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Cyclic GMP levels and membrane current during onset, recovery, and light adaptation of the photoresponse of detached frog photoreceptors*

  • R H Cote
    Correspondence
    To whom correspondence should be addressed.
    Affiliations
    Laboratory of Molecular Biology, University of Wisconsin, Madison, Wisconsin 53706

    Dept. of Biochemistry, University of New Hampshire, Durham, NH 03824-3544
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  • G D Nicol
    Affiliations
    Laboratory of Molecular Biology, University of Wisconsin, Madison, Wisconsin 53706

    Dept. of Pharmacology and Toxicology, Indiana University, 635 Barnhill Dr., Indianapolis, IN 46202
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  • S A Burke
    Affiliations
    Laboratory of Molecular Biology, University of Wisconsin, Madison, Wisconsin 53706
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  • M D Bownds
    Affiliations
    Laboratory of Molecular Biology, University of Wisconsin, Madison, Wisconsin 53706
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  • Author Footnotes
    * This work was supported by Research Grants EY05798 (to R. H. C.) and EY00496 (to M. D. B.) from the National Institutes of Health. Scientific contribution No. 1611 from the New Hampshire Agricultural Experiment Station. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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      We have used a preparation of isolated, intact rod photoreceptors to correlate the effects of flash illumination on the intracellular cyclic GMP content and the membrane current. We find that the recovery of cyclic GMP levels after brief flash illumination requires approximately twice as much time as the recovery of the membrane current. In contrast, the subsecond kinetics of the cyclic GMP response to light are faster than the kinetics of membrane current suppression. Both cyclic GMP and the membrane current show graded responses to a wide range of flash intensities; however, in a low Ca2+-Ringer's solution, dim flashes can trigger a decrease in cyclic GMP concentration with no corresponding decrease in membrane current. These results suggest that either other factors can regulate the membrane current, or that measurements of total cellular cyclic GMP do not accurately reflect dynamic changes in cyclic GMP concentration in the vicinity of the light-regulated channel. Changes in cyclic GMP concentration in the presence of background illumination exhibit adaptational behavior similar to that observed in a light-adapted photoresponse: acceleration in the response kinetics and a decrease in response amplitude. That this result is observed in rods depleted of internal Ca2+ suggests a Ca2+-independent mechanism by which background illumination can accelerate the cyclic GMP response.

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