Light-Induced Potential and Resistance Changes in Vertebrate Photoreceptors

  • Tsuneo Tomita
Part of the Handbook of Sensory Physiology book series (SENSORY, volume 7 / 2)


It has been established from ERG analyses that the cornea-negative component, the Pill of Granit, originates at least in part in the receptors themselves. (Concerning the background and present status of our knowledge, see Chapter 17.) Until just recently, however, a few points still remained to be explained. One of these was the unusual sign of the PIII, first pointed out by Granit (1947). While it is general that a receptor, when excited, forms an electric field of such sign as to make its distal end negative relative to the proximal end, and while this generality applies also to most invertebrate photoreceptors (see Section 7 of this Chapter), the polarity of the PIII is just opposite and is such as to shift the distal margin of the receptors positive, instead of negative. Another point requiring a reasonable account in assigning the PIII to the receptors was the parallel relation between the PIII and inhibition, well established also by Granit (1947). There is a building up of inhibition along with the PIII during photic stimulation, and the sudden destruction of the PIII at the termination of light results in a release of excitation. Does this then mean that the response to light of vertebrate photoreceptors is “inhibitory” in nature?


Outer Segment Receptor Potential Resistance Change Intracellular Recording Single Cone 
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  1. Arden, G.B., Ernst, W.: Mechanism of current production found in pigeon cones but not in pigeon or rat rods. Nature (Lond.) 223, 528–531 (1969).CrossRefGoogle Scholar
  2. Arden, G.B., Ernst, W.:The effect of ions on the photoresponses of pigeon cones. J. Physiol. (Lond.) 211, 311–339 (1970).Google Scholar
  3. Baylor, D. A., Fuortes, M. G. F.: Electrical responses of single cones in the retina of the turtle. J. Physiol. (Lond.) 207, 77–92 (1970).Google Scholar
  4. Baylor, D. A.,Fuortes, M. G. F.,O’Bryan, P.M.: Receptive fields of cones in the retina of the turtle. J. Physiol. (Lond.) 214, 265–294 (1971).Google Scholar
  5. Benolken, R.M.: Reversal of photoreceptor polarity recorded during the graded receptor potential response to light in the eye of Limulus. Biophys. J. 1, 551–564 (1961).PubMedCrossRefGoogle Scholar
  6. Bortoff, A.: Localization of slow potential responses in the Necturus retina. Vision Res. 4, 627–635 (1964).PubMedCrossRefGoogle Scholar
  7. Bortoff, A., Norton, A. L.: Simultaneous recording of photoreceptor potentials and the PIII component of the ERG. Vision Res. 5, 527–533 (1965a).PubMedCrossRefGoogle Scholar
  8. Bortoff, A., Norton, A. L.: Positive and negative potential responses associated with vertebrate photoreceptor cells. Nature (Lond.) 206, 626–627 (1965b).CrossRefGoogle Scholar
  9. Bortoff, A., Norton, A. L.: An electrical model of the vertebrate photoreceptor cell. Vision Res. 7, 253–263 (1967).PubMedCrossRefGoogle Scholar
  10. Brown, H.M., Hagiwara, S., Koike, H.,Meech, R.M.: Membrane properties of a barnacle photoreceptor examined by the voltage clamp technique. J. Physiol. 208, 385–413 (1970).PubMedGoogle Scholar
  11. Brown, K. T., Watanabe, K.: Isolation and identification of a receptor potential from the pure cone fovea of the monkey retina. Nature (Lond.) 193, 958–960 (1962).CrossRefGoogle Scholar
  12. Conn, H. J.: Biological Stains. 7th edition. Baltimore: Waverly 1961.Google Scholar
  13. Crescitelli, F.: The photosensitive retinal pigment system of Gekko gekko. J. gen. Physiol. 47, 33–52 (1963).PubMedCrossRefGoogle Scholar
  14. Eccles, J.C.: The Physiology of Synapses. Berlin-Heidelberg-New York: Springer 1964.CrossRefGoogle Scholar
  15. Frank, R.N., Goldsmith, T.H.: Effects of cardiac glycosides on electrical activity in the isolated retina of the frog. J. gen. Physiol. 50, 1585–1606 (1967).PubMedCrossRefGoogle Scholar
  16. Fuortes, M.G.F.: Initiation of impulses in visual cells of Limulus. J. Physiol. (Lond.) 148, 14–28 (1959).Google Scholar
  17. Furukawa, T., Hanawa, L: Effects of some common cations on electroretinogram of the toad. Jap. J. Physiol. 5, 289–300 (1955).CrossRefGoogle Scholar
  18. Granit, R.: Sensory Mechanisms of the Retina. London: Oxford Univ. Press 1947.Google Scholar
  19. Granit, R., Helme, T.: Changes in retinal excitability due to polarization and some observations on the relation between the processes in retina and nerve. J. Neurophysiol. 2, 556–565 (1939).Google Scholar
  20. Hagins, W.A.: Electrical signs of information flow in photoreceptors. Cold Spr. Harb. Symp. quant. Biol. 30, 403–418 (1965).Google Scholar
  21. Hagins,W.A., Adams, R.G.: The ionic basis of the receptor current of squid photoreceptors. Proc. 22nd Intern. Congr. Physiol. Sci. 2, 970 (1962).Google Scholar
  22. Hagins, W.A., Penn,R. D., Yoshikami, S.: Dark current and photocurrent in retinal rods. Biophys. J. 10, 380–412 (1970).PubMedCrossRefGoogle Scholar
  23. Hamasaki, D. I.: The effect of sodium ion concentration on the electroretinogram of the isolated retina of the frog. J. Physiol. (Lond.) 167, 156–168 (1963).Google Scholar
  24. Hamasaki, D. I.: The electroretinogram after application of various substances to the isolated retina. J. Physiol. (Lond.) 173, 449–458 (1964).Google Scholar
  25. Hanawa, I., Kuge, K., Matsumura,K.: Effects of some common ions on the transretinal de potential and the electroretinogram of the isolated frog retina. Jap, J. Physiol. 17, 1–20 (1967).Google Scholar
  26. Hanitzsch, R.,Trifonow, J.: Intraretinal abgeleitete ERG-Komponenten der isolierten Kaninchennetzhaut. Vision Res. 8, 1445–1455 (1968).PubMedCrossRefGoogle Scholar
  27. Hartline, H.K.,Ratliff, F., Miller,W.H.: Inhibitory interaction in the retina and its significance in vision. In: Florey, E. (Ed.). Nervous Inhibition. Oxford-London-New York-Paris: Pergamon Press 1961.Google Scholar
  28. Hecht, S., Shlaer, S., Pirenne, M.: Energy, quanta, and vision. J. gen. Physiol. 25, 819–840 (1942).PubMedCrossRefGoogle Scholar
  29. Katz, B.: The transmission of impulses from nerve to muscle, and the subcellular unit of synaptic action. Proc. roy. Soc. B 155, 455–479 (1962).CrossRefGoogle Scholar
  30. Kaneko, A.: Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina. J. Physiol. (Lond.) 207, 623–633 (1970).Google Scholar
  31. Kaneko, A.: Electrical connexions between horizontal cells in the dogfish retina. J. Physiol. (Lond.) 213, 95–105 (1971).Google Scholar
  32. Kaneko, A., Hashimoto, H.: Recording site of the single cone response determined by an electrode marking technique. Vision Res. 7, 847–851 (1967).PubMedCrossRefGoogle Scholar
  33. Kikuchi, R., Naito, K., Tanaka, I.: Effect of sodium and potassium ions on the electrical activity of single cells in the lateral eye of the horseshoe crab. J. Physiol. (Lond.) 161, 319–343 (1962).Google Scholar
  34. Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).PubMedCrossRefGoogle Scholar
  35. Marks, W.B.: Visual pigments of single goldfish cones. J. Physiol. (Lond.) 178, 14–32 (1965).Google Scholar
  36. Millecchia, R., Mauro, A.: The ventral photoreceptor cells of Limulus. III. A voltage-clamp study. J. gen. Physiol. 54, 331–351 (1969).PubMedCrossRefGoogle Scholar
  37. Murakami, M., Kaneko, A.: Differentiation of PIII subcomponents in cold-blooded vertebrate retinas. Vision Res. 6, 627–636 (1966).PubMedCrossRefGoogle Scholar
  38. Oikawa, T., Ogawa, T., Motokawa, K.: Origin of so-called cone action potential. J. Neurophysiol. 22, 102–111 (1959).PubMedGoogle Scholar
  39. Penn, R.D., Hagins, W.A.: Signal transmission along vertebrate photoreceptors and the a-wave of the ERG. Biophys. J., 9, 13th Ann. Meeting Abstr., A-244 (1969).Google Scholar
  40. Potter, D.D.,Furshpan, E.J., Lennox, E.S.: Connections between cells of the developing squid as revealed by electrophysiological methods. Proc. nat. Acad. Sci. (Wash.) 55, 328–336 (1966).CrossRefGoogle Scholar
  41. Purple, R.E.,Dodge,F. A.: Interaction of excitation and inhibition in the eccentric cell in the eye of Limulus. Cold Spr. Harb. Symp. quant. Biol. 30, 529–537 (1965).Google Scholar
  42. Rushton, W.A.H.: A theoretical treatment of Fuortes’s observations upon eccentric cell activity in Limulus. J. Physiol. (Lond.) 148, 29–38 (1959).Google Scholar
  43. Sillman, A. J., Ito,H., Tomita, T.: Studies on the mass receptor potential of the isolated frog retina. I. General properties of the response. Vision Res. 9, 1435–1442 (1969a).PubMedCrossRefGoogle Scholar
  44. Sillman, A. J., Ito,H., Tomita,T.: Studies on the mass receptor potential of the isolated frog retina. II. On the basis of the ionic mechanism. Vision Res. 9, 1443–1451 (1969b).PubMedCrossRefGoogle Scholar
  45. Skou, J.C.: Enzymic basis for active transport of Na+ and K+ across cell membrane. Physiol. Rev. 45, 596–617 (1965).Google Scholar
  46. Smith, T.G., Stell, W.K., Brown, J. E.: Conductance changes associated with receptor potentials in Limulus photoreceptors. Science 162, 454–456 (1968a).PubMedCrossRefGoogle Scholar
  47. Smith, T.G.,Stell, W.K.,Brown, J. E.,Freeman, J. A.,Murray, G.C.: A role for the sodium pump in photoreception in Limulus. Science 162, 456–458 (1968b).PubMedCrossRefGoogle Scholar
  48. Stretton, A.O.W., Kravitz, E.A.: Neuronal geometry: Determination with a technique of intracellular dye injection. Science 162, 132–134 (1968).PubMedCrossRefGoogle Scholar
  49. Svaetichin, G.: The cone action potential. Acta physiol. scand. 29, Suppl. 106, 565–600 (1953).Google Scholar
  50. Svaetichin, G.,Negishi, K.,Fatehchand, R.: Cellular mechanisms of a Young-Hering visual system. In: de Reuck, A.V.S., Knight, J. (Eds.): Colour Vision. Boston: Little, Brown Comp. 1965.Google Scholar
  51. Tomita, T.: Electrical activity in the vertebrate retina. J. Opt. Soc. Amer. 53, 49–57 (1963).CrossRefGoogle Scholar
  52. Tomita, T., Electrical response of single photoreceptors. Proc. IEEE 56, 1015–1023 (1968).CrossRefGoogle Scholar
  53. Tomita, T., Electrophysiological study of the mechanisms subserving color coding in the fish retina. Cold Spr. Harb. Symp. quant. Biol. 30, 559–566 (1965).Google Scholar
  54. Tomita, T., Electrical activity of vertebrate photoreceptors. Quart. Rev. Biophys. 3, 179–222 (1970).CrossRefGoogle Scholar
  55. Tomita, T.,Kaneko, A.: An intracellular coaxial microelectrode. Its construction and application. Med. Electron. Biol. Eng. 3. 367–376 (1965).PubMedCrossRefGoogle Scholar
  56. Tomita, T., Kaneko, A., Murakami, M., Pautler, E.L.: Spectral response curves of single cones in the carp. Vision Res. 7, 519–531 (1967).PubMedCrossRefGoogle Scholar
  57. Tomita, T., Murakami, M., Hashimoto, Y., Sasaki, Y.: Electrical activity of single neurons in the frog’s retina. In: Jung, R., Kornhuber, H. (Eds.): The Visual System: Neurophysiology and Psychophysics. Berlin-Heidelberg-New York: Springer 1961.Google Scholar
  58. Toyoda, J., Hashimoto, H., Anno, H., Tomita, T.: The rod response in the frog as studied by intracellular recording. Vision Res. 10, 1093–1100 (1970).PubMedCrossRefGoogle Scholar
  59. Toyoda, J., Nosaki, H., Tomita, T.: Light-induced resistance changes in single photoreceptors of Necturus and Gekko. Vision Res. 9, 453–463 (1969).PubMedCrossRefGoogle Scholar
  60. Walls, G.L.: The Vertebrate Eye and its Adaptive Radiation. New York: Hafner Publ. Co. 1963.Google Scholar
  61. Weinstein, G.W., Hobson, R.R., Dowling, J.E.: Light and dark adaptation in the isolated rat retina. Nature (Lond.) 215, 134–138 (1967).CrossRefGoogle Scholar
  62. Werblin, F.S.: Functional Organization of the Vertebrate Retina Studied by Intracellular Recording from the Retina of the Mudpuppy, Necturus maculosus. Doctoral Dissertation. The Johns Hopkins University, Baltimore 1968.Google Scholar
  63. Werblin, F.S., Dowling, J.E.: Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J. Neurophysiol. 32, 339–355 (1969).PubMedGoogle Scholar
  64. Witkovsky, P.: Peripheral mechanisms of vision. Ann. Rev. Physiol. 33, 257–280 (1971).CrossRefGoogle Scholar
  65. Yoshikami, S.,Hagins, W.A.: Ionic basis of dark current and photocurrent of retinal rods. 1969 Biophys. Soc. Abstr., 60a, WPM-13 (1970).Google Scholar
  66. Yoshikami, S., Hagins, W.A.: Light, calcium, and the photocurrent of rods and cones. 1971 Biophys. Soc. Abstr. 47 a, TPM-E16 (1971).Google Scholar

Copyright information

© Springer-Verlag, Berlin · Heidelberg 1972

Authors and Affiliations

  • Tsuneo Tomita
    • 1
    • 2
  1. 1.TokyoJapan
  2. 2.New HavenUSA

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