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Phototransduction and adaptation in rods, single cones, and twin cones of the striped bass retina: A comparative study

Published online by Cambridge University Press:  02 June 2009

James L. Miller
Affiliation:
Department of Physiology, School of Medicine, University of California at San Francisco, San Francisco
Juan I. Korenbrot
Affiliation:
Department of Physiology, School of Medicine, University of California at San Francisco, San Francisco

Abstract

We investigated the attributes of transduction and light-adaptation in rods, single cones, and twin cones isolated from the retina of striped bass (Morone saxatilis). Outer-segment membrane currents were measured with suction electrodes under voltage clamp provided by tight-seal electrodes applied to the cell’s inner segment. Brief flashes of light transiently reduced the outer-segment current with kinetics and sensitivity characteristic of each receptor type. In all cells, the responses to dim lights increased linearly with light intensity. The amplitude-intensity relation for rods and single cones were well described by an exponential saturation function, while for twin cones it was best described by a Michaelis-Menten function. At the wavelength of maximum absorbance, the average intensity necessary to half-saturate the peak photocurrent in dark-adapted rods was 28 photons/μm2 and in single cones it was 238 photons/μm2. Among twin cones, the common type (88% of all twins recorded) half-saturated at an average of 1454 photons/μm2, while the fast type reached half-saturation at an average of 9402 photons/μm2. The action spectrum of the photocurrent in the three receptor types was well fit by a nomogram that describes the absorption spectrum of a vitamin A2-based photopigment. The wavelength of maximum absorbance for rods was 528 nm, for single cones it was 542 nm and for twin cones it was 605 nm. Both members of the twin pair contained the same photopigment and they were electrically coupled. Under voltage clamp, the response to dim flashes of light in both single and twin cones was biphasic. The initial peak was followed by a smaller amplitude undershoot. Single cones reached peak in 86 ms and common twins in 50 ms. Background light desensitized the flash sensitivity in all photoreceptor types, but was most effective in rods and least effective in fast twins. In the steady state, the desensitizing effect of a background intensity, Ib, at the respective optimum wavelength for each cell was well described by the Weber-Fechner law (1/(1 + Ib/Ibo)), where Ibo was, on average (in units of photons/μm2/s), 1.45 for rods, 1.81 x 103 for single cones, 4.56 x 103 for common twins, and 6.79 x 104 for fast twins.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1993

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References

Ali, M.A. & Anctil, M. (1976). Retinas of Fishes: An Atlas. Berlin-New York: Springer Verlag.CrossRefGoogle Scholar
Attwell, D., Werblin, F.S. & Wilson, M. (1982). The properties of single cones isolated from the tiger salamander retina. Journal of Physiology 328, 259283.CrossRefGoogle ScholarPubMed
Barnes, S. & Hille, B. (1989). Ionic channels of the inner segment of tiger salamander cone photoreceptors. Journal of General Physiology 94, 719744.CrossRefGoogle ScholarPubMed
Baylor, D.A. (1987). Photoreceptor signals and vision. Investigative Ophthalmology and Visual Science 28, 3449.Google ScholarPubMed
Baylor, D.A. & Fuortes, M.G.F. (1970). Electrical responses of single cones in the retina of the turtle. Journal of Physiology 207, 7792.CrossRefGoogle ScholarPubMed
Baylor, D.A., Hodgkin, A.L. & Lamb, T.D. (1974). The electrical response of turtle cones to flashes and steps of light. Journal of Physiology 242, 685727.CrossRefGoogle ScholarPubMed
Baylor, D.A., Lamb, T.D. & Yau, K.-W. (1979). The membrane current of single rod outer segments. Journal of Physiology 288, 589611.Google Scholar
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, 115145.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, 575607.CrossRefGoogle ScholarPubMed
Boehlert, G.W. (1978). Intraspecific evidence for the function of single and double cones in the teleost retina. Science 202, 309311.CrossRefGoogle ScholarPubMed
Bowmaker, J.K. & Kunz, Y.W. (1987). Ultraviolet receptors, tetrachromatic color vision and retinal mosaics in the brown trout (Salmo trutta): Age-dependent changes. Vision Research 27, 21012108.Google Scholar
Burkhardt, D.A., Hassin, G., Levine, J.S. & MacNichol, E.F. Jr, (1980). Electrical responses and photopigments of twin cones in the retina of the walleye. Journal of Physiology 309, 215228.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Kraft, T.W. & Gottesman, J. (1986). Functional properties of twin and single cones. Neuroscience Research 4, S45–S58.CrossRefGoogle ScholarPubMed
Cherr, G.N. & Cross, N.L. (1987). Immobilization of mammalian eggs on solid substrates by lectins for electron microscopy. Journal of Microscopy 145, 341345.Google ScholarPubMed
Cohen, A.I. (1972). Rods and Cones. Handbook of Sensory Physiology, Vol. 7, Berlin-New York: Springer-Verlag.Google Scholar
Dawis, S.M. (1981). Polynomial expressions of pigment nomograms. Vision Research 21, 14271430.CrossRefGoogle ScholarPubMed
Hagins, W.A., Penn, R.D. & Yoshikami, S. (1970). Dark current and photocurrent in retinal rods. Biophysical Journal 10, 380412.CrossRefGoogle ScholarPubMed
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F.J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pfluger Archives 391, 85100.CrossRefGoogle ScholarPubMed
Hestrin, S. & Korenbrot, J.I. (1990). Activation kinetics of retinal cones and rods: Response to intense flashes of light. Journal of Neuroscience 10, 19671973.CrossRefGoogle ScholarPubMed
Hochstrate, P. & Ruppel, H. (1980). On the evaluation of photoreceptor properties by microfluorometric measurements of fluorochrome diffusion. Biophysics of Structure and Mechanism 6, 125.CrossRefGoogle Scholar
Kaneko, A. & Tachibana, M. (1985). Electrophysiological measurements of the spectral sensitivity of three types of cones in the carp retina. Japanese Journal of Physiology 35, 355365.Google Scholar
Kraft, T.W. (1988). Photocurrents of cone photoreceptors of the golden-mantled ground squirrel. Journal of Physiology 404, 199213.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, 463486.CrossRefGoogle ScholarPubMed
Levine, J.S., MacNichol, E.F. Jr, Kraft, T.W. & Collins, B.A. (1979). lntraretinal distribution of cone pigments in certain teleost. Science 204, 523526.Google Scholar
Loew, E.R. & Lythgoe, J.N. (1978). The ecology of cone pigments in teleost fish. Vision Research 18, 715722.CrossRefGoogle Scholar
Lyall, A.H. (1957). The growth of the trout retina. Quarterly Journal Microscopical Science 98, 101110.Google Scholar
MaRchiafava, P.L., Strettoi, E. & Alpigiani, V. (1985). Intracellular recording from single and double cone cells isolated from the fish retina (Tinca tinca) Experimental Biology 44, 173180.Google ScholarPubMed
Maricq, A.V. & Korenbrot, J.I. (1988). Calcium and calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors. Neuron 1, 503515.CrossRefGoogle ScholarPubMed
Maricq, A.V. & Korenbrot, J.I. (1990). Potassium currents in the inner segment of single retinal cone photoreceptors. Journal of Neurophysiology 64, 19291940.CrossRefGoogle ScholarPubMed
McNaughton, P.A. (1990). Light response of vertebrate photoreceptors. Physiological Reviews 70, 847883.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 cytoplasmic Ca concentration. Journal of General Physiology 90, 397426.CrossRefGoogle ScholarPubMed
Miller, J.L. & Korenbrot, J.I. (1992). In intact retinal cones membrane depolarization activates the cGMP-dependent current in the dark: Evidence for Ca control of guanylate cyclase and phosphodiesterase Journal of General Physiology (in press).Google Scholar
Penn, R.D. & Hagins, W.A. (1972). Kinetics of the photocurrent of retinal rods. Biophysical Journal 12, 10731094.CrossRefGoogle ScholarPubMed
Perry, R.J. & McNaughton, P.A. (1991). Response properties of cones from the retina of the tiger salamander. Journal of Physiology 433, 561587.CrossRefGoogle ScholarPubMed
Picones, A. & Korenbrot, J.I. (1992). Permeation and interaction of monovalent cations with the cGMP-gated channel of cone photoreceptors. Journal of General Physiology 100, 647673.CrossRefGoogle ScholarPubMed
Pugh, E.N. Jr, & Cobbs, W.H. (1986). Visual transduction in vertebrate rods and cones: A tale of two transmitters, calcium and cyclic GMP. Vision Research 26, 16131643.Google Scholar
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, 19231948.Google Scholar
Rodieck, R.W. (1973). The Vertebrate Retina. San Francisco, California: W.H. Freeman.Google Scholar
Schnapf, J.L. & McBurney, R.N. (1980). Light-induced changes in membrane current in cone outer segments of tiger salamander and turtle. Nature 287, 239241.CrossRefGoogle ScholarPubMed
Schnapf, J.L., Nunn, B.J., Meister, M. & Baylor, D.A. (1990). Visual transduction in cones of the monkey Macaca fascicularis Journal of Physiology 427, 681713.Google Scholar
Tomita, T. (1970). Electrical activity of vertebrate photoreceptors. Quarterly Review of Biophysics 3, 179.CrossRefGoogle ScholarPubMed
Walls, G.L. (1942). The Vertebrate Eye and Its Adaptive Radiation. Bloomfield Hills, Michigan: Cranbrook Institute of Science.Google Scholar