Skip to main content
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1972 Jul 1;60(1):20–45. doi: 10.1085/jgp.60.1.20

Dark Ionic Flux and the Effects of Light in Isolated Rod Outer Segments

Juan I Korenbrot 1, Richard A Cone 1
PMCID: PMC2226056  PMID: 4537779

Abstract

We have determined the permeability properties of freshly isolated frog rod outer segments by observing their osmotic behavior in a simple continuous flow apparatus. Outer segments obtained by gently shaking a retina are sensitive but nonideal osmometers; a small restoring force prevents them from shrinking or swelling quite as much as expected for ideal behavior. We find that Na+, Cl-, No3 -, glycerol, acetate, and ammonium rapidly enter the outer segment, but K+, SO4 =, and melezitose appear impermeable. The Na flux is rectified; for concentration gradients in the physiological range, 2 x 109 Na+ ions/sec enter the outer segment, but we detect no efflux of Na+, under our conditions, when the gradient is reversed. Illumination of the outer segment produces a specific increase in the resistance to Na+ influx, but has no effect on the flux of other solutes. This light-dependent Na+ resistance increases linearly with the number of rhodopsin molecules bleached. We find that excitation of a single rhodopsin molecule produces a transient (∼1 sec) "photoresistance" which reduces the Na+ influx by about 1%, thus preventing the entry of about 107 Na+ ions. At considerably higher light levels, a stable afterimage resistance appears which reduces the Na influx by one-half when 106 rhodopsin molecules are bleached per rod. We have incorporated these findings into a model for the electrophysiological characteristics of the receptor.

Full Text

The Full Text of this article is available as a PDF (1.3 MB).

Selected References

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

  1. Arden G. B., Ernst W. The effect of ions on the photoresponses of pigeon cones. J Physiol. 1970 Dec;211(2):311–339. doi: 10.1113/jphysiol.1970.sp009281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BARLOW H. B., SPARROCK J. M. THE ROLE OF AFTERIMAGES IN DARK ADAPTATION. Science. 1964 Jun 12;144(3624):1309–1314. doi: 10.1126/science.144.3624.1309. [DOI] [PubMed] [Google Scholar]
  3. BRINDLEY G. S. The discrimination of after-images. J Physiol. 1959 Jun 23;147(1):194–203. doi: 10.1113/jphysiol.1959.sp006234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baylor D. A., O'Bryan P. M. Electrical signaling in vertebrate photoreceptors. Fed Proc. 1971 Jan-Feb;30(1):79–83. [PubMed] [Google Scholar]
  5. Blaurock A. E., Wilkins M. H. Structure of frog photoreceptor membranes. Nature. 1969 Aug 30;223(5209):906–909. doi: 10.1038/223906a0. [DOI] [PubMed] [Google Scholar]
  6. Bonting S. L., Bangham A. D. On the biochemical mechanism of the visual process. Exp Eye Res. 1967 Oct;6(4):400–413. doi: 10.1016/s0014-4835(67)80015-0. [DOI] [PubMed] [Google Scholar]
  7. Bortoff A. Localization of slow potential responses in the Necturus retina. Vision Res. 1964 Dec;4(11):627–635. doi: 10.1016/0042-6989(64)90048-3. [DOI] [PubMed] [Google Scholar]
  8. Bowmaker J. K. Sodium movements from frog rod outer segments. Vision Res. 1970 Jul;10(7):601–604. doi: 10.1016/0042-6989(70)90054-4. [DOI] [PubMed] [Google Scholar]
  9. Bownds D., Gaide-Huguenin A. C. Rhodopsin content of frog photoreceptor outer segments. Nature. 1970 Feb 28;225(5235):870–872. doi: 10.1038/225870a0. [DOI] [PubMed] [Google Scholar]
  10. Bridges C. D. Molar absorbance coefficient of rhodopsin. Nature. 1970 Sep 19;227(5264):1258–1259. doi: 10.1038/2271258a0. [DOI] [PubMed] [Google Scholar]
  11. Brierley G. P., Fleischmen D., Hughes S. D., Hunter G. R., McConnell D. G. On the permeability of isolated bovine retinal outer segment fragments. Biochim Biophys Acta. 1968 Aug;163(1):117–120. doi: 10.1016/0005-2736(68)90041-2. [DOI] [PubMed] [Google Scholar]
  12. CURTIS A. S. Cell contact and adhesion. Biol Rev Camb Philos Soc. 1962 Feb;37:82–129. doi: 10.1111/j.1469-185x.1962.tb01605.x. [DOI] [PubMed] [Google Scholar]
  13. Clark A. W., Branton D. Fracture faces in frozen outer segments from the guinea pig retina. Z Zellforsch Mikrosk Anat. 1968;91(4):586–603. doi: 10.1007/BF00455276. [DOI] [PubMed] [Google Scholar]
  14. Frank R. N., Goldsmith T. H. Effects of cardiac glycosides on electrical activity in the isolated retina of the frog. J Gen Physiol. 1967 Jul;50(6):1585–1606. doi: 10.1085/jgp.50.6.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. HUBBARD R., BROWN P. K., KROPF A. Vertebrate lumi- and meta-rhodopsins. Nature. 1959 Feb 14;183(4659):442–446. [PubMed] [Google Scholar]
  16. HUBBARD R. The molecular weight of rhodopsin and the nature of the rhodopsin-digitonin complex. J Gen Physiol. 1954 Jan 20;37(3):381–399. doi: 10.1085/jgp.37.3.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hagins W. A., Penn R. D., Yoshikami S. Dark current and photocurrent in retinal rods. Biophys J. 1970 May;10(5):380–412. doi: 10.1016/S0006-3495(70)86308-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Heller J., Ostwald T. J., Bok D. The osmotic behavior of rod photoreceptor outer segment discs. J Cell Biol. 1971 Mar;48(3):633–649. doi: 10.1083/jcb.48.3.633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Liebman P. A., Entine G. Visual pigments of frog and tadpole (Rana pipiens). Vision Res. 1968 Jul;8(7):761–775. doi: 10.1016/0042-6989(68)90128-4. [DOI] [PubMed] [Google Scholar]
  20. MATTHEWS R. G., HUBBARD R., BROWN P. K., WALD G. TAUTOMERIC FORMS OF METARHODOPSIN. J Gen Physiol. 1963 Nov;47:215–240. doi: 10.1085/jgp.47.2.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Murakami M., Pak W. L. Intracellularly recorded early receptor potential of the vertebrate photoreceptors. Vision Res. 1970 Oct;10(10):965–975. doi: 10.1016/0042-6989(70)90074-x. [DOI] [PubMed] [Google Scholar]
  22. Penn R. D., Hagins W. A. Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature. 1969 Jul 12;223(5202):201–204. doi: 10.1038/223201a0. [DOI] [PubMed] [Google Scholar]
  23. RUSHTON W. A. Rhodopsin measurement and dark-adaptation in a subject deficient in cone vision. J Physiol. 1961 Apr;156:193–205. doi: 10.1113/jphysiol.1961.sp006668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Robertson J. D. Granulo-fibrillar and globular substructure in unit membranes. Ann N Y Acad Sci. 1966 Jul 14;137(2):421–440. doi: 10.1111/j.1749-6632.1966.tb50174.x. [DOI] [PubMed] [Google Scholar]
  25. SIDMAN R. L. The structure and concentration of solids in photoreceptor cells studied by refractometry and interference microscopy. J Biophys Biochem Cytol. 1957 Jan 25;3(1):15–30. doi: 10.1083/jcb.3.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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. 1969 Dec;9(12):1443–1451. doi: 10.1016/0042-6989(69)90060-1. [DOI] [PubMed] [Google Scholar]
  27. Tomita T. Electrical activity of vertebrate photoreceptors. Q Rev Biophys. 1970 May;3(2):179–222. doi: 10.1017/s0033583500004571. [DOI] [PubMed] [Google Scholar]
  28. Toyoda J., Hashimoto H., Anno H., Tomita T. The rod response in the frog and studies by intracellular recording. Vision Res. 1970 Nov;10(11):1093–1100. doi: 10.1016/0042-6989(70)90026-x. [DOI] [PubMed] [Google Scholar]
  29. Toyoda J., Nosaki H., Tomita T. Light-induced resistance changes in single photoreceptors of Necturus and Gekko. Vision Res. 1969 Apr;9(4):453–463. doi: 10.1016/0042-6989(69)90134-5. [DOI] [PubMed] [Google Scholar]
  30. Weale R. A. On the birefringence of rods and cones. Pflugers Arch. 1971;329(3):244–257. doi: 10.1007/BF00586618. [DOI] [PubMed] [Google Scholar]

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

RESOURCES