F.R., 1998, Complementary roles of two excitatory pathways in retinal directional selectivity, Vis Neurosci. 15: 1119–1127.Google Scholar
  27. Hampson, E.C., Vaney, D.I., and Weiler, R., 1992, Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. J. Neurosci. 12: 4911–4922.Google Scholar
  28. Hankins, M.W., and Ikeda, H., 1991, The role of dopaminergic pathways at the outer plexiform layer of the mammalian retina, Clin. Vis. Sci. 6: 87–93.Google Scholar
  29. He, S., and Masland, RH., 1997, Retinal direction selectivity after targeted laser ablation of starburst amacrine cells, Nature. 389: 378–382.CrossRefGoogle Scholar
  30. Jensen, R.J., and Daw, N.W., 1986, Effects of dopamine and its agonists and antagonists on the receptive field properties of ganglion cells in the rabbit retina, Neurosci. 17: 837–855.CrossRefGoogle Scholar
  31. Kamermans, M., and Spekreijse, H., 1999, The feedback pathway from horizontal cells to cones — A mini review with a look ahead, Vis. Res. 39: 2449–2468.CrossRefGoogle Scholar
  32. Kaplan, E., and Shapley, R.M., 1986, The primate retina contains two types of ganglion cells with high and low contrast sensitivity, Proc. NatL Acad. Sci. USA 83: 2755–2757.CrossRefGoogle Scholar
  33. Kolb, H., Nelson, R., and Mariani A., 1981, Amacrine cells, bipolar cells and ganglion cells of the cat retina: a Golgi study, Vis. Res. 21: 1081–1114.CrossRefGoogle Scholar
  34. Kolb, H., Linberg, K.A., and Fisher, S.K., 1992, Neurons of the human retina: A Golgi study, J. Comp. Neurol. 31: 147–187.CrossRefGoogle Scholar
  35. Kuffler, S.W., 1953, Discharge patterns and functional organization of mammalian retina, Neurophysiol. 16: 37–68.Google Scholar
  36. Lasater, E.M., and Dowling, J.E., 1985, Dopamine decreases conductance of the electrical junctions between cultured retinal horizontal cells, Proc. Natl. Acad. Sci. USA 82: 3025–3029.CrossRefGoogle Scholar
  37. Maffei, L., and Fiorentini, A., 1981, Electroretinographic responses to alternating gratings before and after section of the optic nerve, Science. 211: 953–955.CrossRefGoogle Scholar
  38. Maffei, L., Fiorentini, A., Bisti, S., and Hollander, H., 1985, Pattern ERG in the monkey after section of the optic nerve, Exp. Brain. Res. 59: 423–425.Google Scholar
  39. Maguire, G.W., and Hamasaki, D.I., 1994, The retinal dopamine network alters the adaptational properties of retinal ganglion cells in the cat, J. Neurophysiol. 72: 730–741.Google Scholar
  40. Maguire, G.W., and Smith, E.L.III., 1985, Cat retinal ganglion cell receptive-field alterations after 6-hydroxydopamine induced doparninergic amacrine cell lesions, J. NeurosphysioL 53: 1431–43.Google Scholar
  41. Mangel, S.C., and 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 Scholar
  42. Mariani, A.P., 1990 Amacrine cells of the rhesus monkey retina, J. Comp. Neural. 301: 382–400.CrossRefGoogle Scholar
  43. Marx, A.Ö.Q, Wang, R.F., and Severin, C., 1988. Signs of early damage in glaucomatous monkey eyes: low spatial frequency losses in the pattern ERG and VEP, Exp Eye Res 46: 173–184.CrossRefGoogle Scholar
  44. Matsumoto, N., and Nalca, K.I., 1972, Identification of intracellular responses in the frog retina, Brain Res. 42: 59–71.CrossRefGoogle Scholar
  45. Nguyen-Legros, J., Versaux-Botteri, C., and Vernier, P., 1999, Doparnine receptor localization in the mammalian retina, Mol. Neurobiol. 19: 181–204.CrossRefGoogle Scholar
  46. Ninldas.YK. Youngster, S., Liodt, M.V, 1887. Molecular mechanisms of MPTP induced toxicity.LV. MPTP, MPP+ and mitochondrial function, Life Sci, 40: 72l-729.Google Scholar
  47. Oliver, P., Jolicoeur, F.B., Lafond, B., Drumheller AI. and Brunette, IR, 1986, Dose related effects of 6-OHDA on rabbit retinal dopaniìne concentrations and ERG b-wave amplitudes, Brain Res. Bull. 16: 751–753.CrossRefGoogle Scholar
  48. Pppe.A, Aoual, A, Togliuti, M, 1990. DmêonistCY 208–243 attenuates the pattern electroretinogram to low spatial frequency stimuli in the monkey, Neurosci Lett. 242: 1–4.Google Scholar
  49. Picuuöun.Y, DcKÖondo.G, Yitkovoky, P, Südo-Wollnnr, I., 1987. Dl and D2 dopamine receptors involved in the control of electrical transmission between retinal horizontal cells, in: Symposia in Neuroscience: Central and Peripheral DopumivxngicBooepumrs,. Liviana Press Padova, pp. 1–12.Google Scholar
  50. Uon, Y., Witkmky, P., and Trimarchi C., 1987, Dopaminergic mechanisms underlying the reduction of electrical coupling between horizontal cells of the turtle retina induced by d’amphetuobno, biovcünc, and verutridino.Jevni 7: 2273–2284.Google Scholar
  51. Regan, D..Kvthu, C. and Sharpe, A.. 1991, Recognition of motion-defined shapes in patients with multiple sclerosis and optic neuritis. Brain. 114: 1129–1155.Google Scholar
  52. Rodieck, R.W., and Stone, J., 1965, Analysis of receptive fields of cat retinal ganglion cells, J. Neurophysiol. 28: 833–849.Google Scholar
  53. Qodinuk.R.YV,8ioomodur.K.P, and Dineen, J, 1985, Parasol and midget ganglion cells of the human retina, Comp. Nepnol 33: 5-132.Google Scholar
  54. Schwartz, E.A., 1974, Response of bipolar cells in the retina of the turtle. Physiol.(Lond) 236: 211–224.Google Scholar
  55. Shapley, R., and Perry V.H., 1986, Ca and monkey retinal ganglion cells and their visual functional roles, Trends Neurosci. 9: 229–235.CrossRefGoogle Scholar
  56. Tugimb.M, and Suanzionc.P. 1994, Spatial frequency tuning in the monkey retina depends on D2 receptor-linked action of doparnine, Vis. Res. 34: 2051–2057.CrossRefGoogle Scholar
  57. Tniab.M, Yubr, Y.D, 1996. The pattern electroretinogram in Parkinson’s disease reveals lack of retinal spatial tuning, Electroenceph. Clinic. Neurophysiol. 100: 1–11.CrossRefGoogle Scholar
  58. Teranishi, T., Negishi, K., and Kato, S., 1983, Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina, Nature. 301: 243–246.CrossRefGoogle Scholar
  59. Teranishi, T., Negishi, K., and Kato, S., 1984, Regulatory effect of dopamine on spatial properties of horizontal cells in carp retina, J. Neurosci. 4: 1271–1280.Google Scholar
  60. Ungerstedt, U., and Arbuthnott, G.W., 1970, Quantitative recording of rotational behavior in rats uftohydmxydopuodno lesions of the nigrostriatal dopamine system, Brain Res. 24: 485–493.CrossRefGoogle Scholar
  61. Vaney, D.I., 1994, Patterns of neuronal coupling in the retina, Prog. Ret. Eye Res. 13: 301–355.CrossRefGoogle Scholar
  62. Vaney, D.I., 1990, The mosaic of amacrine cells in the mammalian retina, Prog. Ret. Res. 9: 49–100.CrossRefGoogle Scholar
  63. Vardi, N., and Smith, R.G., 1996, The All amacrine network: coupling can increase correlated activity, Vis. Res. 36: 3743–3757.CrossRefGoogle Scholar
  64. Werblin, F.S., and Dowling, J.E., 1969, Organization of the retina of the mudpuppy, Necturus maculosus II. Intracellular recording, J. Neurophysiol. 32: 339–355.Google Scholar
  65. Witkovsky, P., Alones, V., and Piccolino, M., 1987, Morphological changes induced in turtle retinal neurons by exposure to to 6-hydroxydopamine and 5,6-hycoxytryptamine, J. Neurocytol. 16: 55–67.CrossRefGoogle Scholar
  66. Wong, C., Ishibashi, T., Tucker, G., and Hamasaki, D., 1984, Responses of the pigmented rabbit retina to NMPTP, a chemical inducer of Parkinsonism, Exp. Eye Res. 40: 509–519.CrossRefGoogle Scholar
  67. Xin, D., and Bloomfield, S.A., 1999, Dark-and light-induced changes in coupling between horizontal cells in mammalian retina, J. Comp. Neurol. 405: 75–87.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Iván Bódis-Wollner
    • 1
  • Areti Tzelepi
    • 1
    • 2
  1. 1.Department of NeurologyState University of N.York, Health Science Center at BrooklynBrooklynUSA
  2. 2.Dept. of Computer ScienceHellenic Naval AcademyPiraeusGreece

Personalised recommendations