Suppressive Surrounds and Contrast Gain in Magnocellular-Pathway Retinal Ganglion Cells of Macaque

The modulation sensitivity of visual neurons can be influenced by remote stimuli which, when presented alone, cause no change in the ongoing discharge rate of the neuron. We show here that the extraclassical surrounds that underlie these effects are present in magnocellular-pathway (MC) but not in parvocellular-pathway (PC) retinal ganglion cells of the macaque. The response of MC cells to drifting gratings and flashing spots was halved by drifting or contrast-reversing gratings surrounding their receptive fields, but PC cell responses were unaffected. The suppression cannot have arisen from the classical receptive field, or been caused by scattered light, because it could be evoked by annuli that themselves caused little or no response from the cell, and is consistent with the action of a divisive suppressive mechanism. Suppression in MC cells was broadly tuned for spatial and temporal frequency and greater at high contrast. If perceptual phenomena with similar stimulus contexts, such as the “shift effect” and saccadic suppression, have a retinal component, then they reflect the activity of the MC pathway.

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

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

[3]  J. Mcilwain.  RECEPTIVE FIELDS OF OPTIC TRACT AXONS AND LATERAL GENICULATE CELLS: PERIPHERAL EXTENT AND BARBITURATE SENSITIVITY. , 1964, Journal of neurophysiology.

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

[5]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[6]  D. M. MACKAY,et al.  Elevation of Visual Threshold by Displacement of Retinal Image , 1970, Nature.

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

[8]  F S Werblin,et al.  Lateral Interactions at Inner Plexiform Layer of Vertebrate Retina: Antagonistic Responses to Change , 1972, Science.

[9]  B. Dreher.  Hypercomplex cells in the cat's striate cortex. , 1972, Investigative ophthalmology.

[10]  B. Fischer,et al.  Quantitative aspects of the shift-effect in cat retinal ganglion cells , 1975, Brain Research.

[11]  R. Shapley,et al.  Quantitative analysis of retinal ganglion cell classifications. , 1976, The Journal of physiology.

[12]  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.

[13]  R. Shapley,et al.  Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. , 1976, The Journal of physiology.

[14]  H. Barlow,et al.  The effects of remote retinal stimulation on the responses of cat retinal ganglion cells. , 1977, The Journal of physiology.

[15]  L N Thibos,et al.  The properties of surround antagonism elicited by spinning windmill patterns in the mudpuppy retina. , 1978, The Journal of physiology.

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

[17]  B G Breitmeyer,et al.  Local foveal inhibitory effects of global peripheral excitation. , 1979, Science.

[18]  P. Lennie,et al.  The mechanism of peripherally evoked responses in retinal ganglion cells. , 1979, The Journal of physiology.

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

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

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

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

[23]  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.

[24]  P. Lennie,et al.  Chromatic mechanisms in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

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

[26]  Andrew M. Derrington,et al.  Spatial frequency selectivity of remote pattern masking , 1984, Vision Research.

[27]  J. Allman,et al.  Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. , 1985, Annual review of neuroscience.

[28]  C. Blakemore,et al.  Organization and post‐natal development of the monkey's lateral geniculate nucleus. , 1986, The Journal of physiology.

[29]  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.

[30]  B. Boycott,et al.  Neurofibrillar long-range amacrine cells in mammalian retinae , 1988, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[31]  D. Dacey,et al.  Axon‐bearing amacrine cells of the macaque monkey retina , 1989, The Journal of comparative neurology.

[32]  Bb Lee,et al.  Nonlinear summation of M- and L-cone inputs to phasic retinal ganglion cells of the macaque , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  T. Wiesel,et al.  The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat , 1990, Vision Research.

[34]  J. Pokorny,et al.  Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights. , 1992, The Journal of physiology.

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

[36]  D. Heeger.  Normalization of cell responses in cat striate cortex , 1992, Visual Neuroscience.

[37]  I. Ohzawa,et al.  Length and width tuning of neurons in the cat's primary visual cortex. , 1994, Journal of neurophysiology.

[38]  Barry B. Lee,et al.  The response of macaque ganglion cells and human observers to heterochromatically modulated lights: the effect of stimulus size , 1994, Vision Research.

[39]  D. Burr,et al.  Selective suppression of the magnocellular visual pathway during saccadic eye movements , 1994, Nature.

[40]  Joel Pokorny,et al.  Responses to pulses and sinusoids in macaque ganglion cells , 1994, Vision Research.

[41]  M. Carandini,et al.  Summation and division by neurons in primate visual cortex. , 1994, Science.

[42]  H. Jones,et al.  Visual cortical mechanisms detecting focal orientation discontinuities , 1995, Nature.

[43]  B. B. Lee,et al.  Temporal response of ganglion cells of the macaque retina to cone-specific modulation. , 1995, Journal of the Optical Society of America. A, Optics, image science, and vision.

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

[45]  A. Sillito,et al.  Spatial frequency tuning of orientation‐discontinuity‐sensitive corticofugal feedback to the cat lateral geniculate nucleus. , 1996, The Journal of physiology.

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

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

[48]  J. B. Levitt,et al.  Contrast dependence of contextual effects in primate visual cortex , 1997, nature.

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

[50]  E. Kaplan,et al.  The dynamics of primate M retinal ganglion cells , 1999, Visual Neuroscience.

[51]  R. Shapley,et al.  Contrast's effect on spatial summation by macaque V1 neurons , 1999, Nature Neuroscience.

[52]  A. Derrington,et al.  Long-range interactions modulate the contrast gain in the lateral geniculate nucleus of cats , 1999, Visual Neuroscience.

[53]  J. B. Demb,et al.  Functional Circuitry of the Retinal Ganglion Cell's Nonlinear Receptive Field , 1999, The Journal of Neuroscience.

[54]  Barry B. Lee,et al.  Center surround receptive field structure of cone bipolar cells in primate retina , 2000, Vision Research.

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

[56]  E J Chichilnisky,et al.  A simple white noise analysis of neuronal light responses , 2001, Network.

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

[58]  J. B. Demb,et al.  Bipolar Cells Contribute to Nonlinear Spatial Summation in the Brisk-Transient (Y) Ganglion Cell in Mammalian Retina , 2001, The Journal of Neuroscience.

[59]  R. Shapley,et al.  Visual spatial characterization of macaque V1 neurons. , 2001, Journal of neurophysiology.

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

[61]  J. B. Levitt,et al.  Visual response properties of neurons in the LGN of normally reared and visually deprived macaque monkeys. , 2001, Journal of neurophysiology.

[62]  Barry B. Lee,et al.  An examination of physiological mechanisms underlying the frequency-doubling illusion. , 2002, Investigative ophthalmology & visual science.

[63]  Frances S. Chance,et al.  Gain Modulation from Background Synaptic Input , 2002, Neuron.

[64]  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.

[65]  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.

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

[67]  J. Movshon,et al.  Selectivity and spatial distribution of signals from the receptive field surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[68]  F. Werblin,et al.  Rapid global shifts in natural scenes block spiking in specific ganglion cell types , 2003, Nature Neuroscience.

[69]  R. Barth,et al.  The shift-effect in retinal ganglion cells of the rhesus monkey , 1975, Experimental Brain Research.

[70]  H. K. HAltTLIn.  THE RESPONSE OF SINGLE OPTIC NERVE FIBERS OF THE VERTEBRATE EYE TO ILLUMINATION OF THE RETINA , 2004 .

[71]  The shift-effect in the lateral geniculate body of the rhesus monkey , 1977, Experimental Brain Research.

[72]  Barry B. Lee,et al.  The origin of the chromatic response of magnocellular ganglion cells , 2004 .

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

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

[75]  Paul R. Martin,et al.  Chromatic Organization of Ganglion Cell Receptive Fields in the Peripheral Retina , 2005, The Journal of Neuroscience.

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

[77]  G. Rees,et al.  Saccades Differentially Modulate Human LGN and V1 Responses in the Presence and Absence of Visual Stimulation , 2005, Current Biology.

[78]  G. Einevoll,et al.  Response of the difference-of-Gaussians model to circular drifting-grating patches , 2005, Visual Neuroscience.

[79]  P. Sajda,et al.  Extraclassical receptive field phenomena and short-range connectivity in V1. , 2005, Cerebral cortex.