Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1985 Jan;358:447–468. doi: 10.1113/jphysiol.1985.sp015561

The ionic selectivity and calcium dependence of the light-sensitive pathway in toad rods.

A L Hodgkin, P A McNaughton, B J Nunn
PMCID: PMC1193352  PMID: 2580087

Abstract

A new method is described for determining the effects of rapid changes in ionic concentration on the light-sensitive currents of rod outer segments. Replacing Na with another monovalent cation caused a rapid change in current followed by an exponential decline of time constant 0.5-2 s. From the magnitude of the initial rapid change in current we conclude that Li, Na, and K and Rb ions pass readily through the light-sensitive channel in the presence of 1 mM-Ca, whereas Cs crosses with difficulty and choline, tetramethylammonium and tetraethylammonium not at all. The effect of reducing Ca in the external medium indicates that the residual inward current recorded for a few seconds when Na is replaced by an impermeant ion is carried largely by Ca ions. With 1 microM-Ca in the external medium the relative ability of monovalent cations to carry light-sensitive current is Li:Na:K:Rb:Cs = 1.4:1:0.8:0.6:0.15. The same order applied in the physiological region but the values are less certain. Large transient inward currents are seen if external Ca is raised form 1 microM to 5 mM or more; these currents which are maximal in an isotonic Ca solution are presumably carried by Ca. The effect of monovalent cations on the number of open light-sensitive channels was tested by adding the cation to a solution containing 55 mM-Na. Na ions open light-sensitive channels with a delay, probably by promoting Na-Ca exchange; K and Rb close channels by inhibiting exchange; Li and Cs seem inert in the exchange mechanism. The rate at which inward current declines in low [Na]o or high [Ca]o is accelerated by weak background lights and slowed by 3-isobutyl-1-methylxanthine (IBMX), which inhibits the hydrolysis of cGMP. On returning to Ringer solution after a period in low [Na]o the current recovers with a delay of about 1 s which decreases as the Ca concentration of the low [Na]o medium is reduced. We conclude that intracellular Ca has a strong effect on the number of open light-sensitive channels. None the less, several observations are inconsistent with channel closure being dependent simply on combination with internal Ca.

Full text

PDF
447

Selected References

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

  1. 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]
  2. Bastian B. L., Fain G. L. The effects of sodium replacement on the responses of toad rods. J Physiol. 1982 Sep;330:331–347. doi: 10.1113/jphysiol.1982.sp014344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Baylor D. A., Matthews G., Nunn B. J. Location and function of voltage-sensitive conductances in retinal rods of the salamander, Ambystoma tigrinum. J Physiol. 1984 Sep;354:203–223. doi: 10.1113/jphysiol.1984.sp015372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blaustein M. P., Hodgkin A. L. The effect of cyanide on the efflux of calcium from squid axons. J Physiol. 1969 Feb;200(2):497–527. doi: 10.1113/jphysiol.1969.sp008704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Capovilla M., Caretta A., Cervetto L., Torre V. Ionic movements through light-sensitive channels of toad rods. J Physiol. 1983 Oct;343:295–310. doi: 10.1113/jphysiol.1983.sp014893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Goldberg N. D., Ames A. A., 3rd, Gander J. E., Walseth T. F. Magnitude of increase in retinal cGMP metabolic flux determined by 18O incorporation into nucleotide alpha-phosphoryls corresponds with intensity of photic stimulation. J Biol Chem. 1983 Aug 10;258(15):9213–9219. [PubMed] [Google Scholar]
  8. Hodgkin A. L., McNaughton P. A., Nunn B. J., Yau K. W. Effect of ions on retinal rods from Bufo marinus. J Physiol. 1984 May;350:649–680. doi: 10.1113/jphysiol.1984.sp015223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hubbell W. L., Bownds M. D. Visual transduction in vertebrate photoreceptors. Annu Rev Neurosci. 1979;2:17–34. doi: 10.1146/annurev.ne.02.030179.000313. [DOI] [PubMed] [Google Scholar]
  10. Lamb T. D., McNaughton P. A., Yau K. W. Spatial spread of activation and background desensitization in toad rod outer segments. J Physiol. 1981;319:463–496. doi: 10.1113/jphysiol.1981.sp013921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lewis R. S., Hudspeth A. J. Voltage- and ion-dependent conductances in solitary vertebrate hair cells. Nature. 1983 Aug 11;304(5926):538–541. doi: 10.1038/304538a0. [DOI] [PubMed] [Google Scholar]
  12. Lolley R. N., Racz E. Calcium modulation of cyclic GMP synthesis in rat visual cells. Vision Res. 1982;22(12):1481–1486. doi: 10.1016/0042-6989(82)90213-9. [DOI] [PubMed] [Google Scholar]
  13. Miki N., Baraban J. M., Keirns J. J., Boyce J. J., Bitensky M. W. Purification and properties of the light-activated cyclic nucleotide phosphodiesterase of rod outer segments. J Biol Chem. 1975 Aug 25;250(16):6320–6327. [PubMed] [Google Scholar]
  14. Torre V. The contribution of the electrogenic sodium-potassium pump to the electrical activity of toad rods. J Physiol. 1982 Dec;333:315–341. doi: 10.1113/jphysiol.1982.sp014456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Woodruff M. L., Fain G. L., Bastian B. L. Light-dependent ion influx into toad photoreceptors. J Gen Physiol. 1982 Oct;80(4):517–536. doi: 10.1085/jgp.80.4.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Yau K. W., Nakatani K. Cation selectivity of light-sensitive conductance in retinal rods. Nature. 1984 May 24;309(5966):352–354. doi: 10.1038/309352a0. [DOI] [PubMed] [Google Scholar]
  18. Yellen G. Single Ca2+-activated nonselective cation channels in neuroblastoma. Nature. 1982 Mar 25;296(5855):357–359. doi: 10.1038/296357a0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES