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. 1982;333:315–341. doi: 10.1113/jphysiol.1982.sp014456

The contribution of the electrogenic sodium—potassium pump to the electrical activity of toad rods

Vincent Torre 1
PMCID: PMC1197251  PMID: 7182468

Abstract

1. The membrane potential of rods in the isolated toad retina was recorded while changing the ionic composition of the extracellular medium.

2. Caesium (Cs+) at a concentration of 1 mM was sufficient to completely block the sag from the peak to the plateau in the bright-flash voltage response.

3. In the presence of 10 mM-Cs+ the bright-flash response increased in amplitude to about 90 mV, thus reaching an absolute membrane potential of between -110 and -135 mV. These responses consisted of an initial fast component of about 35 mV followed by a much slower component which could be as large as 50 mV.

4. At the peak of the initial fast component the rod membrane conformed closely to the behaviour of a K+ electrode with a PNa/PK ratio of 0·023. On average the amplitude of the slow component was about 35 mV in the presence of 2·6 mM-K+ and was reduced to about 25 mV in a K+-free Ringer.

5. Addition of 100 μM-strophanthidin to the perfusate induced several reversible changes in the electrical activity of rods. The dark resting membrane potential depolarized by about 5 mV and the kinetics of the voltage response to dim flashes of light slowed down. The voltage sensitivity initially increased by about 30%, but the peak of the response to a bright flash of light was reduced by about 13 mV.

6. In rods treated with 10 mM-Cs+ the slow component present in the bright flash response was abolished by strophanthidin with an apparent Km of 3 μM.

7. The amplitude of the slow component decreased with a time lag of about 2 min when external Na+ was reduced. A previous exposure of the retina to a Na+-free Ringer solution for at least 3 min modified the voltage photoresponse in a way similar to that observed in the presence of 100 μM-strophanthidin.

8. When external Ca2+ concentration ([Ca2+]o) was increased from 2 to 5 mM the slow component decreased by about 30%. When [Ca2+]o was reduced the slow component increased. A twofold increase was observed when [Ca2+]o was lower than 10-4 M.

9. It is suggested that the slow component of the voltage response in the presence of external Cs+ is caused by an electrogenic current driven by the Na+—K+ transport system, during a voltage-dependent block of external Cs+ of some K+ channels.

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Selected References

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

  1. Attwell D., Wilson M. Behaviour of the rod network in the tiger salamander retina mediated by membrane properties of individual rods. J Physiol. 1980 Dec;309:287–315. doi: 10.1113/jphysiol.1980.sp013509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bader C. R., Macleish P. R., Schwartz E. A. A voltage-clamp study of the light response in solitary rods of the tiger salamander. J Physiol. 1979 Nov;296:1–26. doi: 10.1113/jphysiol.1979.sp012988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baylor D. A., Hodgkin A. L. Detection and resolution of visual stimuli by turtle photoreceptors. J Physiol. 1973 Oct;234(1):163–198. doi: 10.1113/jphysiol.1973.sp010340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baylor D. A., Lamb T. D., Yau K. W. The membrane current of single rod outer segments. J Physiol. 1979 Mar;288:589–611. [PMC free article] [PubMed] [Google Scholar]
  5. Benz R., Conti F. Reversible electrical breakdown of squid giant axon membrane. Biochim Biophys Acta. 1981 Jul 6;645(1):115–123. doi: 10.1016/0005-2736(81)90518-6. [DOI] [PubMed] [Google Scholar]
  6. Bezanilla F., Armstrong C. M. Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axons. J Gen Physiol. 1972 Nov;60(5):588–608. doi: 10.1085/jgp.60.5.588. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown J. E., Pinto L. H. Ionic mechanism for the photoreceptor potential of the retina of Bufo marinus. J Physiol. 1974 Feb;236(3):575–591. doi: 10.1113/jphysiol.1974.sp010453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Capovilla M., Cervetto L., Pasino E., Torre V. The sodium current underlying the responses of toad rods to light. J Physiol. 1981 Aug;317:223–242. doi: 10.1113/jphysiol.1981.sp013822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Capovilla M., Cervetto L., Torre V. Effects of changing external potassium and chloride concentrations on the photoresponses of Bufo bufo rods. J Physiol. 1980 Oct;307:529–551. doi: 10.1113/jphysiol.1980.sp013452. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cervetto L., Pasino E., Torre V. Electrical responses of rods in the retina of Bufo marinus. J Physiol. 1977 May;267(1):17–51. doi: 10.1113/jphysiol.1977.sp011799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ciani S., Krasne S., Hagiwara S. A model for the effects of potential and external K+ concentration on the Cs+ blocking of inward rectification. Biophys J. 1980 Apr;30(1):199–204. doi: 10.1016/S0006-3495(80)85089-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Copenhagen D. R., Owen W. G. Current-voltage relations in the rod photoreceptor network of the turtle retina. J Physiol. 1980 Nov;308:159–184. doi: 10.1113/jphysiol.1980.sp013466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Detwiler P. B., Hodgkin A. L., McNaughton P. A. Temporal and spatial characteristics of the voltage response of rods in the retina of the snapping turtle. J Physiol. 1980 Mar;300:213–250. doi: 10.1113/jphysiol.1980.sp013159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eisner D. A., Lederer W. J. Characterization of the electrogenic sodium pump in cardiac Purkinje fibres. J Physiol. 1980 Jun;303:441–474. doi: 10.1113/jphysiol.1980.sp013298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fain G. L., Quandt F. N., Bastian B. L., Gerschenfeld H. M. Contribution of a caesium-sensitive conductance increase to the rod photoresponse. Nature. 1978 Mar 30;272(5652):466–469. doi: 10.1038/272467a0. [DOI] [PubMed] [Google Scholar]
  16. Garay R. P., Garrahan P. J. The interaction of sodium and potassium with the sodium pump in red cells. J Physiol. 1973 Jun;231(2):297–325. doi: 10.1113/jphysiol.1973.sp010234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Garrahan P. J., Glynn I. M. The sensitivity of the sodium pump to external sodium. J Physiol. 1967 Sep;192(1):175–188. doi: 10.1113/jphysiol.1967.sp008295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Glynn I. M., Karlish S. J. The sodium pump. Annu Rev Physiol. 1975;37:13–55. doi: 10.1146/annurev.ph.37.030175.000305. [DOI] [PubMed] [Google Scholar]
  19. HODGKIN A. L., HOROWICZ P. The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol. 1959 Oct;148:127–160. doi: 10.1113/jphysiol.1959.sp006278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hagins W. A., Yoshikami S. Ionic mechanisms in excitation of photoreceptors. Ann N Y Acad Sci. 1975 Dec 30;264:314–325. doi: 10.1111/j.1749-6632.1975.tb31492.x. [DOI] [PubMed] [Google Scholar]
  21. Hagiwara S., Miyazaki S., Rosenthal N. P. Potassium current and the effect of cesium on this current during anomalous rectification of the egg cell membrane of a starfish. J Gen Physiol. 1976 Jun;67(6):621–638. doi: 10.1085/jgp.67.6.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hille B. Potassium channels in myelinated nerve. Selective permeability to small cations. J Gen Physiol. 1973 Jun;61(6):669–686. doi: 10.1085/jgp.61.6.669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Korenbrot J. I., Cone R. A. Dark ionic flux and the effects of light in isolated rod outer segments. J Gen Physiol. 1972 Jul;60(1):20–45. doi: 10.1085/jgp.60.1.20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. MULLINS L. J., NODA K. THE INFLUENCE OF SODIUM-FREE SOLUTIONS ON THE MEMBRANE POTENTIAL OF FROG MUSCLE FIBERS. J Gen Physiol. 1963 Sep;47:117–132. doi: 10.1085/jgp.47.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Oakley B., 2nd, Flaming D. G., Brown K. T. Effects of the rod receptor potential upon retinal extracellular potassium concentration. J Gen Physiol. 1979 Dec;74(6):713–737. doi: 10.1085/jgp.74.6.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Repke K., Est M., Portius H. J. Uber die Ursache der Speciesunterschiede in der Digitalisempfindlichkeit. Biochem Pharmacol. 1965 Dec;14(12):1785–1802. doi: 10.1016/0006-2952(65)90269-8. [DOI] [PubMed] [Google Scholar]
  27. Robinson J. D., Flashner M. S. The (Na+ + K+)-activated ATPase. Enzymatic and transport properties. Biochim Biophys Acta. 1979 Aug 17;549(2):145–176. doi: 10.1016/0304-4173(79)90013-2. [DOI] [PubMed] [Google Scholar]
  28. Robinson J. W. The difference in sensitivity to cardiac steroids of (Na++K+)-stimulated ATPase and amino acid transport in the intestinal mucosa of the rat and other species. J Physiol. 1970 Jan;206(1):41–60. doi: 10.1113/jphysiol.1970.sp008996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sachs J. R. Interaction of external K, Na, and cardioactive steroids with the Na-K pump of the human red blood cell. J Gen Physiol. 1974 Feb;63(2):123–143. doi: 10.1085/jgp.63.2.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Thomas R. C. Electrogenic sodium pump in nerve and muscle cells. Physiol Rev. 1972 Jul;52(3):563–594. doi: 10.1152/physrev.1972.52.3.563. [DOI] [PubMed] [Google Scholar]
  32. Yau K. W., McNaughton P. A., Hodgkin A. L. Effect of ions on the light-sensitive current in retinal rods. Nature. 1981 Aug 6;292(5823):502–505. doi: 10.1038/292502a0. [DOI] [PubMed] [Google Scholar]
  33. Zuckerman R. Ionic analysis of photoreceptor membrane currents. J Physiol. 1973 Dec;235(2):333–354. doi: 10.1113/jphysiol.1973.sp010390. [DOI] [PMC free article] [PubMed] [Google Scholar]

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