Adaptable Mechanisms That Regulate the Contrast Response of Neurons in the Primate Lateral Geniculate Nucleus

The response of the classical receptive field of visual neurons can be suppressed by stimuli that, when presented alone, cause no change in the discharge rate. This suppression reveals the presence of an extraclassical receptive field (ECRF). In recordings from the lateral geniculate nucleus (LGN) of a New World primate, the marmoset, we characterize the mechanisms that contribute to the ECRF by measuring their spatiotemporal tuning during prolonged exposure to a high-contrast grating (contrast adaptation). The ECRF was strongest in magnocellular cells, where contrast adaptation reduced suppression from the ECRF: adaptation of the ECRF transferred across spatial frequency, temporal frequency, and orientation, but not across space. This implies that the ECRF of LGN cells comprises multiple adaptable mechanisms, each broadly tuned but spatially localized, and consistent with a retinal origin. Signals from the ECRF saturated at high contrasts, and so adaptation of one part of the ECRF brought into its operating range signals from other parts of the visual field. Although the ECRF is adaptable, its major impact during contrast adaptation to a spatially extended pattern was to reduce visual response and hence reduce a neuron's susceptibility to contrast adaptation; in normal viewing, a major role of the ECRF might be to protect visual sensitivity in scenes dominated by high contrast.

[1]  J. Movshon,et al.  Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex , 1997, The Journal of Neuroscience.

[2]  P. C. Murphy,et al.  Spatial summation in lateral geniculate nucleus and visual cortex , 2000, Experimental Brain Research.

[3]  J. Movshon,et al.  Pattern adaptation and cross-orientation interactions in the primary visual cortex , 1998, Neuropharmacology.

[4]  S. Solomon,et al.  Spatial properties of koniocellular cells in the lateral geniculate nucleus of the marmoset Callithrix jacchus , 2001, The Journal of physiology.

[5]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[6]  S. W. Kuffler Discharge patterns and functional organization of mammalian retina. , 1953, Journal of neurophysiology.

[7]  Kwabena Boahen,et al.  Functional circuitry for peripheral suppression in Mammalian Y-type retinal ganglion cells. , 2007, Journal of neurophysiology.

[8]  R. W. Rodieck,et al.  Identification, classification and anatomical segregation of cells with X‐like and Y‐like properties in the lateral geniculate nucleus of old‐world primates. , 1976, The Journal of physiology.

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

[10]  M. Carandini,et al.  Functional Mechanisms Shaping Lateral Geniculate Responses to Artificial and Natural Stimuli , 2008, Neuron.

[11]  E. Chichilnisky,et al.  Adaptation to Temporal Contrast in Primate and Salamander Retina , 2001, The Journal of Neuroscience.

[12]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

[13]  L. Croner,et al.  Receptive fields of P and M ganglion cells across the primate retina , 1995, Vision Research.

[14]  P. Lennie,et al.  Rapid adaptation in visual cortex to the structure of images. , 1999, Science.

[15]  Barry B. Lee,et al.  Suppressive Surrounds and Contrast Gain in Magnocellular-Pathway Retinal Ganglion Cells of Macaque , 2006, The Journal of Neuroscience.

[16]  M. Meister,et al.  Fast and Slow Contrast Adaptation in Retinal Circuitry , 2002, Neuron.

[17]  P. Lennie,et al.  Habituation Reveals Fundamental Chromatic Mechanisms in Striate Cortex of Macaque , 2008, The Journal of Neuroscience.

[18]  R. W. Rodieck Quantitative analysis of cat retinal ganglion cell response to visual stimuli. , 1965, Vision research.

[19]  F. Werblin,et al.  Control of Retinal Sensitivity: I. Light and Dark Adaptation of Vertebrate Rods and Cones , 1974 .

[20]  K. K. Ghosh,et al.  Analysis of two types of cone bipolar cells in the retina of a New World monkey, the marmoset, Callithrix jacchus , 1999, Visual Neuroscience.

[21]  R. Masland,et al.  Spatial scale and cellular substrate of contrast adaptation by retinal ganglion cells , 2001, Nature Neuroscience.

[22]  C. Enroth-Cugell,et al.  Effects of Remote Stimulation on the Mean Firing Rate of Cat Retinal Ganglion Cells , 2001, The Journal of Neuroscience.

[23]  H. Wässle,et al.  Synaptic Currents Generating the Inhibitory Surround of Ganglion Cells in the Mammalian Retina , 2001, The Journal of Neuroscience.

[24]  A. B. Bonds Role of Inhibition in the Specification of Orientation Selectivity of Cells in the Cat Striate Cortex , 1989, Visual Neuroscience.

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

[26]  W. Levick,et al.  Lateral geniculate neurons of cat: retinal inputs and physiology. , 1972, Investigative ophthalmology.

[27]  R. Shapley,et al.  Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque , 1981, Nature.

[28]  Peter D Lukasiewicz,et al.  Spike-dependent GABA inputs to bipolar cell axon terminals contribute to lateral inhibition of retinal ganglion cells. , 2003, Journal of neurophysiology.

[29]  Chris J. Tinsley,et al.  Spatial distribution of suppressive signals outside the classical receptive field in lateral geniculate nucleus. , 2005, Journal of neurophysiology.

[30]  H. Barlow,et al.  Evidence for a Physiological Explanation of the Waterfall Phenomenon and Figural After-effects , 1963, Nature.

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

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

[33]  P. Cook,et al.  Lateral inhibition in the inner retina is important for spatial tuning of ganglion cells , 1998, Nature Neuroscience.

[34]  P. Lennie,et al.  Profound Contrast Adaptation Early in the Visual Pathway , 2004, Neuron.

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

[36]  J. B. Demb,et al.  Presynaptic Mechanism for Slow Contrast Adaptation in Mammalian Retinal Ganglion Cells , 2006, Neuron.

[37]  F. Rieke Temporal Contrast Adaptation in Salamander Bipolar Cells , 2001, The Journal of Neuroscience.

[38]  T R Vidyasagar,et al.  Response of neurons in the cat's lateral geniculate nucleus to moving bars of different length , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  D. Hubel,et al.  Integrative action in the cat's lateral geniculate body , 1961, The Journal of physiology.

[40]  B. Borghuis,et al.  Cellular Basis for Contrast Gain Control over the Receptive Field Center of Mammalian Retinal Ganglion Cells , 2007, The Journal of Neuroscience.

[41]  A. Derrington,et al.  Long-range interactions in the lateral geniculate nucleus of the New-World monkey, Callithrix jacchus , 2001, Visual Neuroscience.

[42]  J. B. Levitt,et al.  The spatial extent over which neurons in macaque striate cortex pool visual signals , 2002, Visual Neuroscience.

[43]  R. Shapley,et al.  The nonlinear pathway of Y ganglion cells in the cat retina , 1979, The Journal of general physiology.

[44]  F. Werblin Control of Retinal Sensitivity II . Lateral Interactions at the Outer Plexiform Layer , 2022 .

[45]  P. Lennie,et al.  Pattern-selective adaptation in visual cortical neurones , 1979, Nature.

[46]  M. O'Shea,et al.  Protection from habituation by lateral inhibition , 1975, Nature.

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

[48]  M. Pettet,et al.  Dynamic changes in receptive-field size in cat primary visual cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[49]  I. Ohzawa,et al.  Receptive field structure in the visual cortex: does selective stimulation induce plasticity? , 1995, Proceedings of the National Academy of Sciences of the United States of America.

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

[51]  R. Shapley,et al.  The contrast gain control of the cat retina , 1979, Vision Research.

[52]  J. Movshon,et al.  Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[53]  P. Lennie,et al.  Early and Late Mechanisms of Surround Suppression in Striate Cortex of Macaque , 2005, The Journal of Neuroscience.

[54]  M. Carandini,et al.  The Suppressive Field of Neurons in Lateral Geniculate Nucleus , 2005, The Journal of Neuroscience.

[55]  L. Palmer,et al.  Suppression at high spatial frequencies in the lateral geniculate nucleus of the cat. , 2007, Journal of neurophysiology.

[56]  Luiz Pessoa,et al.  Fear perception: can objective and subjective awareness measures be dissociated? , 2007, Journal of vision.

[57]  H. Barlow Summation and inhibition in the frog's retina , 1953, The Journal of physiology.

[58]  Ralph D Freeman,et al.  Spatial frequency-specific contrast adaptation originates in the primary visual cortex. , 2007, Journal of neurophysiology.

[59]  W. Martin Usrey,et al.  Origin and Dynamics of Extraclassical Suppression in the Lateral Geniculate Nucleus of the Macaque Monkey , 2008, Neuron.

[60]  F. Sengpiel,et al.  Orientation specificity of contrast adaptation in visual cortical pinwheel centres and iso‐orientation domains , 2002, The European journal of neuroscience.

[61]  C. Enroth-Cugell,et al.  The receptive‐field spatial structure of cat retinal Y cells. , 1987, The Journal of physiology.

[62]  D. Copenhagen,et al.  Control of Retinal Sensitivity II. Lateral Interactions at the Outer Plexiform Layer , 1974 .

[63]  Paul R. Martin,et al.  Extraclassical Receptive Field Properties of Parvocellular, Magnocellular, and Koniocellular Cells in the Primate Lateral Geniculate Nucleus , 2002, The Journal of Neuroscience.

[64]  R. Shapley,et al.  The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[65]  A. M. Sillito,et al.  Orientation sensitive elements in the corticofugal influence on centre-surround interactions in the dorsal lateral geniculate nucleus , 1993, Experimental Brain Research.

[66]  A. Kohn Visual adaptation: physiology, mechanisms, and functional benefits. , 2007, Journal of neurophysiology.

[67]  B. Dreher,et al.  Relationship between contrast adaptation and orientation tuning in V1 and V2 of cat visual cortex. , 2006, Journal of neurophysiology.

[68]  Amanda Parker,et al.  Feedback from V1 and inhibition from beyond the classical receptive field modulates the responses of neurons in the primate lateral geniculate nucleus , 2002, Visual Neuroscience.

[69]  Kerry J. Kim,et al.  Temporal Contrast Adaptation in the Input and Output Signals of Salamander Retinal Ganglion Cells , 2001, The Journal of Neuroscience.