Abstract
The vertebrate visual system can operate over a large range of light intensities. This is possible in part because the sensitivity of photoreceptors decreases approximately in inverse proportion to the background light intensity1–3. This process, called photoreceptor light adaptation, is known to be mediated by a diffusible intracellular messenger4–6, but the identity of the messenger is still unclear. There has been considerable speculation that decreased cytoplasmic Ca2+ concentration (Cai2+) may play a role in light adaptation7–11, and recent experiments in which Ca2+ buffer was incorporated into rod-cells10,11 have supported this notion. The extent of the contribution of calcium, however, remains unresolved. We now show that light-dependent changes in sensitivity in amphibian photoreceptors can be abolished by preventing movements of Ca2+ across the outer-segment plasma membrane. These experiments demonstrate that light adaptation in photoreceptors is mediated in cones primarily, and in rods perhaps exclusively, by changes in Cai2+.
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References
Baylor, D. A. & Hodgkin, A. L. J. Physiol 242, 729–758 (1974).
Fain, G. L. J. Physiol. 261, 71–101 (1976).
Baylor, D. A., Matthews, G. & Yau, K.-W. J. Physiol. 309, 591–621 (1980).
Dornner, K. O. & Hemilä, S. Med. biol. 56, 52–63 (1978).
Bastian, B. & Fain, G. L. J. Physiol 297, 493–520 (1979).
Lamb, T. D., McNaughton, P. A. & Yau, K.-W. J. Physiol. 319, 463–496 (1981).
Bownds, M. D. Photochem. Photobiol. 32, 487–490 (1980).
Yau, K.-W. & Nakatani, K. Nature 313, 579–581 (1985).
Cervetto, L., Torre, V., Rispoli, G. & Marroni, P. Expl Biol. 44, 147–157 (1985).
Torre, V., Matthews, H. R. & Lamb, T. D. Proc. natn. Acad. Sci. U.S.A. 83, 7109–7113 (1986).
Korenbrot, J. I. & Miller, D. L. Neurosci. Res. 4, S11–S34 (1986).
Capovilla, M., Caretta, A., Cervetto, L. & Torre, V. J. Physiol. 343, 295–310 (1983).
Yau, K.-W. & Nakatani, K. Nature 309, 352–354 (1984).
Hodgkin, A. L., McNaughton, P. A. & Nunn, B. J. J. Physiol. 358, 447–468 (1985).
Yau, K.-W. & Nakatani, K. Nature 311, 579–581 (1984).
Hodgkin, A. L., McNaughton, P. A. & Nunn, B. J. J. Physiol. 391, 347–370 (1987).
Lagnado, L., Cervetto, L. & McNaughton, P. A. Proc. natn. Acad. Sci. U.S.A. 85 (in the press).
McNaughton, P. A., Cervetto, L. & Nunn, B. J. Nature 322, 261–263 (1986).
Gold, G. H. Proc. natn. Acad. Sci. U.S.A. 83, 1150–1154 (1986).
Ratto, G. M., Payne, R., Owen, W. G. & Tsien, R. Y. J. Neurosci. (in the press).
Yau, K.-W. & Nakatani, K. Biophys. J. 53, 473a (1988).
Lamb, T. D. & Matthews, H. R. J. Physiol. 403 (in the press).
Baylor, D. A., Nunn, B. J. & Schnapf, J. L. J. Physiol. 357, 575–607 (1984).
Tsien, R. Y. Biochemistry 19, 2396–2404 (1980).
Fleischman, D. & Denisevich, M. Biochemistry 18, 5060–5066 (1979).
Lolley, R. N. & Racz, E. Vision Res. 22, 1481–1486 (1982).
Pepe, I. M., Panfoli, I. & Cugnoli, C. FEBS Lett. 203, 73–76 (1986).
Koch, K.-W. & Stryer, L. Nature 334, 64–66 (1988).
Hodgkin, A. L. & Nunn, B. J., J. Physiol. 403 (in the press).
Robinson, P. R., Kawamura, S., Abramson, B. & Bownds, M. D. J. gen. Physiol. 76, 631–645 (1980).
Lisman, J. E. & Brown, J. E. in The Visual System: Neurophysiology, Biophysics and Their Clinical Applications (ed. Arden, G. B.) 23–33 (Plenum, New York, 1971).
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Matthews, H., Murphy, R., Fain, G. et al. Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature 334, 67–69 (1988). https://doi.org/10.1038/334067a0
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DOI: https://doi.org/10.1038/334067a0
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