The cGMP-Gated Channels of Rod and Cone Photoreceptors

  • Lawrence W. Haynes
  • King-Wai Yau
Part of the Series of the Centro de Estudios Científicos de Santiago book series (SCEC)


Light generates a hyperpolarizing response in retinal photoreceptors by stopping a steady inward current (the dark current) that is present at their outer segments in darkness.(1–3) The mechanism underlying this phototransduction process has been a subject of intense interest and controversy for many years, and is only now becoming fairly clear. The present picture for rods(4–6) is that upon absorbing a photon a visual pigment molecule isomerizes and catalytically activates a GTP-binding protein (also called G-protein) that is bound peripherally to disk membranes within the outer segment. The activated G-protein in turn stimulates a phosphodiesterase that hydrolyzes cGMP, a cyclic nucleotide known to be present at a high concentration in the outer segment. In darkness, this high cGMP level maintains a plasma membrane cationic conductance (the light-regulated conductance) in the open state, thus sustaining the dark current. In the light, the fall in the cGMP level leads to the closure of this conductance, and therefore the cessation of the dark current. This picture for phototransduction in rods now seems to apply to cones as well,(7) despite their different surface membrane geometries.


Divalent Cation Dark Current Outer Segment Tiger Salamander cGMP Concentration 
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. 1.
    Tomita, T., 1970, Electrical activity of vertebrate photoreceptors, Quart. Rev. Biophys. 3: 179–222.CrossRefGoogle Scholar
  2. 2.
    Hagins, W. A., Perm, R. D., and Yoshikami, S., 1970, Dark current and photocurrent in retinal rods, Biophys. J. 10: 380–412.PubMedCrossRefGoogle Scholar
  3. 3.
    Baylor, D. A., Lamb, T. D., and Yau, K.-W., 1979, The membrane current of single rod outer segments, J. Physiol. 288: 589–611.PubMedGoogle Scholar
  4. 4.
    Pugh, Jr., E. N., and Cobbs, W. H., 1986, Visual transduction in vertebrate rods and cones: A tale of two transmitters, calcium and cyclic-GMP, Vision Res. 26: 1613–1643.PubMedCrossRefGoogle Scholar
  5. 5.
    Stryer, L., 1986, Cyclic GMP cascade in vision, Ann. Rev. Neurosci. 9: 87–119.PubMedCrossRefGoogle Scholar
  6. 6.
    Yau, K.-W., and Baylor, D. A., 1989, Cyclic-GMP-activated conductance of retinal photoreceptor cells, Ann. Rev. Neurosci. 12: 289–327.PubMedCrossRefGoogle Scholar
  7. 7.
    Yau, K.-W., Haynes, L. W., and Nakatani, K., 1988, Study of the phototransduction mechanism in rods and cones, in: Proceedings of the Retina Research Foundation Symposium (D. M. K. Lam, ed.) Portfolio Publishing, Woodlands, TX, 1: 41–58.Google Scholar
  8. 8.
    Nakatani, K., and Yau, K.-W, 1985, cGMP opens the light-sensitive conductance in retinal rods, Biophys. J. 47: 356a.Google Scholar
  9. 9.
    Haynes, L. W., and Yau, K.-W., 1985, Cyclic-GMP-sensitive conductance in outer segment membranes of catfish cones, Nature 317: 61–64.PubMedCrossRefGoogle Scholar
  10. 10.
    Yau, K.-W, and Haynes, L. W., 1986, Effect of divalent cations on the macroscopic cGMP-activated current in excised rod membrane patches, Biophys. J. 49: 33a.CrossRefGoogle Scholar
  11. 11.
    Haynes, L. W, Kay, A. R., and Yau, K.-W, 1986, Single cGMP-activated channel activity in excised patches of rod outer segment membranes, Nature 321: 66–70.PubMedCrossRefGoogle Scholar
  12. 12.
    Yau, K.-W, Haynes, L. W., and Nakatani, K., 1986, Roles of calcium and cyclic-GMP in visual transduction, in: Membrane Control of Cellular Activity (H. Ch. Luettgau, ed.), Gustav Fischer, Stuttgart, pp. 343–366.Google Scholar
  13. 13.
    Haynes, L. W., and Yau, K.-W., 1987, Single cGMP-activated channel activity recorded from excised cone membrane patches, Biophys. J. 51: 18a.Google Scholar
  14. 14.
    Fesenko, E. E., Kolesnikov, S. S., and Lyubarsky, A. L., 1985, Induction by cyclic-GMP of cationic conductance in plasma membrane of retinal rod outer segment, Nature 313: 310–313.PubMedCrossRefGoogle Scholar
  15. 15.
    Zimmerman, A. L., Yamanaka, G., Eckstein, F., Baylor, D. A., and Stryer, L., 1985, Interaction of hydrolysis-resistant analogs of cyclic-GMP with the phosphodiesterase and light-sensitive channel of retinal rod outer segments, Proc. Natl. Acad. Sci. U.S.A. 82: 8813–8817.PubMedCrossRefGoogle Scholar
  16. 16.
    Fesenko, E. E., Kolesnikov, S. S., and Lyubarsky, A. L., 1986, Direct action of cGMP on the conductance of retinal rods plasma membrane, Biochem. Biophys. Acta 856: 661–671.PubMedCrossRefGoogle Scholar
  17. 17.
    Matthews, G., 1986, Comparison of the light-sensitive and cyclic-GMP-sensitive conductance of the rod photoreceptor: Noise characteristics, J. Neurosci. 6: 2521–2526.PubMedGoogle Scholar
  18. 18.
    Stern, J. H., Kaupp, U. B., and MacLeish, P. R., 1986, Control of the light-regulated current in rod photoreceptors by cyclic-GMP and L-cis-Diltiazem, Proc. Natl. Acad. Sci., U.S.A. 83: 1163–1167.PubMedCrossRefGoogle Scholar
  19. 19.
    Zimmerman, A. L., and Baylor, D. A., 1986, Cyclic-GMP-sensitive conductance of retinal rods consists of aqueous pores, Nature 321: 70–72.PubMedCrossRefGoogle Scholar
  20. 20.
    Stern, J. H., Knutsson, H., and MacLeish, P. R., 1987, Divalent cations directly affect the conductance of excised patches of rod photoreceptor membrane, Science 236: 1674–1678.PubMedCrossRefGoogle Scholar
  21. 21.
    Matthews, G., 1987, Single-channel recordings demonstrate that cGMP opens the light-sensitive ion channel of the rod photoreceptor, Proc. Natl. Acad. Sci. U.S.A. 84: 299–302.PubMedCrossRefGoogle Scholar
  22. 22.
    Matthews, G., and 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: 691–716.PubMedGoogle Scholar
  23. 23.
    Karpen, J. W., Zimmerman, A. L. Stryer, L., and Baylor, D. A., 1988, Gating kinetics of the cyclic-GMP-activated channel of retinal rods: Flash photolysis and voltage-jump studies, Proc. Natl. Acad. Sci., U.S.A. 85: 1287–1291.PubMedCrossRefGoogle Scholar
  24. 24.
    Bader, C. R., MacLeish, P. R., and Schwartz, E. A., 1979, A voltage-clamp study of the light response in solitary rods of the tiger salamander, J. Physiol. 296: 1–26.PubMedGoogle Scholar
  25. 25.
    Bodoia, R. D., and Detwiler, P. B., 1985, Patch-clamp recordings of the light-sensitive dark noise in retinal rods from lizard and frog, J. Physiol. 367: 183–216.PubMedGoogle Scholar
  26. 26.
    Baylor, D. A., and 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
  27. 27.
    Attwell, D., Werblin, F. S., and Wilson, M., 1982, The properties of single cones isolated from the tiger salamander retina, J. Physiol. 328: 259–283.PubMedGoogle Scholar
  28. 28.
    Yau, K.-W., and Nakatani, K., 1984, Cation selectivity of light-sensitive conductance in retinal rods, Nature 309: 352–354.PubMedCrossRefGoogle Scholar
  29. 29.
    Hodgkin, A. L., McNaughton, P. A., and Nunn, B. J., 1985, The ionic selectivity and calcium dependence of the light-sensitive pathway in toad rods, J. Physiol. 358: 447–468.PubMedGoogle Scholar
  30. 30.
    Jack, J. J. B., Noble, D., and Tsien, R. W., 1975, Electric Current Flow in Excitable Cells, Clarenden, Oxford.Google Scholar
  31. 31.
    Yau, K.-W., and Nakatani, K., 1984, Electrogenic Na-Ca exchange in retinal rod outer segment, Nature 311: 661–663.PubMedCrossRefGoogle Scholar
  32. 32.
    Almers, W., and McCleskey, E. W., 1984, Nonselective conductance in calcium channels of frog muscle: Calcium selectivity in a single-file pore, J. Physiol 353: 585–608.PubMedGoogle Scholar
  33. 33.
    Hess, P., and Tsien, R. W., 1984, Mechanism of ion permeation through calcium channels, Nature 309: 453–456.PubMedCrossRefGoogle Scholar
  34. 34.
    Zimmerman, A. L., and Baylor, D. A., 1988, Ionic permeation in the cGMP-activated channel of retinal rods, Biophys. J. 53: 472a.Google Scholar
  35. 35.
    Detwiler, P. B., Conner, P. B., and Bodoia, R. D., 1982, Gigaseal patch-clamp recording from outer segments of intact retinal rods, Nature 300: 59–61.PubMedCrossRefGoogle Scholar
  36. 36.
    Gray, P., and Attwell, D., 1985, Kinetics of light-sensitive channels in vertebrate photoreceptors, Proc. Roy. Soc. Lond. B. 223: 379–388.CrossRefGoogle Scholar
  37. 37.
    Zimmerman, A. L., and Baylor, D. A., 1985, Electrical properties of the light-sensitive conductance of salamander retinal rods, Biophys. J. 47: 357a.CrossRefGoogle Scholar
  38. 38.
    Lansman, J. B., Hess, P., and Tsien, R. W., 1985, Direct measurement of entry and exit rates for calcium ions in single calcium channels, Biophys. J. 47: 67a.Google Scholar

Copyright information

© Plenum Press, New York 1990

Authors and Affiliations

  • Lawrence W. Haynes
    • 1
  • King-Wai Yau
    • 1
  1. 1.Howard Hughes Medical Institute, and Department of NeuroscienceThe Johns Hopkins University School of MedicineBaltimoreUSA

Personalised recommendations