Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1988 Sep;403:439–471. doi: 10.1113/jphysiol.1988.sp017258

Control of light-sensitive current in salamander rods.

A L Hodgkin 1, B J Nunn 1
PMCID: PMC1190722  PMID: 2473195

Abstract

1. The exponential decline of light-sensitive current seen after switch from Na+ to Li+ in the presence of Ca2+ probably depends on the activity of the phosphodiesterase (PDE) which hydrolyses cyclic GMP. 2. This probability is supported by experiments with suction electrodes which show that in toad and salamander rods the rate constant, b, of the exponential decline of current was increased at least 10-fold by moderate light intensities and decreased about 10-fold by 3-isobutyl-1-methylxanthine (IBMX), an inhibitor of PDE. 3. The rate constant b is about 3 times more sensitive to weak lights or to IBMX than the membrane current. This may be explained by a feed-back involving calcium ions which tends to hold current constant, perhaps by calcium inhibition of guanylate cyclase. 4. The time course of b, which probably represents the changes in PDE activity, was measured by switching from Na+ to Li+ at various times after a flash. The results suggest that a moderate flash (140 Rh) increased b about 7 times in 0.5 s and that b then declined with a time constant of 1.5-2 s. 5. Extrapolated values of the parameter b suggest that strong flashes (5000-10,000 Rh) increased b from 1 s-1 in the dark to perhaps 60 s-1 and that b continued to increase with flash strength for several log units after the current had reached saturation. 6. The observations in 4 and 5 fit well with the idea that b is related to PDE activity and that changes in the latter are sufficient to account for the rising phase of the flash response. 7. After a flash the light-sensitive current recovers much more rapidly than the time constant b-1, a discrepancy which is explained if a light flash causes a delayed increase in guanylate cyclase activity. 8. The apparent delayed increase in cyclase activation is consistent with an inhibitory effect of [Ca2+]i which is reduced when calcium is pumped out during the plateau of the response. 9. Experiments in which pulses of IBMX were applied at different times during a flash response support the idea that a flash causes a delayed increase in the rate of supply of cyclic GMP. Quantitative analysis of these and other tests with IBMX gave rate constants similar to those obtained by the Na+----Li+ method.

Full text

PDF
439

Selected References

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

  1. Baylor D. A., Hodgkin A. L., Lamb T. D. The electrical response of turtle cones to flashes and steps of light. J Physiol. 1974 Nov;242(3):685–727. doi: 10.1113/jphysiol.1974.sp010731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cervetto L., McNaughton P. A. The effects of phosphodiesterase inhibitors and lanthanum ions on the light-sensitive current of toad retinal rods. J Physiol. 1986 Jan;370:91–109. doi: 10.1113/jphysiol.1986.sp015924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cote R. H., Biernbaum M. S., Nicol G. D., Bownds M. D. Light-induced decreases in cGMP concentration precede changes in membrane permeability in frog rod photoreceptors. J Biol Chem. 1984 Aug 10;259(15):9635–9641. [PubMed] [Google Scholar]
  4. Fesenko E. E., Kolesnikov S. S., Lyubarsky A. L. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature. 1985 Jan 24;313(6000):310–313. doi: 10.1038/313310a0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Haynes L. W., Kay A. R., Yau K. W. Single cyclic GMP-activated channel activity in excised patches of rod outer segment membrane. Nature. 1986 May 1;321(6065):66–70. doi: 10.1038/321066a0. [DOI] [PubMed] [Google Scholar]
  7. Hodgkin A. L., McNaughton P. A., Nunn B. J. Measurement of sodium-calcium exchange in salamander rods. J Physiol. 1987 Oct;391:347–370. doi: 10.1113/jphysiol.1987.sp016742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hodgkin A. L., McNaughton P. A., Nunn B. J. The ionic selectivity and calcium dependence of the light-sensitive pathway in toad rods. J Physiol. 1985 Jan;358:447–468. doi: 10.1113/jphysiol.1985.sp015561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hodgkin A. L., Nunn B. J. The effect of ions on sodium-calcium exchange in salamander rods. J Physiol. 1987 Oct;391:371–398. doi: 10.1113/jphysiol.1987.sp016743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kawamura S., Murakami M. In situ cGMP phosphodiesterase and photoreceptor potential in gecko retina. J Gen Physiol. 1986 May;87(5):737–759. doi: 10.1085/jgp.87.5.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lamb T. D., Matthews H. R., Torre V. Incorporation of calcium buffers into salamander retinal rods: a rejection of the calcium hypothesis of phototransduction. J Physiol. 1986 Mar;372:315–349. doi: 10.1113/jphysiol.1986.sp016011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Liebman P. A., Mueller P., Pugh E. N., Jr Protons suppress the dark current of frog retinal rods. J Physiol. 1984 Feb;347:85–110. doi: 10.1113/jphysiol.1984.sp015055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Miller W. H. Physiological evidence that light-mediated decrease in cyclic GMP is an intermediary process in retinal rod transduction. J Gen Physiol. 1982 Jul;80(1):103–123. doi: 10.1085/jgp.80.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pepe I. M., Panfoli I., Cugnoli C. Guanylate cyclase in rod outer segments of the toad retina. Effect of light and Ca2+. FEBS Lett. 1986 Jul 14;203(1):73–76. doi: 10.1016/0014-5793(86)81439-9. [DOI] [PubMed] [Google Scholar]
  17. Pugh E. N., Jr, Cobbs W. H. Visual transduction in vertebrate rods and cones: a tale of two transmitters, calcium and cyclic GMP. Vision Res. 1986;26(10):1613–1643. doi: 10.1016/0042-6989(86)90051-9. [DOI] [PubMed] [Google Scholar]
  18. Robinson P. R., Kawamura S., Abramson B., Bownds M. D. Control of the cyclic GMP phosphodiesterase of frog photoreceptor membranes. J Gen Physiol. 1980 Nov;76(5):631–645. doi: 10.1085/jgp.76.5.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sather W. A., Detwiler P. B. Intracellular biochemical manipulation of phototransduction in detached rod outer segments. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9290–9294. doi: 10.1073/pnas.84.24.9290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sitaramayya A., Harkness J., Parkes J. H., Gonzalez-Oliva C., Liebman P. A. Kinetic studies suggest that light-activated cyclic GMP phosphodiesterase is a complex with G-protein subunits. Biochemistry. 1986 Feb 11;25(3):651–656. doi: 10.1021/bi00351a021. [DOI] [PubMed] [Google Scholar]
  21. Stryer L. Cyclic GMP cascade of vision. Annu Rev Neurosci. 1986;9:87–119. doi: 10.1146/annurev.ne.09.030186.000511. [DOI] [PubMed] [Google Scholar]
  22. Torre V., Matthews H. R., Lamb T. D. Role of calcium in regulating the cyclic GMP cascade of phototransduction in retinal rods. Proc Natl Acad Sci U S A. 1986 Sep;83(18):7109–7113. doi: 10.1073/pnas.83.18.7109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Yamazaki A., Sen I., Bitensky M. W., Casnellie J. E., Greengard P. Cyclic GMP-specific, high affinity, noncatalytic binding sites on light-activated phosphodiesterase. J Biol Chem. 1980 Dec 10;255(23):11619–11624. [PubMed] [Google Scholar]
  24. Yau K. W., Nakatani K. Electrogenic Na-Ca exchange in retinal rod outer segment. Nature. 1984 Oct 18;311(5987):661–663. doi: 10.1038/311661a0. [DOI] [PubMed] [Google Scholar]
  25. Zimmerman A. L., Baylor D. A. Cyclic GMP-sensitive conductance of retinal rods consists of aqueous pores. Nature. 1986 May 1;321(6065):70–72. doi: 10.1038/321070a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES