Skip to main content
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1994 Jun 1;103(6):939–956. doi: 10.1085/jgp.103.6.939

The light-sensitive conductance of hyperpolarizing invertebrate photoreceptors: a patch-clamp study

PMCID: PMC2216883  PMID: 7931139

Abstract

Tight-seal recording was employed to investigate membrane currents in hyperpolarizing ciliary photoreceptors enzymatically isolated from the eyes of the file clam (Lima scabra) and the bay scallop (Pecten irradians). These two organisms are unusual in that their double retinas also possess a layer of depolarizing rhabdomeric cells. Ciliary photoreceptors from Lima have a rounded soma, 15-20 microns diam, and display a prominent bundle of fine processes up to 30 microns long. The cell body of scallop cells is similar in size, but the ciliary appendages are modified, forming small spherical structures that protrude from the cell. In both species light stimulation at a voltage near the resting potential gives rise to a graded outward current several hundred pA in amplitude, accompanied by an increase in membrane conductance. The reversal potential of the photocurrent is approximately -80 mV, and shifts in the positive direction by approximately 39 mV when the concentration of extracellular K is increased from 10 to 50 mM, consistent with the notion that light activates K-selective channels. The light-activated conductance increases with depolarization in the physiological range of membrane voltages (-30 to -70 mV). Such outward rectification is greatly reduced after removal of divalent cations from the superfusate. In Pecten, cell- attached recordings were also obtained; in some patches outwardly directed single-channel currents could be activated by light but not by voltage. The unitary conductance of these channels was approximately 26 pS. Solitary ciliary cells also gave evidence of the post stimulus rebound, which is presumably responsible for initiating the "off" discharge of action potentials at the termination of a light stimulus: in patches containing only voltage-dependent channels, light stimulation suppressed depolarization-induced activity, and was followed by a strong burst of openings, directly related to the intensity of the preceding photostimulation.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bacigalupo J., Chinn K., Lisman J. E. Ion channels activated by light in Limulus ventral photoreceptors. J Gen Physiol. 1986 Jan;87(1):73–89. doi: 10.1085/jgp.87.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bacigalupo J., Lisman J. E. Single-channel currents activated by light in Limulus ventral photoreceptors. Nature. 1983 Jul 21;304(5923):268–270. doi: 10.1038/304268a0. [DOI] [PubMed] [Google Scholar]
  3. Barber V. C., Evans E. M., Land M. F. The fine structure of the eye of the mollusc Pecten maximus. Z Zellforsch Mikrosk Anat. 1967;76(3):25–312. [PubMed] [Google Scholar]
  4. Barber V. C., Land M. F. Eye of the cockle, Cardium edule: anatomical and physiological investigations. Experientia. 1967 Aug 15;23(8):677–678. doi: 10.1007/BF02144199. [DOI] [PubMed] [Google Scholar]
  5. Brown J. E., Blinks J. R. Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin. J Gen Physiol. 1974 Dec;64(6):643–665. doi: 10.1085/jgp.64.6.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cornwall M. C., Gorman A. L. Contribution of calcium and potassium permeability changes to the off response of scallop hyperpolarizing photoreceptors. J Physiol. 1979 Jun;291:207–232. doi: 10.1113/jphysiol.1979.sp012808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cornwall M. C., Gorman A. L. Ionic and spectral mechanisms of the off response to light in hyperpolarizing photoreceptors of the clam, Lima scabra. Cell Mol Neurobiol. 1983 Dec;3(4):311–328. doi: 10.1007/BF00734713. [DOI] [PubMed] [Google Scholar]
  8. Eakin R. M. Evolution of photoreceptors. Cold Spring Harb Symp Quant Biol. 1965;30:363–370. doi: 10.1101/sqb.1965.030.01.036. [DOI] [PubMed] [Google Scholar]
  9. Fein A., Charlton J. S. Local membrane current in Limulus photoreceptors. Nature. 1975 Nov 20;258(5532):250–252. doi: 10.1038/258250a0. [DOI] [PubMed] [Google Scholar]
  10. Gorman A. L., McReynolds J. S. Hyperpolarizing and depolarizing receptor potentials in the scallop eye. Science. 1969 Jul 18;165(3890):309–310. doi: 10.1126/science.165.3890.309. [DOI] [PubMed] [Google Scholar]
  11. Gorman A. L., McReynolds J. S. Ionic effects on the membrane potential of hyperpolarizing photoreceptors in scallop retina. J Physiol. 1978 Feb;275:345–355. doi: 10.1113/jphysiol.1978.sp012193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gotow T., Nishi T. Roles of cyclic GMP and inositol trisphosphate in phototransduction of the molluscan extraocular photoreceptor. Brain Res. 1991 Aug 23;557(1-2):121–128. doi: 10.1016/0006-8993(91)90124-e. [DOI] [PubMed] [Google Scholar]
  13. Gotow T. Photoresponses of an extraocular photoreceptor associated with a decrease in membrane conductance in an opisthobranch mollusc. Brain Res. 1989 Feb 6;479(1):120–129. [PubMed] [Google Scholar]
  14. KENNEDY D. Neural photoreception in a lamellibranch mollusc. J Gen Physiol. 1960 Nov;44:277–299. doi: 10.1085/jgp.44.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. MILLER W. H. Derivatives of cilia in the distal sense cells of the retina of Pecten. J Biophys Biochem Cytol. 1958 Mar 25;4(2):227–228. doi: 10.1083/jcb.4.2.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Matthews G., Watanabe S. Properties of ion channels closed by light and opened by guanosine 3',5'-cyclic monophosphate in toad retinal rods. J Physiol. 1987 Aug;389:691–715. doi: 10.1113/jphysiol.1987.sp016678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. McReynolds J. S., Gorman A. L. Membrane conductances and spectral sensitivities of Pecten photoreceptors. J Gen Physiol. 1970 Sep;56(3):392–406. doi: 10.1085/jgp.56.3.392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McReynolds J. S., Gorman A. L. Photoreceptor potentials of opposite polarity in the eye of the scallop, Pecten irradians. J Gen Physiol. 1970 Sep;56(3):376–391. doi: 10.1085/jgp.56.3.376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mpitosos G. J. Physiology of vision in the mollusk Lima scabra. J Neurophysiol. 1973 Mar;36(2):371–383. doi: 10.1152/jn.1973.36.2.371. [DOI] [PubMed] [Google Scholar]
  20. Nasi E. Electrophysiological properties of isolated photoreceptors from the eye of Lima scabra. J Gen Physiol. 1991 Jan;97(1):17–34. doi: 10.1085/jgp.97.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nasi E., Gomez M. P. Light-activated ion channels in solitary photoreceptors of the scallop Pecten irradians. J Gen Physiol. 1992 May;99(5):747–769. doi: 10.1085/jgp.99.5.747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nasi E. Whole-cell clamp of dissociated photoreceptors from the eye of Lima scabra. J Gen Physiol. 1991 Jan;97(1):35–54. doi: 10.1085/jgp.97.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nishi T., Gotow T. A light-induced decrease of cyclic GMP is involved in the photoresponse of molluscan extraocular photoreceptors. Brain Res. 1989 Apr 17;485(1):185–188. doi: 10.1016/0006-8993(89)90682-3. [DOI] [PubMed] [Google Scholar]
  24. Stern J., Chinn K., Bacigalupo J., Lisman J. Distinct lobes of Limulus ventral photoreceptors. I. Functional and anatomical properties of lobes revealed by removal of glial cells. J Gen Physiol. 1982 Dec;80(6):825–837. doi: 10.1085/jgp.80.6.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wiederhold M. L., MacNichol E. F., Jr, Bell A. L. Photoreceptor spike responses in the hardshell clam, Mercenaria mercenaria. J Gen Physiol. 1973 Jan;61(1):24–55. doi: 10.1085/jgp.61.1.24. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yau K. W., Baylor D. A. Cyclic GMP-activated conductance of retinal photoreceptor cells. Annu Rev Neurosci. 1989;12:289–327. doi: 10.1146/annurev.ne.12.030189.001445. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES