Electrophysiology of the Retina: Response to Stimulation and the Transduction Process

  • Hugh Davson


When a receptor is stimulated, a succession of electrical changes takes place in its conducting nerve fibre. These changes are measured by placing electrodes on the nerve fibre and connecting them to a device for recording rapidly occurring potential differences, an oscillograph. A series of electrical variations, called action potentials or ‘spikes’, is obtained when the receptor is stimulated. The duration of an individual spike is very short (it is measured in milliseconds) and, as the strength of the stimulus is increased, the frequency of the discharge (the number of spikes per second) increases, but the size of the individual spikes remains unaltered (‘all-or-none’ effect).


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  1. Bader, C. R., Macleish, P. R. & Schwartz, E. A. (1979) A voltage-clamp study of the light response in solitary rods of the tiger salamander. J. Physiol. 296, 1–26.Google Scholar
  2. Barlow, H. B., Fitzhugh, R. & Kuffer, S. W. (1957) Change of organization of the receptive fields of the cat’s retina during dark adaptation. J. Physiol. 137, 338–354.Google Scholar
  3. Bastian, B. L. & Fain, G. L. (1979) Light adaptation in toad rods: requirement for an internal messenger which is not calcium. J. Physiol. 297, 493–520.Google Scholar
  4. Bastian, B. L. & Fain, G. L. (1982) The effect of low calcium and background light on the sensitivity of toad rods. J. Physiol. 330, 307–328.Google Scholar
  5. Baylor, D. A. & Fuortes, M. G. F. (1970) Electrical responses of single cones in the retina of the turtle. J. Physiol. 207, 77–92.Google Scholar
  6. Baylor, D. A., Hodgkin, A. L. & Lamb, T. D. (1974) The electrical response of turtle cones to flashes and steps of light. J. Physiol. 242, 685–727.Google Scholar
  7. Baylor, D. A., Lamb, T. D. & Yau, K.-W. (1979a) The membrane current of single rod outer segments. J. Physiol. 288, 589–612.Google Scholar
  8. Baylor, D. A., Lamb, T. D. & Yau, K.-W.. (1979b) Responses of retinal rods to single photons. J. Physiol. 288, 613–634.Google Scholar
  9. Baylor, D. A., Matthews, G. & Yau, K.-W. (1980) Two components of electrical dark noise in toad retinal rod outer segments. J. Physiol. 309, 591–621.Google Scholar
  10. Baylor, D. A. & Nunn, B. J. (1986) Electrical properties of the light-sensitive conductance of rods of the salamander Ambystoma tigrinum. J. Physiol. 371, 115–145.Google Scholar
  11. Baylor, D. A., Nunn, B. J. & Schnapf, J. L. (1984) The photo-current, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J. Physiol. 357, 575–607.Google Scholar
  12. Behrens, M. E. & Wulff, V. J. (1965) Light-initiated responses of retinula and eccentric cells in the Limulus lateral eye. J. Gen. Physiol. 48, 1081–1093.Google Scholar
  13. Bennett, N., Michel-Villaz, M. & Kuhn, H. (1982) Light-induced interaction between rhodopsin and the GTP-binding protein. Metarhodopsin II is the major photoproduct involved. Eur. J. Biochem. 127, 97–103.Google Scholar
  14. Bignetti, E., Cavaggioni, A. & Sorbi, R. T. (1978) Light-activated hydrolysis of GTP and cyclic GMP in the rod outer segments. J. Physiol. 279, 55–69.Google Scholar
  15. Bodoia, R. D. & Detwiler, P. B. (1984) Patch-clamp recordings of the light-sensitive dark noise in retinal rods from lizard and frog. J. Physiol. 367, 183–216.Google Scholar
  16. Bortoff, A. & Norton, A. L. (1967) An electrical model of the vertebrate photoreceptor cell. Vision Res. 7, 253–262.Google Scholar
  17. Bowmaker, J. K. & Dartnall, H. J. A. (1980) Visual pigments of rods and cones in a human retina. J. Physiol. 298, 501–511.Google Scholar
  18. Bowmaker, J. K., Dartnall, H. J. A., Lythgoe, J. N. & Mollon, J. D. (1978) The visual pigments of rods and cones in the rhesus monkey, Macaca mulatta. J. Physiol. 274, 329–348.Google Scholar
  19. Bowmaker, J. K., Dartnall, H. J. A. & Mollon, J. D. (1980) Microspectrophotometric demonstration of four classes of photoreceptor in an old world primate Macaca fascicularis. J. Physiol. 298, 131–143.Google Scholar
  20. Brown, J. E. & Blinks, J. R. (1974) Changes in intracellular free calcium during illumination of invertebrate photoreceptors: detection with aequorin. J. Gen. Physiol. 64, 643–665.Google Scholar
  21. Brown, J. E., Brown, P. K. & Pinto, L. H. (1977) Detection of light-induced changes of intracellular ionized calcium concentration in Limulus ventral photoreceptors using arsenazo III. J. Physiol. 267, 299–320.Google Scholar
  22. Brown, J. E., Coles, J. A. & Pinto, L. H. (1977) Effects of injections of calcium and EGTA into the outer segments of retinal rods of Bufo marinus. J. Physiol. 269, 707–722.Google Scholar
  23. Brown, J. E., Kaupp, V. B. & Malbon, C. C. (1984) 3′-5′-cyclic adenosine monophosphate and adenylate cyclase in photo-transduction by Limulus photoreceptors. J. Physiol. 353, 523–539.Google Scholar
  24. Brown, J. E. & Pinto, L. H. (1974) Ionic mechanisms of the photoreceptor potential of the retina of Bufo marinus. J. Physiol. 236, 575–591.Google Scholar
  25. Capovilla, M., Cervetto, L. & Torre, V. (1983) The effect of phosphodiesterase inhibitors on the electrical activity of toad rods. J. Physiol. 343, 277–294.Google Scholar
  26. Caretta, A. & Cavaggioni, A. (1983) Fast ionic flux activated by cyclic GMP in the membrane of the cattle rod outer segments. Eur. J. Biochem. 132, 1–8.Google Scholar
  27. Caretta, A., Cavaggioni, A. & Sorbi, R. T. (1979) Cyclic GMP and the permeability of the discs of the frog photoreceptors. J. Physiol. 295, 171–178.Google Scholar
  28. Cervetto, L., Pasino, E. & Torre, V. (1977) Electrical responses of rods in the retina of Bufo marinus. J. Physiol. 267, 17–51.Google Scholar
  29. Clack, J. W., Oakley, B. & Stein, P. J. (1983) Injection of GTP-binding protein or cyclic GMP phosphodiesterase hyperpolarizes retinal rods. Nature 305, 50–53.Google Scholar
  30. Cobbs, W. H. & Pugh, E. N. (1985) Cyclic GMP can increase rod outer-segment light-sensitive current 10-fold without delay of excitation. Nature 313, 585–587.Google Scholar
  31. Cote, R. H., Biernbaum, M. S., Nicol, G. D. & Bownds, M. D. (1984) Light-induced decreases in cGMP concentration precede changes in membrane permeability in frog rod photoreceptors, J. Biol. Chem. 259, 9635–9641.Google Scholar
  32. Crawford, B. H. (1949) The scotopic visibility function. Proc. Phys. Soc. B 62, 321–334.Google Scholar
  33. Detwiler, P. B., Hodgkin, A. L. & McNaughton, P. A. (1980) Temporal and spatial characteristics of the voltage response of rods in the retina of the snapping turtle. J. Physiol. 300, 213–250.Google Scholar
  34. DeValois, R. L., Morgan, H. C., Polson, M. C., Mead, W. R. & Hull, E. M. (1974) Psychophysical studies of monkey vision. I. Macaque luminosity and color vision tests. Vision Res. 14, 53–67.Google Scholar
  35. Dixon, R. A. F. et al. (1986) Cloning of the gene and a DNA for mammalian β-adrenergic receptor and homology with rhodopsin. Nature 321, 75–79.Google Scholar
  36. Dowling, J. E. & Werblin, F. S. (1969) Organization of the retina of the mudpuppy, Necturus maculosus. I. Synaptic structure. J. Neurophysiol. 32, 315–335.Google Scholar
  37. Emeis, D., Kuhn, H., Reichert, J. & Hofmann, K. P. (1982) Complex formation between metarhodopsin II and GTP-binding protein in bovine photoreceptor membranes leads to a shift of the photoproduct equilibrium. FEBS Letters 143, 29–34.Google Scholar
  38. Enroth-Cugell, C. & Robson, J. G. (1984) Functional characteristics and diversity of cat retinal ganglion cells. Invest. Ophthal. 25, 250–267.Google Scholar
  39. Farber, D. B. & Lolley, R. N. (1977) Light-induced reduction in cyclic GMP of retinal photoreceptor cells in vivo: abnormalities in the degenerative diseases of RCS rats and rd mice. J. Neurochem. 28, 1089–1095.Google Scholar
  40. Fesenko, E. E., Kolesnikov, S. S. & Lyubarsky, A. L. (1985) Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313, 31–313.Google Scholar
  41. Frank, R. N. & Goldsmith, T. H. (1967) Effects of cardiac glycosides on electrical activity in the isolated retina of the frog. J. Gen. Physiol. 50, 1585–1606.Google Scholar
  42. Fung, B. K.-K., Hurley, J. B. & Stryer, L. (1981) Flow of information in the light-triggered cyclic nucleotide cascade of vision. Proc. Nat. Acad. Sci. 78, 152–156.Google Scholar
  43. Fung, B. K.-F. & Stryer, L. (1980) Photolyzed rhodopsin catalyzes the exchange of GTP for bound GDP in retinal rod outer segments. Proc. Nat. Acad. Sci. 77, 2500–2504.Google Scholar
  44. Fuortes, M. G. F. (1959) Initiation of impulses in visual cells of Limulus. J. Physiol. 148, 14–28.Google Scholar
  45. Fuortes, M. G. F. & Hodgkin, A. L. (1964) Changes in time scale and sensitivity in the ommatidium of Limulus. J. Physiol. 172, 239–263.Google Scholar
  46. Goldberg, N. D., Ames, A., Gander, J. E. & Walseth, T. F. (1983) Magnitude of increase in retinal cGMP metabolic flux determined by 13O incorporation into nucleotide α-phosphoryl compounds with intensity of photic stimulation. J. Biol. Chem. 258, 9213–9219.Google Scholar
  47. Gold, G. H. & Korenbrot, J. I. (1980) Light-induced calcium release by intact retinal rods. Proc. Nat. Acad. Sci. 77, 5557–5561.Google Scholar
  48. Granit, R. (1947) Receptors and Sensory Perception. Newhaven: Yale University Press.Google Scholar
  49. Granit, R. (1955) Receptors and Sensory Perception. New Haven: Yale University Press.Google Scholar
  50. Gray, P. & Attwell, D. (1985) Kinetics of light-sensitive channels in vertebrate photoreceptors. Proc. Roy. Soc. B 223, 379–388.Google Scholar
  51. Greenblatt, R. E. (1983) Adapting lights and lowered extracellular free calcium desensitize toad photoreceptors by differing mechanisms. J. Physiol. 336, 579–605.Google Scholar
  52. Hagins, W. A., Penn, R. D. & Yoshikami, S. (1970) Dark current and photocurrent in retinal rods. Biophys. J. 10, 380–412.Google Scholar
  53. Hagins, W. A. & Yoshikami, S. (1977) In Vertebrate Photoreceptors. Ed. Barlow, H. B. & Fatt, P. Academic Press, London. (Quoted by Matthews et al., 1985.)Google Scholar
  54. Hartline, H. K. (1940) The nerve messages in the fibres of the visual pathway. J. Opt. Soc. Amer. 30, 239–247.Google Scholar
  55. Hartline, H. K. (1941/2) The neutral mechanisms of vision. Harvey Lectures, Ser. 37, 39–68.Google Scholar
  56. Haynes, L. & Yau, K.-W. (1985) Cyclic GMP sensitive conductance in outer segment membrane of catfish cones. Nature 317, 61–64.Google Scholar
  57. Hemilä, S. & Reuter, T. (1981) Longitudinal spread of adaptation in the rods of the frog’s retina. J. Physiol. 310, 501–528.Google Scholar
  58. Hodgkin, A. L., McNaughton, P. A. & Nunn, B. J. (1985) The ionic selectivity and calcium dependence of the light-sensitive pathway in toad rods. J. Physiol. 358, 447–468.Google Scholar
  59. Katz, B. & Miledi, R. (1972) The statistical nature of the acetylcholine potential and its molecular components. J. Physiol. 224, 665–699.Google Scholar
  60. Kawamura, S. & Bownds, M. D. (1981) Light adaptation of the cyclic GMP phosphodiesterase of frog photoreceptor membranes mediated by ATP and calcium ions. J. Gen. Physiol. 77, 571–591.Google Scholar
  61. Korenbrot, J. I., Brown, D. T. & Cone, R. A. (1973) Membrane characteristics and osmotic behaviour of isolated rod outer segments. J. Cell Biol. 56, 389–398.Google Scholar
  62. Korenbrot, J. I. & Cone, R. A. (1972) Dark ionic flux and the effects of light in isolated rod outer segments. J. Gen. Physiol. 60, 20–45.Google Scholar
  63. Kuffler, S. W. (1953) Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. 16, 37–68.Google Scholar
  64. Kuhn, H. (1978) Light-regulated binding of rhodopsin kinase and other proteins to cattle photoreceptor membranes. Biochemistry 17, 4389–4395.Google Scholar
  65. Kühn, H. (1980) Light- and GTP-regulated interaction of GTPase and other proteins with bovine photoreceptor membranes. Nature 283, 588–590.Google Scholar
  66. Kühn, H., Bennett, N., Michet-Villaz, M. & Chabre, M. (1981) Interactions between photoexcited rhodopsin and GTP-binding protein: kinetic and stoichiometric analyses from light-scattering changes. Proc. Nat. Acad. Sci. 78, 6873–6877.Google Scholar
  67. Lamb, T. D., McNaughton, P. A. & Yau, K. W. (1981) Spatial spread of activation and background desensitization in toad rod outer segments. J. Physiol. 319, 463–496.Google Scholar
  68. Liebman, P. A. & Pugh, E. N. (1980) ATP mediates rapid reversal of cyclic GMP phosphodiesterase activation in visual receptor membranes. Nature 287, 734–736.Google Scholar
  69. Lipton, S.A., Ostroy, S.E. & Dowling, J.E. (1977) Electrical and adaptive properties of rod photoreceptors in Bufo marinus. J. Gen. Physiol. 70, 747–770.Google Scholar
  70. Lisman, J. E. & Brown, J. E. (1972) The effects of intracellular iontophoretic injection of sodium and calcium ions on the light response of Limulus ventral photoreceptors. J. Gen. Physiol. 59, 701–719.Google Scholar
  71. Lisman, J. E. & Strong, J. A. (1979) The initiation of excitation and light adaptation in Limulus ventral photoreceptors. J. Gen. Physiol. 73, 219–243.Google Scholar
  72. Lolley, R. N. & Racz, E. (1982) Calcium modulation of cyclic GMP synthesis in rat visual cells. Vision Res. 22, 1481–1486.Google Scholar
  73. MacLeish, P. R. M. Schwartz, E. A. & Tachibana, M. (1984) Control of the generator current in solitary rods of Ambystoma tigrinum retina. J. Physiol. 348, 645–664.Google Scholar
  74. Matthews, G. & Watanabe, S.-I. (1987) Properties of ion channels closed by light and opened by guanosine 3′-5′-cyclic monophosphate in toad retinal rods. J. Physiol. 389, 691–715.Google Scholar
  75. Matthews, H. R., Torre, V. & Lamb, T. D. (1985) Effects on the photoresponse of calcium buffers and cyclic GMP incorporated into the cytoplasm of retinal rods. Nature313, 582–585.Google Scholar
  76. McDowell, J. H. & Kühn, H. (1977) Light induced phosphorylation of rhodopsin in cattle photoreceptor membranes: substrate activation and inactivation. Biochemistry 16, 4054–4060.Google Scholar
  77. McNaughton, P. A., Cervetto, L. & Nunn, B. J. (1986) Measurement of the intracellular free calcium concentration in salamander rods. Nature 322, 261–263.Google Scholar
  78. Meyertholen, E. P., Wilson, M. J. & Ostroy, S. E. (1986) The effects of HEPS, bicarbonate and calcium on the GMP content of vertebrate rod photoreceptors and the isolated electrophysiologic effects and calcium. Vision Res. 26, 521–533.Google Scholar
  79. Naka, K. I. & Rushton, W. A. H. (1966) S-potentials from colour units in the retina of the fish (Cypridinae). J. Physiol. 185, 536–555.Google Scholar
  80. Penn, R. D. & Hagins, W. A. (1969) Signal transmission along vertebrate rods and the origin of the electroretinographic a-wave. Nature 233, 201–205.Google Scholar
  81. Pugh, E. N. & Cobbs, W. H. (1986) Visual transduction in vertebrate rods and cones: a tale of two transmitters, calcium and cyclic GMP. Vision Res. 26, 1613–1649.Google Scholar
  82. Schwartz, E. A. (1973) Organization of ON-OFF cells in the retina of the turtle. J. Physiol. 230, 1–14.Google Scholar
  83. Schwartz, E. A. (1974) Responses of bipolar cells in the retina of the turtle. J. Physiol. 236, 211–224.Google Scholar
  84. Schwartz, E. A. (1975a) Responses of single rods in the turtle. J. Physiol. 232, 503–514.Google Scholar
  85. Schwartz, E. A. (1975b) Rod-rod interaction in the retina of the turtle. J. Physiol. 246, 617–638.Google Scholar
  86. Schwartz, E. A. (1975c) Cones excite rods in the retina of the turtle. J. Physiol. 246, 639–651.Google Scholar
  87. Schwartz, E. A. (1976) Electrical properties of the rod syncytium in the retina of the turtle. J. Physiol. 257, 379–406.Google Scholar
  88. Schwartz, E. A. (1985) Phototransduction in vertebrate rods. Ann. Rev. Neurosci. 8, 339–367.Google Scholar
  89. Sitaramayya, A. & Liebman, P. A. (1983a) Mechanism of ATP quench of phosphodiesterase activation in rod disc membranes. J. Biol. Chem. 258, 1205–1209.Google Scholar
  90. Sitaramayya, A. & Liebman, P. A. (1983b) Phosphorylation of rhodopsin and quenching of cyclic GMP phosphodiesterase activation by ATP at weak bleaches. J. Biol. Chem. 258, 12106–12109.Google Scholar
  91. Smith, T. G., Baumann, F. & Fuortes, M. G. F. (1965) Electrical connexions between visual cells in the ommatidium of Limulus. Science 147, 1446–1447.Google Scholar
  92. Stryer, L. (1986) Cyclic GMP cascade in vision. Annu. Rev. Neurosci. 9, 87–119.Google Scholar
  93. Stryer, L., Hurley, J. B. & Fung, B. K.-K. (1981) Transducin: an amplifier protein in vision. Trends Biochem. Sci. 6, 245–247.Google Scholar
  94. Tomita, T., Kikuchi, R. & Tanaka, I. (1960) Excitation and inhibition in lateral eye of horseshoe crab. In Electrical Activity of Single Cells, Ed. Y. Katsuki, pp. 11–23. Tokyo: I. Shoin.Google Scholar
  95. Torre, V., Matthews, H. R. & Lamb, T. D. (1986) Role of calcium in regulating the cyclic GMP cascade of phototransduction in retinal rods. Proc. Nat. Acad. Sci. 83, 7109–7113.Google Scholar
  96. Toyoda, J., Nosaki, H. & Tomita, T. (1969) Light-induced resistance changes in single receptors of Necturus and Gecko. Vision Res 9, 453–463.Google Scholar
  97. Wald, G. (1968) The molecular basis of visual excitation. Nature 219, 800–807.Google Scholar
  98. Werblin, F. S. & Dowling, J. E. (1969) Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J. Neurophysiol. 32, 339–354.Google Scholar
  99. Woodruff, M. I. & Bownds, M. D. (1979) Amplitude, kinetics, and reversibility of a light-induced decrease in guanosine 3′,5′- cyclic monophosphate in frog photoreceptor membranes. J. Gen. Physiol.73, 629–653.Google Scholar
  100. Yau, K. W. & Nakatani, K. (1984) Electrogenic Na-Ca exchange in retinal rod outer segment. Nature 311, 661–663.Google Scholar
  101. Yau, K. W. & Nakatani, K. (1985a) Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment. Nature 313, 579–582.Google Scholar
  102. Yau, K. W. & Nakatani, K. (1985b) Light-suppressible, cyclic GMP-sensitive conductance in the plasma membrane of a truncated rod outer segment. Nature 317, 252–255.Google Scholar
  103. Yee, R. & Liebman, P.A. (1978) Light-activated phosphodiesterase of the rod outer segment. J. Biol. Chem. 253, 8902–8909.Google Scholar
  104. Yoshikama, S. & Hagins, W. A. (1973) Control of the dark current in vertebrate rods and cones. In Biochemistry and Physiology of the Visual PigmentsGoogle Scholar
  105. Zimmerman, A. L. & Baylor, D. A. (1986) Cyclic GMP-sensitive conductance of retinal rods consists of aqueous pores. Nature 321, 70–72.Google Scholar
  106. Zuckerman, R., Buzdygon, B., Philp, N., Liebman, P. & Sitaramayya, A. (1985) Arrestin: an ATP/ADP exchange protein that regulates cGMP phosphodiesterase activity in retinal rod disk membranes (RDM). Biophys. J. 47, 37a.Google Scholar
  107. Zuckerman, R., Schmidt, G. J. & Dacko, S. M. (1983) Rhodopsin-to-metarhodopsin II transition triggers amplified changes in cytosol ATP and ADP in intact retinal rod outer segments. Proc. Nat. Acad. Sci. 79, 6414–6418.Google Scholar

Copyright information

© Hugh Davson 1990

Authors and Affiliations

  • Hugh Davson
    • 1
    • 2
    • 3
  1. 1.St. Thomas’s HospitalSouthampton University Medical SchoolsLondonUK
  2. 2.King’s CollegeLondonUK
  3. 3.University CollegeLondonUK

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