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A neural model of foveal light adaptation and afterimage formation1

Published online by Cambridge University Press:  02 June 2009

Hugh R. Wilson
Hugh R. Wilson
Affiliation:
Visual Sciences Center, University of Chicago, Chicago
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Abstract

Psychophysical research has documented the existence of three processes in light adaptation: a fast subtractive process, a divisive process that is fast at light onset and slower at light offset, and a very slow subtractive process (Hayhoe et al., 1987). In the neural model developed here, the fast subtractive process is identified with horizontal cell feedback onto cones and the divisive process with amacrine cell feedback onto bipolar cells. The very slow subtractive process is identified with the modulatory feedback circuit from amacrines via interplexiform cells to horizontal cells. A nonlinear dynamical model is developed incorporating these aspects of retinal circuitry along with both ON- and OFF-center M and P pathways. This model is shown to account for many aspects of foveal light adaptation, including negative afterimage formation, and to explain a number of the physiological differences between M and P ganglion cells, including their differing contrast-response functions.

Keywords

Neural modelLight adaptationAfterimagesM cellP cellFovea
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 3 , May 1997 , pp. 403 - 423
Copyright
Copyright © Cambridge University Press 1997

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References

REFERENCES

Adelson, E.H. (1982). Saturation and adaptation in the rod system. Vision Research 22, 1299–1312.CrossRefGoogle ScholarPubMed
Benardete, E.A., Kaplan, E. & Knight, B.W. (1992). Contrast gain control in the primate retina: P cells are not X-like, some M cells are. Visual Neuroscience 8, 483–486.CrossRefGoogle ScholarPubMed
Bodis-Wollner, I. (1990). The visual system in Parkinson's disease. In Vision and the Brain, ed. Cohen, B. & Bodis-Wollner, I., pp. 297–316. New York: Raven Press.Google Scholar
Burbeck, C.A. & Kelly, D.H. (1984). Role of local adaptation in the fading of stabilized images. Journal of the Optical Society of America A 1, 216–220.CrossRefGoogle ScholarPubMed
Burbeck, C.A. (1986). Negative afterimages and photopic luminance adaptation in human vision. Journal of the Optical Society of America A 3, 1159–1165.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. (1993). Synaptic feedback, depolarization, and color opponency in cone photoreceptors. Visual Neuroscience 10, 981–989.CrossRefGoogle ScholarPubMed
Campbell, F.W. & Gubisch, R.W. (1966). Optical quality of the human eye. Journal of Physiology 186, 558–578.CrossRefGoogle ScholarPubMed
Chen, B., Makous, W. & Williams, D.R. (1993). Serial spatial filters in vision. Vision Research 33, 413–427.CrossRefGoogle ScholarPubMed
Corwin, T.J., Volpe, L.C. & Tyler, C.W. (1976). Images and afterimages of sinusoidal gratings. Vision Research 16, 345–349.CrossRefGoogle ScholarPubMed
Crawford, B.H. (1947). Visual adaptation in relation to brief conditioning stimuli. Proceedings of the Royal Society B 134, 283–302.Google ScholarPubMed
Croner, L.J. & Kaplan, E. (1995). Receptive fields of P and M ganglion cells across the primate retina. Vision Research 35, 7–24.CrossRefGoogle Scholar
Curcio, C.A., Sloan, K.R., Packer, O., Hendrickson, A.E. & Kalina, R.E. (1987). Distribution of cones in human and monkey retina: Individual variability and radial asymmetry. Science 236, 579–582.CrossRefGoogle ScholarPubMed
Dacey, D.M. (1994). Physiology, morphology and spatial densities of identified ganglion cell types in primate retina. In Higher Order Processing in the Visual System, ed. Goode, J., pp. 12–28. New York: CIBA Foundation, John Wiley.Google Scholar
Dacey, D.M., Lee, B.B., Stafford, D.K., Pokorny, J. & Smith, V.C. (1996). Horizontal cells of the primate retina: Cone specifīcity without spectral opponency. Science 271, 656–659.CrossRefGoogle ScholarPubMed
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology 357, 219–240.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Massachusetts: Harvard University Press.Google Scholar
Dowling, J.E. (1991). Retinal neuromodulation: The role of dopamine. Visual Neuroscience 7, 87–97.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
Gaudiano, P. (1994). Simulations of X and Y retinal ganglion cell behavior with a nonlinear push-pull model of spatiotemporal retinal processing. Vision Research 34, 1767–1784.CrossRefGoogle ScholarPubMed
Geisler, W.S. (1978). Adaptation, afterimages and cone saturation. Vision Research 18, 279–289.CrossRefGoogle ScholarPubMed
Graham, N. & Hood, D.C. (1992). Modeling the dynamics of light adaptation: The merging of two traditions. Vision Research 32, 1373–1393.CrossRefGoogle ScholarPubMed
Hayhoe, M.M., Benimoff, N.I. & Hood, D.C. (1987). The time course of multiplicative and subtractive adaptation processes. Vision Research 27, 1981–1996.CrossRefGoogle Scholar
Hayhoe, M.M. (1990). Spatial interactions and models of adaptation. Vision Research 30, 957–965.CrossRefGoogle ScholarPubMed
Hayhoe, M.M., Levin, M.E. & Koshel, R.J. (1992). Subtractive processes in light adaptation. Vision Research 32, 323–333.CrossRefGoogle ScholarPubMed
Hecht, S. & Verrijp, C.D. (1933). Intermittent stimulation by light. III. The relation between intensity and critical fusion frequency for different retinal locations. Journal of General Physiology 17, 251–265.CrossRefGoogle ScholarPubMed
Hood, D.C., Finkelstein, M.A. & Buckingham, E. (1979). Psychophysical tests of models of the response function. Vision Research 19, 401–406.CrossRefGoogle ScholarPubMed
Hood, D.C. & Birch, D.G. (1993). Human cone receptor activity: The leading edge of the a-wave and models of receptor activity. Visual Neuroscience 10, 857–871.CrossRefGoogle Scholar
Kaplan, E. & Shapley, R.M. (1986). The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proceedings of the National Academy of Sciences of the U.S.A. 83, 2755–2757.CrossRefGoogle ScholarPubMed
Kelly, D.H. (1966). Frequency doubling in visual responses. Journal of the Optical Society of America 56, 1628–1633.CrossRefGoogle Scholar
Kelly, D.H. (1971). Theory of flicker and transient Responses I. Uniform fields. Journal of the Optical Society of America 61, 537–546.CrossRefGoogle ScholarPubMed
Kelly, D.H. (1972). Adaptation effects on spatio-temporal sine wave thresholds. Vision Research 12, 89–101.CrossRefGoogle ScholarPubMed
Kelly, D.H. & Wilson, H.R. (1978). Human flicker sensitivity: Two stages of retinal diffusion. Science 202, 896–899.CrossRefGoogle ScholarPubMed
Kelly, D.H. & Martinez-Uriegas, E. (1993). Measurements of chromatic and achromatic afterimages. Journal of the Optical Society of America A 10, 29–37.CrossRefGoogle ScholarPubMed
Kolb, H. (1994). The architecture of functional neural circuits in the vertebrate retina. Investigative Ophthalmology and Visual Science 35, 2385–2404.Google ScholarPubMed
Koonitz, M.A. (1993). GABA immunoreactive profiles provide synaptic input to the soma, axon hillock, and axon initial segment of ganglion cells in primate retina. Vision Research 33, 2629–2636.CrossRefGoogle Scholar
Kremers, J., Lee, B.B., Pokorny, J. & Smith, V.C. (1993). Responses of macaque ganglion cells and human observers to compound periodic waveforms. Vision Research 33, 1997–2011.CrossRefGoogle ScholarPubMed
Lankheet, M.J.M., Van Wezel, R.J.A. & Van De Grind, W.A. (1991). Light adaptation and frequency transfer properties of cat horizontal cells. Vision Research 31, 1129–1142.CrossRefGoogle ScholarPubMed
Lankheet, M.J.M., Prickaerts, J.H. & Van De Grind, W.A. (1992). Responses of cat horizontal cells to sinusoidal gratings. Vision Research 32, 997–1008.CrossRefGoogle ScholarPubMed
Lankheet, M.J.M., Van Wezel, R.J.A., Prickaerts, J.H. & Van De Grind, W.A. (1993). The dynamics of light adaptation in cat horizontal cell responses. Vision Research 33, 1153–1171.CrossRefGoogle ScholarPubMed
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 A 7, 2223–2236.CrossRefGoogle ScholarPubMed
Levi, D.M., Klein, S.A. & Aitsebaomo, A.P. (1985). Vernier acuity, crowding and cortical magnifīcation. Vision Research 25, 963–977.CrossRefGoogle ScholarPubMed
Loomis, J.M. (1978). Complementary afterimages and the unequal adapting effects of steady and flickering light. Journal of the Optical Society of America 68, 411–416.CrossRefGoogle ScholarPubMed
Macleod, D.I.A., Williams, D.R. & Makous, W. (1992). A visual non-linearity fed by single cones. Vision Research 32, 347–363.Google Scholar
Masland, R.H. (1988). Amacrine cells. TINS 9, 405–410.Google Scholar
Mcguire, B.A., Stevens, J.K. & Sterling, P. (1986). Microcircuitry of beta ganglion cells in cat retina. Journal of Neuroscience 6, 907–918.CrossRefGoogle ScholarPubMed
Naka, K.I. & Rushton, W.A. (1966). S-potentials from colour units in the retina of fīsh. Journal of Physiology 185, 584–599.Google ScholarPubMed
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 1183–1195.CrossRefGoogle ScholarPubMed
Ohshima, S., Yagi, T. & Funahashi, Y. (1995). Computational studies on the interaction between red cone and H1 horizontal cell. Vision Research 35, 149–160.CrossRefGoogle ScholarPubMed
Perry, V.H., Oehler, R. & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 1101–1123.CrossRefGoogle Scholar
Pokorny, J. (1968). The effect of target area on grating acuity. Vision Research 8, 543–554.CrossRefGoogle ScholarPubMed
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
Rodieck, R.W. (1989). Starburst amacrine cells of the primate retina. Journal of Comparative Neurology 285, 18–37.CrossRefGoogle ScholarPubMed
Rushton, W.A.H. & Henry, G.H. (1968). Bleaching and regeneration of cone pigments in man. Vision Research 8, 617–631.CrossRefGoogle ScholarPubMed
Schiller, P.H., Sandell, J.H. & Maunsell, J.H.R. (1986). Functions of the ON and OFF channels of the visual system. Nature 322, 824–825.CrossRefGoogle ScholarPubMed
Schiller, P. (1992). The ON and OFF channels of the visual system. Trends in Neurosciences 15, 86–92.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
Shah, S. & Levine, M.D. (1996). Visual information processing in primate cone pathways—Part I: A model. IEEE Transactions on Systems, Man & Cybernetics, B 26, 259–274.CrossRefGoogle Scholar
Shapley, R.B. & Victor, J.D. (1978). The effect of contrast on the transfer properties of cat retinal ganglion cells. Journal of Physiology 285, 275–298.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Victor, J.D. (1981). How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. Journal of Physiology 318, 161–179.CrossRefGoogle ScholarPubMed
Shapley, R. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. Progress in Retinal Research 3, 263–343.CrossRefGoogle Scholar
Shlaer, S. (1937). The relation between visual acuity and illumination. Journal of General Physiology 21, 165–188.CrossRefGoogle ScholarPubMed
Snowden, R.J. & Hammett, S.T. (1992). Subtractive and divisive adaptation in the human visual system. Nature 355, 248–250.CrossRefGoogle ScholarPubMed
Sperling, G. & Sondhi, M.M. (1968). Model for visual luminance discrimination and flicker detection. Journal of the Optical Society of America 58, 1133–1145.CrossRefGoogle ScholarPubMed
Swanson, W.H. & Wilson, H.R. (1985). Eccentricity dependence of contrast matching and oblique masking. Vision Research 25, 1285–1295.CrossRefGoogle ScholarPubMed
Trachina, D., Gordon, J. & Shapley, R.M. (1984). Retinal light adaptation-evidence for a feedback mechanism. Nature 310, 314–316.CrossRefGoogle Scholar
Troy, J.B. & Lee, B.B. (1994). Steady discharges of macaque retinal ganglion cells. Visual Neuroscience 11, 111–118.CrossRefGoogle ScholarPubMed
Tyler, C.W. (1985). Analysis of visual modulation sensitivity. II. Peripheral retina and the role of photoreceptor dimensions. Journal of the Optical Society of America A 2, 393–398.CrossRefGoogle ScholarPubMed
Virsu, V. & Laurinen, P. (1977). Long-lasting afterimages caused by neural adaptation. Vision Research 17, 853–860.CrossRefGoogle ScholarPubMed
Von Wiegand, T.E., Hood, D.C. & Graham, N. (1995). Testing a computational model of light-adaptation dynamics. Vision Research 35, 3037–3051.CrossRefGoogle ScholarPubMed
Wagner, H.-J. & Djamgoz, M.B.A. (1993). Spinules: A case for retinal synaptic plasticity. Trends in Neurosciences 16, 201–206.CrossRefGoogle ScholarPubMed
Walraven, J., Enroth-Cugell, C., Hood, D.C., Macleod, D.I.A. & Schnapf, J.L. (1990). The control of visual sensitivity: Receptoral and postreceptoral processes. In Visual Perception: The Neurophysiological Foundations, ed. Spillmann, L. & Werner, J.S., pp. 53–101. New York: Academic Press.CrossRefGoogle Scholar
Wässle, H., Boycott, B.B. & Röhrenbeck, J. (1989). Horizontal cells in the monkey retina: Cone connections and dendritic network. European Journal of Neuroscience 1, 421–435.CrossRefGoogle ScholarPubMed
Wässle, H., Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447–480.CrossRefGoogle ScholarPubMed
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. Journal of Comparative Neurology 289, 434–454.CrossRefGoogle ScholarPubMed
Westheimer, G. (1967). Spatial interaction in human cone vision. Journal of Physiology 190, 139–154.CrossRefGoogle ScholarPubMed
Williams, D.R. (1988). Topography of the foveal cone mosaic in the living human eye. Vision Research 28, 433–454.CrossRefGoogle ScholarPubMed
Williams, D.R., Brainard, D.H., Mcmahon, M.J. & Navarro, R. (1994). Double-pass and interferometric measures of the optical quality of the eye. Journal of the Optical Society of America A 11, 3123–3135.CrossRefGoogle ScholarPubMed
Wilson, H.R. & Humanski, R. (1993). Spatial frequency adaptation and contrast gain control. Vision Research 33, 1133–1149.CrossRefGoogle ScholarPubMed
Witkovsky, P. & Schütte, M. (1991). The organization of dopaminergic neurons in vertebrate retinas. Visual Neuroscience 7, 113–124.CrossRefGoogle ScholarPubMed
Yang, X.-L. & Wu, S.M. (1989). Effects of background illumination on the horizontal cell responses in the tiger salamander retina. Journal of Neuroscience 9, 815–827.CrossRefGoogle ScholarPubMed