Spatial scale and cellular substrate of contrast adaptation by retinal ganglion cells

Human visual perception and many visual system neurons adapt to the luminance and contrast of the stimulus. Here we describe a form of contrast adaptation that occurs in the retina. This adaptation had a local scale smaller than the dendritic or receptive fields of single ganglion cells and was insensitive to pharmacological manipulation of amacrine cell function. These results implicate the bipolar cell pathway as a site of contrast adaptation. The time required for contrast adaptation varied with stimulus size, ranging from approximately 100 ms for the smallest stimuli, to seconds for stimuli the size of the receptive field. The differing scales and time courses of these effects suggest that multiple types of contrast adaptation are used in viewing natural scenes.

[1]  W. Levick Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit's retina , 1967, The Journal of physiology.

[2]  P Kuyper,et al.  Triggered correlation. , 1968, IEEE transactions on bio-medical engineering.

[3]  R. Shapley,et al.  The effect of contrast on the transfer properties of cat retinal ganglion cells. , 1978, The Journal of physiology.

[4]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[5]  R. Shapley,et al.  Nonlinear spatial summation and the contrast gain control of cat retinal ganglion cells. , 1979, The Journal of physiology.

[6]  C. Enroth-Cugell,et al.  Suppression of cat retinal ganglion cell responses by moving patterns. , 1980, The Journal of physiology.

[7]  R. Shapley,et al.  The effect of contrast on the non‐linear response of the Y cell. , 1980, The Journal of physiology.

[8]  J D Victor,et al.  How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. , 1981, The Journal of physiology.

[9]  C. Enroth-Cugell,et al.  Chapter 9 Visual adaptation and retinal gain controls , 1984 .

[10]  D. G. Albrecht,et al.  Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. , 1984, The Journal of physiology.

[11]  M. Lings,et al.  Articles , 1967, Soil Science Society of America Journal.

[12]  I. Ohzawa,et al.  Contrast gain control in the cat's visual system. , 1985, Journal of neurophysiology.

[13]  L. Peichl,et al.  Morphology of rabbit retinal ganglion cells projecting to the medial terminal nucleus of the accessory optic system , 1986, The Journal of comparative neurology.

[14]  B. Boycott,et al.  Alpha ganglion cells in the rabbit retina , 1987, The Journal of comparative neurology.

[15]  B. Cleland,et al.  Visual adaptation is highly localized in the cat's retina. , 1988, The Journal of physiology.

[16]  J. Dowling,et al.  Bipolar cells in the turtle retina are strongly immunoreactive for glutamate. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[17]  S. K. Park,et al.  Random number generators: good ones are hard to find , 1988, CACM.

[18]  F. Amthor,et al.  Morphologies of rabbit retinal ganglion cells with complex receptive fields , 1989, The Journal of comparative neurology.

[19]  F. Amthor,et al.  Morphologies of rabbit retinal ganglion cells with concentric receptive fields , 1989, The Journal of comparative neurology.

[20]  D. I. Vaney,et al.  Chapter 2 The mosaic of amacrine cells in the mammalian retina , 1990 .

[21]  Paul Witkovsky,et al.  Chapter 10 Functional roles of dopamine in the vertebrate retina , 1991 .

[22]  B. Knight,et al.  Contrast gain control in the primate retina: P cells are not X-like, some M cells are , 1992, Visual Neuroscience.

[23]  S. Massey,et al.  Morphology of bipolar cells labeled by DAPI in the rabbit retina , 1992, The Journal of comparative neurology.

[24]  A. Hendrickson,et al.  Immunocytochemical localization of GABA and glycine in amacrine and displaced amacrine cells of macaque monkey retina , 1993, Vision Research.

[25]  R H Masland,et al.  Receptive fields and dendritic structure of directionally selective retinal ganglion cells , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  S. Massey,et al.  Distribution and coverage of A- and B-type horizontal cells stained with Neurobiotin in the rabbit retina , 1994, Visual Neuroscience.

[27]  G. Fain,et al.  Neurotransmitter receptors of starburst amacrine cells in rabbit retinal slices , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  H. Wässle,et al.  Receptive Field Properties of Starburst Cholinergic Amacrine Cells in the Rabbit Retina , 1995, The European journal of neuroscience.

[29]  W. Taylor Response properties of long-range axon-bearing amacrine cells in the dark-adapted rabbit retina , 1996, Visual Neuroscience.

[30]  S. Massey,et al.  A calbindin‐immunoreactive cone bipolar cell type in the rabbit retina , 1996, The Journal of comparative neurology.

[31]  R. Masland,et al.  Responses to light of starburst amacrine cells. , 1996, Journal of neurophysiology.

[32]  R. Marc,et al.  Amino Acid Signatures in the Primate Retina , 1996, The Journal of Neuroscience.

[33]  D. Pow,et al.  Analysis of the distribution of glycine and GABA in amacrine cells of the developing rabbit retina: A comparison with the ontogeny of a functional GABA transport system in retinal neurons , 1997, Visual Neuroscience.

[34]  D. Baylor,et al.  Mosaic arrangement of ganglion cell receptive fields in rabbit retina. , 1997, Journal of neurophysiology.

[35]  Michael J. Berry,et al.  Adaptation of retinal processing to image contrast and spatial scale , 1997, Nature.

[36]  D. Dacey,et al.  Physiology of the A1 amacrine: A spiking, axon-bearing interneuron of the macaque monkey retina , 1997, Visual Neuroscience.

[37]  Richard H. Masland,et al.  Retinal direction selectivity after targeted laser ablation of starburst amacrine cells , 1997, Nature.

[38]  R. Shapley,et al.  The use of m-sequences in the analysis of visual neurons: Linear receptive field properties , 1997, Visual Neuroscience.

[39]  S. Massey,et al.  Contributions of GABAA receptors and GABAC receptors to acetylcholine release and directional selectivity in the rabbit retina , 1997, Visual Neuroscience.

[40]  R. Shapley Retinal physiology: Adapting to the changing scene , 1997, Current Biology.

[41]  R. Wong,et al.  GABAC receptors on ferret retinal bipolar cells: A diversity of subtypes in mammals? , 1997, Visual Neuroscience.

[42]  R. Normann,et al.  Light adaptation and sensitivity controlling mechanisms in vertebrate photoreceptors , 1998, Progress in Retinal and Eye Research.

[43]  R. Masland,et al.  ON direction-selective ganglion cells in the rabbit retina: Dendritic morphology and pattern of fasciculation , 1998, Visual Neuroscience.

[44]  Richard H Masland,et al.  Extreme Diversity among Amacrine Cells: Implications for Function , 1998, Neuron.

[45]  W R Taylor,et al.  TTX attenuates surround inhibition in rabbit retinal ganglion cells , 1999, Visual Neuroscience.

[46]  R H Masland,et al.  Costratification of a population of bipolar cells with the direction‐selective circuitry of the rabbit retina , 1999, The Journal of comparative neurology.

[47]  R. Masland,et al.  The shapes and numbers of amacrine cells: Matching of photofilled with Golgi‐stained cells in the rabbit retina and comparison with other mammalian species , 1999, The Journal of comparative neurology.

[48]  Richard H. Masland,et al.  Receptive Field Microstructure and Dendritic Geometry of Retinal Ganglion Cells , 2000, Neuron.

[49]  Maria V. Sanchez-Vives,et al.  Membrane Mechanisms Underlying Contrast Adaptation in Cat Area 17In Vivo , 2000, The Journal of Neuroscience.