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Modulation of transduction gain in light adaptation of retinal rods

Published online by Cambridge University Press:  02 June 2009

David R. Pepperberg ,
Jing Jin  and
Gregor J. Jones
David R. Pepperberg
Affiliation:
Lions of Illinois Eye Research Institute, Department of Ophthalmology and Visual Sciences, University of Illinois at Chicago College of Medicine, Chicago
Jing Jin
Affiliation:
Department of Physiology, Boston University School of Medicine, Boston
Gregor J. Jones
Affiliation:
Department of Physiology, Boston University School of Medicine, Boston
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Abstract

The effect of light adaptation on the period of photocurrent saturation induced by a bright stimulating flash was examined in rod photoreceptors of the larval-stage tiger salamander (Ambystoma tigrinum). Using suction electrodes, photocurrent responses to brief flashes were recorded from single, isolated rods in the presence and absence of steady background illumination. Background light decreased the saturation period (T) measured at fixed flash intensity (fixed If) and in this respect light-adapted the saturating response. Effects of the background on responses to weak (i.e. subsaturating) and bright flashes were compared with changes in a parameter, where ΔT is the decrease in saturation period, and where TR* is the slope of the line that relates T and ln If in a given state of adaptation. Dark- and light-adapted responses to flash intensities and , respectively, exhibited similar absolute peak photocurrent and falling-phase kinetics when and satisfied the relation, , where Ib is the background intensity. It is argued that ψ approximates the relative PDE*/R* gain of transduction, i.e. the relative peak level of activated cGMP phosphodiesterase (PDE*) produced by a given, small amount of photoactivated visual pigment (R*). Interpreted on this view, the results imply that light adaptation derives largely from a decrease in PDE*/R* gain, rather than from the stimulation of guanylate cyclase activity. The data are consistent with the possibility that modulation of the lifetime of PDE* underlies the background dependence of ψ.

Keywords

Light adaptationBackground desensitizationRodPhotoreceptorPhototransduction
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 1 , January 1994 , pp. 53 - 62
Copyright
Copyright © Cambridge University Press 1994

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References

Ames, A. III, Walseth, T.F., Heyman, R.A., Barad, M., Graeff, R.M. & Goldberg, N.D. (1986). Light-induced increases in cGMP metabolic flux correspond with electrical responses of photoreceptors. Journal of Biological Chemistry 261, 13034–13042.CrossRefGoogle ScholarPubMed
Arshavsky, V.Y. & Bownds, M.D. (1992). Regulation of deactivation of photoreceptor G protein by its target enzyme and cGMP. Nature 357, 416–417.CrossRefGoogle Scholar
Arshavsky, V.Y., Dumke, C.L. & Bownds, M.D. (1992). Noncatalytic cGMP-binding sites of amphibian rod cGMP phosphodiesterase control interaction with its inhibitory γ-subunits. A putative regulatory mechanism of the rod photoresponse. Journal of Biological Chemistry 267, 24501–24507.CrossRefGoogle ScholarPubMed
Arshavsky, V.Y., Gray-Keller, M.P. & Bownds, M.D. (1991). cGMP suppresses GTPase activity of a portion of transducin equimolar to phosphodiesterase in frog rod outer segments. Light-induced cGMP decreases as a putative feedback mechanism of the photoresponse. Journal of Biological Chemistry 266, 18530–18537.Google Scholar
Barkdoll, A.E. III, Puch, E.N. Jr. & Sitaramayya, A. (1989). Calcium dependence of the activation and inactivation kinetics of the light-activated phosphodiesterase of retinal rods. Journal of General Physiology 93, 1091–1108.CrossRefGoogle ScholarPubMed
Baylor, D.A., Lamb, T.D. & Yau, K.-W. (1979). The membrane current of single rod outer segments. Journal of Physiology 288, 589–611.CrossRefGoogle ScholarPubMed
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1984). The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. Journal of Physiology 357, 575–607.CrossRefGoogle ScholarPubMed
Bruckert, F., Vuong, T.M. & Chabre, M. (1988). Light and GTP dependence of transducin solubility in retinal rods. Further analysis by near infra-red light scattering. European Biophysics Journal 16, 207–218.CrossRefGoogle ScholarPubMed
Chabre, M. & Vuong, T. M. (1992). Kinetics and energetics of the rho-dopsin-transducin-cGMP phosphodiesterase cascade of visual transduction. Biochimica et Biophysica Acta 1101, 260–263.CrossRefGoogle ScholarPubMed
Clack, J.W. & Pepperberg, D.R. (1982). Desensitization of skate photoreceptors by bleaching and background light. Journal of General Physiology 80, 863–883.CrossRefGoogle ScholarPubMed
Cobbs, W.H. (1991). Light and dark active phosphodiesterase regulation in salamander rods. Journal of General Physiology 98, 575–614.CrossRefGoogle ScholarPubMed
Cobbs, W.H. & Pugh, E.N. Jr. (1987). Kinetics and components of the flash photocurrent of isolated retinal rods of the larval salamander, Ambystoma tigrinum. Journal of Physiology 394, 529–572.CrossRefGoogle ScholarPubMed
Cohen, A.I. & Blazynski, C. (1993). The determination of total cGMP levels in rod outer segments from intact toad photoreceptors in response to light superimposed on background and to consecutive flashes: A second light flash accelerates the dark recovery rate of cGMP levels in control media, but not in Na+-free, low Ca2+ medium. Visual Neuroscience 10, 73–79.CrossRefGoogle Scholar
Cornwall, M.C. & Fain, G.L. (1992). Bleaching of rhodopsin in isolated rods causes a sustained activation of PDE and cyclase which is reversed by pigment regeneration. Investigative Ophthalmology and Visual Science (Abstr.) 33, 1103.Google Scholar
Cornwall, M.C., Fein, A. & MacNichol, E.F. Jr. (1990). Cellular mechanisms that underlie bleaching and background adaptation. Journal of General Physiology 96, 345–372.CrossRefGoogle ScholarPubMed
Cornwall, M.C., MacNichol, E.F. Jr. & Fein, A. (1984). Absorptance and spectral sensitivity measurements of rod photoreceptors of the tiger salamander, Ambystoma tigrinum. Vision Research 24, 1651–1659.CrossRefGoogle ScholarPubMed
Cornwall, M.C., Ripps, H., Chappell, R.L. & Jones, G.J. (1989). Membrane current responses of skate photoreceptors. Journal of General Physiology 94, 633–647.CrossRefGoogle ScholarPubMed
Corson, D.W., Cornwall, M.C. & Pepperberg, D.R. (1994). Evidence for the prolonged photoactivated lifetime of an analogue visual pigment containing 11–cis 9–desmethylretinal. Visual Neuroscience 11, 91–98 (this issue).CrossRefGoogle ScholarPubMed
Dawis, S.M. (1991). A molecular basis for Weber’s law. Visual Neuroscience 7, 285–320.CrossRefGoogle ScholarPubMed
Dawis, S.M., Graeff, R.M., Heyman, R.A., Walseth, T.F. & Goldberg, N.D. (1988). Regulation of cyclic GMP metabolism in toad photoreceptors. Definition of the metabolic events subserving photoexcited and attenuated states. Journal of Biological Chemistry 263, 8771–8785.CrossRefGoogle ScholarPubMed
Dizhoor, A.M., Ray, S., Kumar, S., Niemi, G., Spencer, M., Brolley, D., Walsh, K.A., Philipov, P.P., Hurley, J.B. & Stryer, L. (1991). Recoverin: A calcium sensitive activator of retinal rod guanylate cyclase. Science 251, 915–918.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Ripps, H. (1972). Adaptation in skate photoreceptors. Journal of General Physiology 60, 698–719.CrossRefGoogle ScholarPubMed
Fain, G.L., Lamb, T.D., Matthews, H.R. & Murphy, R.L.W. (1989). Cytoplasmic calcium as the messenger for light adaptation in salamander rods. Journal of Physiology 416, 215–243.CrossRefGoogle ScholarPubMed
Forti, S., Menini, A., Rispoli, G. & Torre, V. (1989). Kinetics of phototransduction in retinal rods of the newt Triturus cristatus. Journal of Physiology 419, 265–295.CrossRefGoogle ScholarPubMed
Green, D.G., Dowling, J.E., Siegel, I.M. & Ripps, H. (1975). Retinal mechanisms of visual adaptation in the skate. Journal of General Physiology 65, 483–502.CrossRefGoogle ScholarPubMed
Hodgkin, A.L. & Nunn, B.J. (1988). Control of light-sensitive current in salamander rods. Journal of Physiology 403, 439–471.CrossRefGoogle ScholarPubMed
Hsu, Y.-T. & Molday, R.S. (1993). Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin. Nature 361, 76–79.CrossRefGoogle ScholarPubMed
Jones, G.J. (1993). Light adaptation and the initial rise of the retinal rod photoresponse. Investigative Ophthalmology and Visual Science (Abstr.) 34, 1326.Google Scholar
Kahlert, M., Pepperberg, D.R. & Hofmann, K.P. (1990). Effect of bleached rhodopsin on signal amplification in rod visual receptors. Nature 345, 537–539.CrossRefGoogle ScholarPubMed
Kawamura, S. (1993). Rhodopsin phosphorylation as a mechanism of cyclic GMP phosphodiesterase regulation by S-modulin. Nature 362, 855–857.CrossRefGoogle ScholarPubMed
Kawamura, S. & Murakami, M. (1991). Calcium-dependent regulation of cyclic GMP phosphodiesterase by a protein from frog retinal rods. Nature 349, 420–423.CrossRefGoogle ScholarPubMed
Koch, K.-W. & Stryer, L. (1988). Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334, 64–66.CrossRefGoogle ScholarPubMed
Kondo, H. & Miller, W.H. (1988). Rod light adaptation may be mediated by acceleration of the phosphodiesterase-guanylate cyclase cycle. Proceedings of the National Academy of Sciences of the U.S.A. 85, 1322–1326.CrossRefGoogle ScholarPubMed
Lagnado, L., Cervetto, L. & McNaughton, PA. (1992). Calcium homeostasis in the outer segments of retinal rods from the tiger salamander. Journal of Physiology 455, 111–142.CrossRefGoogle ScholarPubMed
Lamb, T.D., McNaughton, P.A. & Yau, K.-W. (1981). Spatial spread of activation and background desensitization in toad rod outer segments. Journal of Physiology 319, 463–496.CrossRefGoogle ScholarPubMed
Lamb, T.D. & Pugh, E.N. Jr. (1992). A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. Journal of Physiology 449, 719–758.CrossRefGoogle ScholarPubMed
Liebman, P.A., Parker, K.R. & Dratz, E.A. (1987). The molecular mechanism of visual excitation and its relation to the structure and composition of the rod outer segment. Annual Review of Physiology 49, 765–791.CrossRefGoogle Scholar
Liebman, P.A. & Pugh, E.N. Jr. (1982). Gain, speed and sensitivity of GTP binding vs. PDE activation in visual excitation. Vision Research 22, 1475–1480.CrossRefGoogle ScholarPubMed
Lolley, R.N. & Racz, E. (1982). Calcium modulation of cyclic GMP synthesis in rat visual cells. Vision Research 22, 1481–1486.CrossRefGoogle ScholarPubMed
Matthews, H.R. (1991). Incorporation of chelator into guinea-pig rods shows that calcium mediates mammalian photoreceptor light adaptation. Journal of Physiology 436, 93–105.CrossRefGoogle ScholarPubMed
Matthews, H.R., Murphy, R.L.W., Fain, G.L. & Lamb, T.D. (1988). Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature 334, 67–69.CrossRefGoogle ScholarPubMed
McNaughton, P.A., Cervetto, L. & Nunn, B.J. (1986). Measurement of the intracellular free calcium concentration in salamander rods. Nature 322, 261–263.CrossRefGoogle ScholarPubMed
Miller, D.L. & Korenbrot, J.I. (1987). Kinetics of light-dependent Ca fluxes across the plasma membrane of rod outer segments. A dynamic model of the regulation of the cytoplasmic Ca concentration. Journal of General Physiology 90, 397–425.CrossRefGoogle ScholarPubMed
Nakatani, K. & Yau, K.-W. (1988). Calcium and light adaptation in retinal rods and cones. Nature 334, 69–71.CrossRefGoogle ScholarPubMed
Nicol, G.D. & Bownds, M.D. (1989). Calcium regulates some, but not all, aspects of light adaptation in rod photoreceptors. Journal of General Physiology 94, 233–259.CrossRefGoogle Scholar
Pepperberg, D.R., Cornwall, M.C., Kahlert, M., Hofmann, K.P., Jin, J., Jones, G.J. & Ripps, H. (1992). Light-dependent delay in the falling phase of the retinal rod photoresponse. Visual Neuro-science 8, 9–18.CrossRefGoogle ScholarPubMed
Pepperberg, D.R., Kahlert, M., Krause, A. & Hofmann, K.P. (1988). Photic modulation of a highly sensitive, near-infrared light-scattering signal recorded from intact retinal photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 85, 5531–5535.CrossRefGoogle ScholarPubMed
Pugh, E.N. Jr. & Lamb, T.D. (1990). Cyclic GMP and calcium: The internal messengers of excitation and adaptation in vertebrate photoreceptors. Vision Research 30, 1923–1948.CrossRefGoogle ScholarPubMed
Ratto, G.M., Payne, R., Owen, W.G. & Tsien, R.Y. (1988). The concentration of cytosolic free calcium in vertebrate rod outer segments measured with fura-2. Journal of Neuroscience 8, 3240–3246.CrossRefGoogle ScholarPubMed
Rispoli, G. & Detwiler, P.B. (1989). Light adaptation in gekko rods may involve changes in both the initial and terminal stages of the transduction cascade. Biophysical Journal (Abstr.) 55, 380a.Google Scholar
Robinson, P.R., Kawamura, S., Abramson, B. & Bownds, M.D. (1980). Control of the cyclic GMP phosphodiesterase of frog photoreceptor membranes. Journal of General Physiology 76, 631–645.CrossRefGoogle ScholarPubMed
Shapley, R. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. In Progress in Retinal Research, Vol. 3, ed. Osborne, N.N. & Chader, G.J., pp. 263–346. Oxford, England: Pergamon Press.Google Scholar
Tamura, T., Nakatani, K. & Yau, K.-W. (1989). Light adaptation in cat retinal rods. Science 245, 755–758.CrossRefGoogle ScholarPubMed
Tamura, T., Nakatani, K. & Yau, K.-W. (1991). Calcium feedback and sensitivity regulation in primate rods. Journal of General Physiology 98, 95–130.CrossRefGoogle ScholarPubMed
Torre, V., Matthews, H.R. & Lamb, T.D. (1986). Role of calcium in regulating the cyclic GMP cascade of phototransduction in retinal rods. Proceedings of the National Academy of Sciences of the U.S.A. 83, 7109–7113.CrossRefGoogle ScholarPubMed
Tranchina, D., Sneyd, J. & Cadenas, I.D. (1991). Light adaptation in turtle cones. Testing and analysis of a model for phototransduction. Biophysical Journal 60, 217–237.CrossRefGoogle Scholar
Vuong, T.M. & Chabre, M. (1991). Deactivation kinetics of the transduction cascade of vision. Proceedings of the National Academy of Sciences of the U.S.A. 88, 9813–9817.CrossRefGoogle ScholarPubMed
Yau, K.-W. & Nakatani, K. (1985). Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment. Nature 313, 579–582.CrossRefGoogle ScholarPubMed