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. 1996 Aug 15;495(Pt 1):1–13. doi: 10.1113/jphysiol.1996.sp021569

Kinetics of desensitization induced by saturating flashes in toad and salamander rods.

J G Murnick 1, T D Lamb 1
PMCID: PMC1160720  PMID: 8866347

Abstract

1. The suction pipette technique was used to examine the effect of a conditioning pre-flash on the saturation time (tsat) of a bright test flash (intensity 10,000-250,000 isomerizations) delivered to intact salamander or toad rod outer segments. The conditioning flash was delivered 0-60 s before the test flash; its intensity was typically between six and sixty times dimmer than the test flash, and it was sufficient by itself to fully saturate the photocurrent. 2. A saturating pre-flash delivered before a saturating test flash reduced the tsat of the test flash. This was equivalent to a reduction in phototransduction gain (psi). 3. The pre-flash had little effect on tau zero the time constant of decay of the rate-limiting species in photoresponse inactivation (activated rhodopsin or the activated G-protein-phosphodiesterase complex). 4. The tsat declined exponentially as the separation time between a fixed intensity pre-flash and test flash was increased. The time constant (tau p) of decline in tsat was approximately 2.4s. The maximum reduction in tsat corresponded to a reduction in the apparent gain of phototransduction to approximately 0.10 of its original level. This exponential decline is consistent with a [Ca2+]i-mediated effect. 5. We conclude that the rate-limiting step in response inactivation and the step responsible for light-induced gain reduction constitute separate and distinct steps of the phototransduction cascade.

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Selected References

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  1. 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]
  2. 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]
  3. Baylor D. A., Lamb T. D., Yau K. W. Responses of retinal rods to single photons. J Physiol. 1979 Mar;288:613–634. [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. Corson D. W., Cornwall M. C., Pepperberg D. R. Evidence for the prolonged photoactivated lifetime of an analogue visual pigment containing 11-cis 9-desmethylretinal. Vis Neurosci. 1994 Jan-Feb;11(1):91–98. doi: 10.1017/s0952523800011135. [DOI] [PubMed] [Google Scholar]
  6. Gray-Keller M. P., Detwiler P. B. The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron. 1994 Oct;13(4):849–861. doi: 10.1016/0896-6273(94)90251-8. [DOI] [PubMed] [Google Scholar]
  7. Koch K. W., Stryer L. Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature. 1988 Jul 7;334(6177):64–66. doi: 10.1038/334064a0. [DOI] [PubMed] [Google Scholar]
  8. Koutalos Y., Nakatani K., Tamura T., Yau K. W. Characterization of guanylate cyclase activity in single retinal rod outer segments. J Gen Physiol. 1995 Nov;106(5):863–890. doi: 10.1085/jgp.106.5.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Koutalos Y., Nakatani K., Yau K. W. The cGMP-phosphodiesterase and its contribution to sensitivity regulation in retinal rods. J Gen Physiol. 1995 Nov;106(5):891–921. doi: 10.1085/jgp.106.5.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lagnado L., Baylor D. A. Calcium controls light-triggered formation of catalytically active rhodopsin. Nature. 1994 Jan 20;367(6460):273–277. doi: 10.1038/367273a0. [DOI] [PubMed] [Google Scholar]
  11. Lagnado L., Cervetto L., McNaughton P. A. Calcium homeostasis in the outer segments of retinal rods from the tiger salamander. J Physiol. 1992 Sep;455:111–142. doi: 10.1113/jphysiol.1992.sp019293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Lamb T. D., Pugh E. N., Jr A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. J Physiol. 1992 Apr;449:719–758. doi: 10.1113/jphysiol.1992.sp019111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lyubarsky A., Nikonov S., Pugh E. N., Jr The kinetics of inactivation of the rod phototransduction cascade with constant Ca2+i. J Gen Physiol. 1996 Jan;107(1):19–34. doi: 10.1085/jgp.107.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Matthews H. R. Effects of lowered cytoplasmic calcium concentration and light on the responses of salamander rod photoreceptors. J Physiol. 1995 Apr 15;484(Pt 2):267–286. doi: 10.1113/jphysiol.1995.sp020664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Matthews H. R., Fain G. L., Murphy R. L., Lamb T. D. Light adaptation in cone photoreceptors of the salamander: a role for cytoplasmic calcium. J Physiol. 1990 Jan;420:447–469. doi: 10.1113/jphysiol.1990.sp017922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Matthews H. R. Incorporation of chelator into guinea-pig rods shows that calcium mediates mammalian photoreceptor light adaptation. J Physiol. 1991 May;436:93–105. doi: 10.1113/jphysiol.1991.sp018541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Matthews H. R., Murphy R. L., Fain G. L., Lamb T. D. Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature. 1988 Jul 7;334(6177):67–69. doi: 10.1038/334067a0. [DOI] [PubMed] [Google Scholar]
  19. Matthews H. R. Static and dynamic actions of cytoplasmic Ca2+ in the adaptation of responses to saturating flashes in salamander rods. J Physiol. 1996 Jan 1;490(Pt 1):1–15. doi: 10.1113/jphysiol.1996.sp021123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. McCarthy S. T., Younger J. P., Owen W. G. Free calcium concentrations in bullfrog rods determined in the presence of multiple forms of Fura-2. Biophys J. 1994 Nov;67(5):2076–2089. doi: 10.1016/S0006-3495(94)80691-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nakatani K., Yau K. W. Calcium and light adaptation in retinal rods and cones. Nature. 1988 Jul 7;334(6177):69–71. doi: 10.1038/334069a0. [DOI] [PubMed] [Google Scholar]
  22. Pepperberg D. R., Cornwall M. C., Kahlert M., Hofmann K. P., Jin J., Jones G. J., Ripps H. Light-dependent delay in the falling phase of the retinal rod photoresponse. Vis Neurosci. 1992 Jan;8(1):9–18. doi: 10.1017/s0952523800006441. [DOI] [PubMed] [Google Scholar]
  23. Pepperberg D. R., Jin J., Jones G. J. Modulation of transduction gain in light adaptation of retinal rods. Vis Neurosci. 1994 Jan-Feb;11(1):53–62. doi: 10.1017/s095252380001110x. [DOI] [PubMed] [Google Scholar]
  24. Pulvermüller A., Palczewski K., Hofmann K. P. Interaction between photoactivated rhodopsin and its kinase: stability and kinetics of complex formation. Biochemistry. 1993 Dec 28;32(51):14082–14088. doi: 10.1021/bi00214a002. [DOI] [PubMed] [Google Scholar]
  25. Ratto G. M., Payne R., Owen W. G., Tsien R. Y. The concentration of cytosolic free calcium in vertebrate rod outer segments measured with fura-2. J Neurosci. 1988 Sep;8(9):3240–3246. doi: 10.1523/JNEUROSCI.08-09-03240.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tamura T., Nakatani K., Yau K. W. Calcium feedback and sensitivity regulation in primate rods. J Gen Physiol. 1991 Jul;98(1):95–130. doi: 10.1085/jgp.98.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Yau K. W., Nakatani K. Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment. Nature. 1985 Feb 14;313(6003):579–582. doi: 10.1038/313579a0. [DOI] [PubMed] [Google Scholar]

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