Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-10T22:24:20.619Z Has data issue: false hasContentIssue false
  • English
  • Français

Light-dependent delay in the falling phase of the retinal rod photoresponse

Published online by Cambridge University Press:  02 June 2009

David R. Pepperberg ,
M. Carter Cornwall ,
Martina Kahlert ,
Klaus Peter Hofmann ,
Jing Jin ,
Gregor J. Jones  and
Harris Ripps
David R. Pepperberg
Affiliation:
Lions of Illinois Eye Research Institute, Department of Ophthalmology and Visual Sciences, University of Illinois College of Medicine, Chicago
M. Carter Cornwall
Affiliation:
Department of Physiology, Boston University School of Medicine, Boston
Martina Kahlert
Affiliation:
Institut für Biophysik und Strahlenbiologie, Albert-Ludwigs Universität, D-7800 Freiburg, Federal Republic of Germany
Klaus Peter Hofmann
Affiliation:
Institut für Biophysik und Strahlenbiologie, Albert-Ludwigs Universität, D-7800 Freiburg, Federal Republic of Germany
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
Harris Ripps
Affiliation:
Lions of Illinois Eye Research Institute, Department of Ophthalmology and Visual Sciences, University of Illinois College of Medicine, Chicago Department of Anatomy–Cell Biology, University of Illinois College of Medicine, Chicago
Get access Rights & Permissions [Opens in a new window]

Abstract

Using suction electrodes, photocurrent responses to 100-ms saturating flashes were recorded from isolated retinal rods of the larval-stage tiger salamander (Ambystoma tigrinum). The delay period (Te) that preceded recovery of the dark current by a criterion amount (3 pA) was analyzed in relation to the flash intensity (If), and to the corresponding fractional bleach (R*0/Rtot) of the visual pigment; R*0/Rtot was compared with R*s/Rtot the fractional bleach at which the peak level of activated transducin approaches saturation. Over an approximately 8 In unit range of If that included the predicted value of R*s/Rtot, Te increased linearly with In If. Within the linear range, the slope of the function yielded an apparent exponential time constant (TC) of 1.7 ± 0.2 s (mean ± S.D.). Background light reduced the value of Tc measured at a given flash intensity but preserved a range over which Tc increased linearly with In If; the linear-range slope was similar to that measured in the absence of background light. The intensity dependence of Tc resembles that of a delay (Td) seen in light-scattering experiments on bovine retinas, which describes the period of essentially complete activation of transducin following a bright flash; the slope of the function relating Td and In flash intensity is thought to reflect the lifetime of photoactivated visual pigment (R*) (Pepperberg et al., 1988; Kahlert et al., 1990). The present data suggest that the electrophysiological delay has a similar basis in the deactivation kinetics of R*, and that Tc represents TR* the lifetime of R* in the phototransduction process. The results furthermore suggest a preservation of the “dark-adapted” value of TR* within the investigated range of background intensity.

Keywords

Visual pigmentRod photocurrentR* deactivationTransducinPhotoreceptor
Type
Research Articles
Information
Visual Neuroscience , Volume 8 , Issue 1 , January 1992 , pp. 9 - 18
Copyright
Copyright © Cambridge University Press 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bader, C.R., Macleish, P.R. & Schwartz, E.A. (1979). A voltage-clamp study of the light response in solitary rods of the tiger salamander. Journal of Physiology 296, 1–26.CrossRefGoogle ScholarPubMed
Baehr, W., Morita, E.A., Swanson, R.J. & Applebury, M.L. (1982). Characterization of bovine rod outer segment G-protein. Journal of Biological Chemistry 257, 6452–6460.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Lamb, T.D. (1982). Local effects of bleaching in retinal rods of the toad. Journal of Physiology 328, 49–71.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., Matthews, G. & Nunn, B.J. (1984 a). Location and function of voltage-sensitive conductances in retinal rods of the salamander, Ambystoma tigrinum. Journal of Physiology 354, 203–223.CrossRefGoogle ScholarPubMed
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1984 b). The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. Journal of Physiology 357, 575–607.CrossRefGoogle ScholarPubMed
Baylor, D.A., Matthews, G. & Yau, K.-W. (1983). Temperature effects on the membrane current of retinal rods of the toad. Journal of Physiology 337, 723–734.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Nunn, B.J. (1986). Electrical properties of the light-sensitive conductance of rods of the salamander Ambystoma tigrinum. Journal of Physiology 371, 115–145.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. & Deterre, P. (1989). Molecular mechanism of visual transduction. European Journal of Biochemistry 179, 255–266.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
Cornwall, M.C., Fein, A. & MacNichol, E.F. Jr (1983). Spatial localization of bleaching adaptation in isolated vertebrate rod photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 80, 2785–2788.CrossRefGoogle ScholarPubMed
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
Dartnall, H.J.A. (1957). The Visual Pigments. London: Methuen.CrossRefGoogle Scholar
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
Ernst, W., Kemp, C.M. & Price, D.E. (1978). Studies on the effects of bleaching amphibian rod pigments in situ. I. The absorbance spectra of axolotl and tiger salamander rhodopsin and porphyropsin. Experimental Eye Research 26, 329–336.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
Fain, G.L. & Schröder, W.H. (1990). Light-induced calcium release and re-uptake in toad rods. Journal of Neuroscience 10, 2238–2249.CrossRefGoogle ScholarPubMed
Fesenko, E.E., Kolesnikov, S.S. & Lyubarsky, A.L. (1985). Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313, 310–313.Google Scholar
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
Godchaux, W. III & Zimmerman, W.F. (1979). Membrane-dependent guanine nucleotide binding and GTPase activities of soluble protein from bovine rod cell outer segments. Journal of Biological Chemistry 254, 7874–7884.CrossRefGoogle ScholarPubMed
Hamm, H.E. & Bownds, M.D. (1986). Protein complement of rod outer segments of frog retina. Biochemistry 25, 4512–4523.CrossRefGoogle ScholarPubMed
Harosi, F.I. (1975). Absorption spectra and linear dichroism of some amphibian photoreceptors. Journal of General Physiology 66, 357–382.Google Scholar
Hestrin, S. & Korenbrot, J.I. (1987). Effects of cyclic GMP on the kinetics of the photocurrent in rods and in detached rod outer segments. Journal of General Physiology 90, 527–551.CrossRefGoogle ScholarPubMed
Hodgkin, A.L., McNaughton, P.A., Nunn, B.J. & Yau, K.-W. (1984). Effect of ions on retinal rods from Bufo marinus. Journal of Physiology 350, 649–680.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
Jones, G.J., Crouch, R.K., Wiggert, B., Cornwall, M.C. & Chader, G.J. (1989). Retinoid requirements for recovery of sensitivity after visual-pigment bleaching in isolated photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 86, 9606–9610.Google Scholar
Kahlert, M. & Hofmann, K.P. (1991). Reaction rate and collisional efficiency of the rhodopsin-transducin system in intact retinal rods. Biophysical Journal 59, 375–386.CrossRefGoogle ScholarPubMed
Kahlert, M., Pepperberg, D.R. & Hofmann, K.P. (1990). Effect of bleached rhodopsin on signal amplification in rod visual receptors. Nature 345, 537–539.Google Scholar
Kamps, K.M.P., Reichert, J. & Hofmann, K.P. (1985). Light-induced activation of the rod phosphodiesterase leads to a rapid transient increase of near-infrared light scattering. Federation of European Biochemical Societies Letters 188, 15–20.CrossRefGoogle ScholarPubMed
Kawamura, S. & Murakami, M. (1986). In situ cGMP phosphodiesterase and photoreceptor potential in gecko retina. Journal of General Physiology 87, 737–759.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
Kühn, H., Bennett, N., Michel-Villaz, M. & Chabre, M. (1981). Interactions between photoexcited rhodopsin and GTP-binding protein: Kinetic and stoichiometric analyses from light-scattering changes. Proceedings of the National Academy of Sciences of the U.S.A. 78, 6873–6877.CrossRefGoogle ScholarPubMed
Lamb, T.D. (1980). Spontaneous quantal events induced in toad rods by pigment bleaching. Nature 287, 349–351.CrossRefGoogle ScholarPubMed
Lamb, T.D. (1984). Effects of temperature changes on toad rod photocurrents. Journal of Physiology 346, 557–578.CrossRefGoogle ScholarPubMed
Lamb, T.D. (1986). Photoreceptor adaptation–vertebrates. In The Molecular Mechanism of Photoreception, ed. Stieve, H., pp. 267–286. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Lamb, T.D. & Matthews, H.R. (1988). External and internal actions in the response of salamander retinal rods to altered external calcium concentration. Journal of Physiology 403, 473–494.CrossRefGoogle ScholarPubMed
Lamb, T.D., Matthews, H.R. & Torre, V. (1986). Incorporation of calcium buffers into salamander retinal rods: A rejection of the calcium hypothesis of phototransduction. Journal of Physiology 372, 315–349.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
Mangini, N.J., Pepperberg, D.R. & Baehr, W. (1986). Light-dependent binding of G-protein to outer segment membranes of toad photoreceptors. Journal of General Physiology 88, 675–694.CrossRefGoogle ScholarPubMed
Matthews, G. (1983). Physiological characteristics of single green rod photoreceptors from toad retina. Journal of Physiology 342, 347–359.CrossRefGoogle Scholar
Matthews, G. (1987). Single-channel recordings demonstrate that cGMP opens the light-sensitive ion channel of the rod photoreceptor. Proceedings of the National Academy of Sciences of the U.S.A. 84, 299–302.Google Scholar
Matthews, G. & Baylor, D.A. (1981). The photocurrent and dark current of retinal rods. In Current Topics in Membranes and Transport, Vol. 15: Molecular Mechanisms of Photoreceptor Transduction, ed. Miller, W.H., pp. 3–18. New York: Academic Press.CrossRefGoogle Scholar
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
Penn, R.D. & Hagins, W.A. (1972). Kinetics of the photocurrent of retinal rods. Biophysical Journal 12, 1073–1094.CrossRefGoogle ScholarPubMed
Pepe, I.M., Boero, A., Vergani, L., Panfoli, I. & Cugnoli, C. (1986). Effect of light and calcium on cyclic GMP synthesis in rod outer segments of toad retina. Biochimica et Biophysica Acta 889, 271–276.CrossRefGoogle ScholarPubMed
Pepperberg, D.R. (1984). Rhodopsin and visual adaptation: Analysis of photoreceptor thresholds in the isolated skate retina. Vision Research 24, 357–366.Google Scholar
Pepperberg, D.R., Brown, P.K., Lurie, M. & Dowling, J.E. (1978). Visual pigment and photoreceptor sensitivity in the isolated skate retina. Journal of General Physiology 71, 369–396.CrossRefGoogle ScholarPubMed
Pepperberg, D.R., Cornwall, M.C., Kahlert, M., Hofmann, K.P., Jin, J., Jones, G.J. & Ripps, H. (1991). Photocurrent recovery and R* lifetime in retinal rods. Biophysical Journal 59, 408a.Google Scholar
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
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
Roof, D.J., Korenbrot, J.I. & Heuser, J.E. (1982). Surfaces of rod photoreceptor disk membranes: Light-activated enzymes. Journal of Cell Biology 95, 501–509.CrossRefGoogle ScholarPubMed
Townes-Anderson, E., MacLeish, P.R. & Raviola, E. (1985). Rod cells dissociated from mature salamander retina: Ultrastructure and uptake of horseradish peroxidase. Journal of Cell Biology 100, 175–188.CrossRefGoogle ScholarPubMed
Vuong, T.M. & Chabre, M. (1990). Subsecond deactivation of transducin by endogenous GTP hydrolysis. Nature 346, 71–74.CrossRefGoogle ScholarPubMed
Vuong, T.M., Chabre, M. & Stryer, L. (1984). Millisecond activation of transducin in the cyclic nucleotide cascade of vision. Nature 311, 659–661.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