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Human cone receptor activity: The leading edge of the a–wave and models of receptor activity

Published online by Cambridge University Press:  02 June 2009

Donald C. Hood  and
David G. Birch
Donald C. Hood
Affiliation:
Department of Psychology, Columbia University, New York
David G. Birch
Affiliation:
Retina Foundation of the Southwest, Dallas
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Abstract

The leading edge of the a–wave of the electroretinogram (ERG) was evaluated as a measure of human cone photoreceptor activity. The amplitude of the cone a–wave elicited by flashes of different energy was compared to the predictions of a class of models from in vitro studies of cone photoreceptors. These models successfully describe the leading edge of the a–wave. Thus, the human cone a–wave can be used to test hypotheses about normal and abnormal cone receptors. The ability of the human cone to adjust its sensitivity in the presence of steady adapting lights was assessed by recording cone a–waves to flashes on adapting fields up to 3.9 log td in intensity and by comparing these responses to quantitative models of adaptation. The first 10 ms of the cone's response is little affected by field intensities up to 2.9 log td. The 3.9 log td field reduced the response to weak flashes by about a factor of 2.5 (0.4 log unit). This relatively small reduction in sensitivity can be attributed to a combination of response compression, pigment bleaching, and an adaptation mechanism that changes the gain without changing the time course. We conclude that either the human cones show relatively little adaptation or that they have an adaptation mechanism that involves a time-course change. That is, as we are limited with the a–wave to the first 10 ms or so of the cone's response, we cannot rule out a gain mechanism linked to a time-course change.

Keywords

ConeReceptorAdaptationElectroretinogramHuman
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 5 , September 1993 , pp. 857 - 871
Copyright
Copyright © Cambridge University Press 1993

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References

Abraham, F.A., Alpern, M. & Kirk, D.B. (1985). Electroretinograms evoked by sinusoidal excitation of human cones. Journal of Physiology 363, 135–150.CrossRefGoogle ScholarPubMed
Adelson, E.H. (1982). Saturation and adaptation in the rod system. Vision Research 22, 1299–1312.CrossRefGoogle ScholarPubMed
Baron, W.S. & Boyton, R.M. (1975). Response of primate cones to sinusoidally flickering homochromatic stimuli. Journal of Physiology 246, 311–331.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Hodgkin, A.L. (1974). Changes in the time scale and sensitivity in turtle photoreceptors. Journal of Physiology 242, 729–758.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, 685–727.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. & Yau, K.W. (1983). Two components of electrical dark noise in toad retinal rod outer segments. Journal of Physiology 309, 591–621.CrossRefGoogle Scholar
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1984). The photocurrent, noise, and spectral sensitivity of rods of the monkey, Macacafas-cicularis. Journal of Physiology 357, 575–607.CrossRefGoogle Scholar
Birch, D.G. & Fish, G.E. (1987). Rod ERGs in retinitis pigmentosa and cone-rod degeneration. Investigative Ophthalmology and Visual Science 28, 140–150.Google ScholarPubMed
Boynton, R.M. & Whitten, D.N. (1970). Visual adaptation in monkey cones: Recordings of late receptor potentials. Science 170, 1423–1426.CrossRefGoogle ScholarPubMed
Breton, M.E. & Montzka, D. (1992). Empirical limits of rod photocurrent component response in the electroretinogram. Documenta Ophthalmologica 79, 337–361.CrossRefGoogle ScholarPubMed
Breton, M.E. & Schueller, A.W. (1992). Analysis of a–wave maximum velocity in terms of cGMP cascade. Investigative Ophthalmology and Visual Science 33, 1407.Google Scholar
Breton, M.E., Pugh, E.N. & Schueller, A.W. (1992). Intensity dependence of cGMP models applied to a–wave leading edge. Noninvasive Assessment of the Visual System Technical Digest 1992(OSA) 1, 128–131.Google Scholar
Brown, K.T. (1968). The electroretinogram: Its components and their origin. Vision Research 8, 633–678.CrossRefGoogle Scholar
Burns, S.A., Elsner, A.E. & Kreitz, B.S. (1992). Analysis of nonlinearities in the flicker ERG. Optometry and Visual Science 69, 95–105.CrossRefGoogle ScholarPubMed
Burns, S.A., Elsner, A.E., Lobes, L.A. & DOFT, B.H. (1987). A psychophysical technique for measuring cone photopigment bleaching. Investigative Ophthalmology and Visual Science 28, 712–717.Google ScholarPubMed
Burr, D.C., Ross, J. & Morrone, M.C. (1985). Local regulation of luminance gain. Vision Research 25, 717–727.CrossRefGoogle ScholarPubMed
Bush, R.A. & Sieving, P.A. (1992). Do photoreceptors alone contribute to the primate photopic ERG a–wave? Investigative Ophthalmology and Visual Science (Suppl.) 33, 836.Google Scholar
Cicerone, C.M., Hayhoe, M.M. & MacLeod, D.I.A. (1990). The spread of adaptation in human foveal and parafoveal cone vision. Vision Research 30, 1603–1615.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
Coevorden, R.E., Breton, M.E. & Quinn, G.E. (1992). Changes in ERG a–wave maximum velocity in the developing infant eye. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1409.Google Scholar
Donner, K., Hemila, S. & Koskelainen, A. (1988). Temperature dependence of rod photoresponses from the aspartate-treated retina of the frog (Rana temporaria). Acta Physiologica Scandinavica 134, 535–541.CrossRefGoogle ScholarPubMed
Finkelstein, M.A. & Hood, D.C. (1981). Cone system saturation: More than one stage of sensitivity loss. Vision Research 21, 319–328.CrossRefGoogle ScholarPubMed
Finkelstein, M.A., Harrison, M. & Hood, D.C. (1990). Sites of sensitivity control within a long–wavelength cone pathway. Vision Research 30, 1145–1158.CrossRefGoogle ScholarPubMed
Fourtes, M.G.F. & Hodgkin, A.L. (1964). Changes in time scale and sensitivity in the ommatidia of Limulus. Journal of Physiology (London) 172, 239–263.CrossRefGoogle Scholar
Geisler, W.S. (1978). Adaptation, afterimages, and cone saturation. Vision Research 18, 279–289.CrossRefGoogle ScholarPubMed
Geisler, W.S. (1979). Initial image and afterimage discrimination in the human rod and cone systems. Journal of Physiology 294, 165–179.CrossRefGoogle ScholarPubMed
Graham, N. & Hood, D.C. (1992 a). Quantal noise and decision rules in dynamic models of light adaptation. Vision Research 32, 779–787.CrossRefGoogle ScholarPubMed
Graham, N. & Hood, D.C. (1992 b). Models of adaptation: The merging of two traditions. Vision Research 32, 1373–1393.CrossRefGoogle ScholarPubMed
Granit, R. (1933). Components of the retinal action potential in mammals and their relations to the discharge in the optic nerve. Journal of Physiology 77, 207–238.CrossRefGoogle Scholar
Granit, R. (1947). Sensory Mechanism of the Retina. London: Oxford University Press.Google Scholar
Hayhoe, M.M., Benimoff, N.I. & Hood, D.C. (1987). The time course of multiplicative and subtractive adaptation process. Vision Research 27, 1981–1996.CrossRefGoogle ScholarPubMed
Heynen, H.G.M. & Van Norren, D. (1985). Origin of the electroretinogram in the intact macaque eye — I. Principle component analysis. Vision Research 25, 697–707.CrossRefGoogle Scholar
Hood, D.C. (1978). Psychophysical and electrophysiological tests of physiological proposals of light adaptation. In Visual Psychophysics: Its Physiological Basis, ed. Armington, J., Krauskopf, J. & Wooten, B., pp. 141–155. New York: Academic Press.CrossRefGoogle Scholar
Hood, D.C. & Birch, D.G. (1990 a). The a–wave of the human ERG and rod receptor function. Investigative Ophthalmology and Visual Science 31, 2070–2081.Google ScholarPubMed
Hood, D.C. & Birch, D.G. (1990 b). Light adaptation of human rod receptors. Investigative Ophthalmology and Visual Science (Suppl.) 31, 493.Google Scholar
Hood, D.C. & Birch, D.G. (1990 c). A quantitative measure of the electrical activity of human rod photoreceptors using electroretinography. Visual Neuroscience 5, 379–387.CrossRefGoogle ScholarPubMed
Hood, D.C. & Birch, D.G. (1991 a). Light adaptation of human photoreceptors. Society of Neuroscience Abstracts 3, 6.Google Scholar
Hood, D.C. & Birch, D.G. (1991 b). Models of human rod receptors and the ERG. In Computational Models of Visual Processing, ed. Movshon, M.L.A., pp. 57–67. Cambridge, Massachusetts: MIT Press.Google Scholar
Hood, D.C. & Birch, D.G. (1992 a). A computational model of implicit times and amplitudes of the human rod ERG b–wave. Visual Neuroscience 8, 107–126.CrossRefGoogle Scholar
Hood, D.C. & Birch, D.G. (1992 b). The time course of the response of human photoreceptors. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1407.Google Scholar
Hood, D.C. & Birch, D.G. (1993). Light adaptation of human rod receptors: The leading edge of the human a–wave and models of rod receptor activity. Vision Research (in press).CrossRefGoogle Scholar
Hood, D.C., Birch, D.G. & Birch, E.E. (1993). The use of models to improve hypothesis delineation: A study of the infant ERG. In Infant Vision: Basic and Clinical Research, ed. Simons, K., (in press). New York: Oxford University Press.Google Scholar
Hood, D.C. & Finkelstein, M.A. (1979). Comparison of changes in sensitivity and sensation: Implications for the response-intensity function of the human photopic system. Journal of Experimental Psychology: Human Perception and Performance 5, 391–405.Google ScholarPubMed
Hood, D.C. & Finkelstein, M.A. (1983). A case for the revision of textbook models of color vision: The detection and appearance of small brief lights. In Colour Vision: Physiology and Psychophysics, ed. Mollon, J.D. & Sharpe, L.T., pp. 385–398. London: Academic Press.Google Scholar
Hood, D.C. & Finkelstein, M.A. (1986). Sensitivity to light. In Handbook of Perception and Human Performance, ed. Boff, K., Kaufman, L. & Thomas, J., pp. 5.1–5.66. New York: Wiley.Google Scholar
Hood, D.C., Finkelstein, M.A. & Buckingham, E. (1979). Psycho-physical tests of models of the response-intensity function. Vision Research 19, 401–406.CrossRefGoogle Scholar
Hood, D.C. & Grover, B.G. (1974). Temporal summation of light energy by a vertebrate visual receptor. Vision Research 184, 1003–1005.Google ScholarPubMed
Hood, D.C. & Hock, P.A. (1975). Light adaptation of the receptors: Increment threshold functions for the frog's rods and cones. Vision Research 15, 545–553.CrossRefGoogle ScholarPubMed
Lamb, T. D. (1984). Effects of temperature changes on toad rod photo-currents. Journal of Physiology 346, 557–578.CrossRefGoogle Scholar
Lamb, T.D., McNaughton, P.A. & Yau, K.-W. (1981). Spatial spread of activation and background desensitization in toad outer segments. Journal of Physiology 319, 463–496.CrossRefGoogle ScholarPubMed
Lamb, T.D. & Pugh, E.N. (1992). A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. Journal of Physiology 499, 719–758.CrossRefGoogle Scholar
Lee, B.B., Pokorny, J., Smith, V.C., Martin, P.R. & Valberg, A. (1990). Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers. Journal of the Optical Society of America 7, 2223–2236.CrossRefGoogle ScholarPubMed
MacLeod, D.I.A., Chen, B. & Crognale, M. (1989). Spatial organization of sensitivity regulation in rod vision. Vision Research 29, 965–978.CrossRefGoogle ScholarPubMed
MacLeod, D.I.A., Williams, D.R. & Makous, W. (1992). Visual non-linearity fed by single cones. Vision Research 32, 347–363.CrossRefGoogle Scholar
Makous, W. (1990). Partitioning visual processes. In Advances In Photoreception, pp. 78–102. Washington, DC: National Academy Press.Google Scholar
Penn, R.D. & Hagins, W.A. (1972). Kinetics of the photocurrent of retinal rods. Biophysical Journal 12, 1073–1094.CrossRefGoogle ScholarPubMed
Pokorny, J. & Smith, V.C. (1976). Effect of field size on red-green color mixture equations. Journal of the Optical Society of America 66, 705–708.CrossRefGoogle ScholarPubMed
Pugh, E.N. (1988). Vision: Physics and Retinal Physiology. New York: John Wiley & Sons, pp. 75–163.Google Scholar
Purpura, K., Tranchina, D., Kaplan, E. & Shapley, R.M. (1990). Light adaptation in the primate retina: Analysis of changes in gain and dynamics of monkey retinal ganglion cells. Visual Neuroscience 4, 75–93.CrossRefGoogle ScholarPubMed
Rushton, W.A.H. (1965). Visual adaptation. The Ferrier lecture. Proceedings of the Royal Society B 162, 20–46.Google Scholar
Rushton, W.A.H. & Henry, G.H. (1968). Bleaching and regeneration of cone pigments in man. Vision Research 8, 617–631.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, 681–713.CrossRefGoogle ScholarPubMed
Seiple, W., Holopigian, K., Greenstein, V. & Hood, D. (1992). Adaptation at the level of the human cone photoreceptors. Vision Research 32, 2043–2048.CrossRefGoogle Scholar
Shapley, R. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. Progress in Retinal Research 3, 263–346.CrossRefGoogle Scholar
Sneyd, J. & Tranchina, D. (1989). Phototransduction in cones: An inverse problem in enzyme kinetics. Bulletin of Mathematical Biology 51, 749–784.CrossRefGoogle ScholarPubMed
Tamura, T., Nakatani, K. & Yau, K.-W. (1989). Light adaptation in cat retinal rods. Science 245, 755–757.CrossRefGoogle ScholarPubMed
Teller, D.Y. (1989). Visual science as a scientific domain. In Visual Perception: The Neurophysiological Foundations, ed. Spillman, L. & Werner, J.S., pp. 11–21. San Diego, California: Academic Press, Inc.Google Scholar
Valeton, J.M. & van Norren, D. (1983). Light adaptation of primate cones: An analysis based on extracellular data. Vision Research 23, 1539–1547.CrossRefGoogle ScholarPubMed
Walraven, J., Enroth-Cugell, C., Hood, D.C, MacLeod, D.I.A & Schnapf, J. (1989). The control of visual sensitivity: Receptoral and postreceptoral processes. In Visual Perception: The Neurophysiological Foundations, ed. Spillman, L. & Werner, J., pp. 53–101, Chap. 5. San Diego, California: Academic Press, Inc.Google Scholar
Williams, D.R. (1985). Visibility of interference fringes near the resolution limit. Journal of the Optical Society of America 42, 1087–1093.CrossRefGoogle Scholar