The Suppressive Field of Neurons in Lateral Geniculate Nucleus

The responses of neurons in lateral geniculate nucleus (LGN) exhibit powerful suppressive phenomena such as contrast saturation, size tuning, and masking. These phenomena cannot be explained by the classical center-surround receptive field and have been ascribed to a variety of mechanisms, including feedback from cortex. We asked whether these phenomena might all be explained by a single mechanism, contrast gain control, which is inherited from retina and possibly strengthened in thalamus. We formalized an intuitive model of retinal contrast gain control that explicitly predicts gain as a function of local contrast. In the model, the output of the receptive field is divided by the output of a suppressive field, which computes the local root-mean-square contrast. The model provides good fits to LGN responses to a variety of stimuli; with a single set of parameters, it captures saturation, size tuning, and masking. It also correctly predicts that responses to small stimuli grow proportionally with contrast: were it not for the suppressive field, LGN responses would be linear. We characterized the suppressive field and found that it is similar in size to the surround of the classical receptive field (which is eight times larger than commonly estimated), it is not selective for stimulus orientation, and it responds to a wide range of frequencies, including very low spatial frequencies and high temporal frequencies. The latter property is hardly consistent with feedback from cortex. These measurements thoroughly describe the visual properties of contrast gain control in LGN and provide a parsimonious explanation for disparate suppressive phenomena.

[1]  Robert A. Frazor,et al.  Independence of luminance and contrast in natural scenes and in the early visual system , 2005, Nature Neuroscience.

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

[3]  J. B. Demb,et al.  Contrast Adaptation in Subthreshold and Spiking Responses of Mammalian Y-Type Retinal Ganglion Cells , 2005, The Journal of Neuroscience.

[4]  T. Shou,et al.  Orientation bias of the extraclassical receptive field of the relay cells in the cat's dorsal lateral geniculate nucleus , 2004, Neuroscience.

[5]  L. Palmer,et al.  Contrast-dependent spatial summation in the lateral geniculate nucleus and retina of the cat. , 2004, Journal of neurophysiology.

[6]  J. Kremers,et al.  Lateral interactions in the perception of flicker and in the physiology of the lateral geniculate nucleus. , 2004, Journal of vision.

[7]  Henry J. Alitto,et al.  Influence of contrast on orientation and temporal frequency tuning in ferret primary visual cortex. , 2004, Journal of neurophysiology.

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

[9]  H. Ozeki,et al.  Relationship between Excitation and Inhibition Underlying Size Tuning and Contextual Response Modulation in the Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.

[10]  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.

[11]  M. Wright,et al.  Spatial and temporal properties of ‘sustained’ and ‘transient’ neurones in area 17 of the cat's visual cortex , 1975, Experimental Brain Research.

[12]  J. Krüger,et al.  Strong periphery effect in cat retinal ganglion cells. Excitatory responses in ON- and OFF-center neurones to single grid displacements , 1973, Experimental Brain Research.

[13]  T. Carney,et al.  Binocular interaction in the perigeniculate nucleus of the cat , 2004, Experimental Brain Research.

[14]  G. Sclar,et al.  Expression of “retinal” contrast gain control by neurons of the cat's lateral geniculate nucleus , 2004, Experimental Brain Research.

[15]  Trichur Raman Vidyasagar,et al.  Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18 , 2004, Experimental Brain Research.

[16]  C. Koch,et al.  The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus , 2004, Experimental Brain Research.

[17]  Microstimulation in LGN produces focal visual percepts , 2004 .

[18]  J. Morgan,et al.  Spatial properties of neurones in the lateral geniculate nucleus of the pigmented ferret , 2004, Experimental Brain Research.

[19]  G. Ahlsén,et al.  Functional distinction of perigeniculate and thalamic reticular neurons in the cat , 2004, Experimental Brain Research.

[20]  W. Singer,et al.  Reciprocal lateral inhibition of on- and off-center neurones in the lateral geniculate body of the cat , 2004, Experimental Brain Research.

[21]  Henry J. Alitto,et al.  Corticothalamic feedback and sensory processing , 2003, Current Opinion in Neurobiology.

[22]  J. B. Demb,et al.  Different Circuits for ON and OFF Retinal Ganglion Cells Cause Different Contrast Sensitivities , 2003, The Journal of Neuroscience.

[23]  Luiz Carlos L Silveira,et al.  Centre and surround responses of marmoset lateral geniculate neurones at different temporal frequencies , 2003, The Journal of physiology.

[24]  Jianzhong Jin,et al.  GABAA and GABAB receptors mediated inhibition affect the pattern adaptation of relay cells in the dorsal lateral geniculate nucleus (LGNd) of cats , 2003, Brain Research.

[25]  R. Navarro,et al.  Input–output statistical independence in divisive normalization models of V1 neurons , 2003, Network.

[26]  Adam M Sillito,et al.  Corticothalamic interactions in the transfer of visual information. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[27]  F. Wörgötter,et al.  The influence of the corticothalamic projection on responses in thalamus and cortex. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[29]  Jonathan B Demb,et al.  Multiple Mechanisms for Contrast Adaptation in the Retina , 2002, Neuron.

[30]  Cyrille C. Girardin,et al.  The effect of moving textures on the responses of cells in the cat's dorsal lateral geniculate nucleus , 2002, The European journal of neuroscience.

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

[32]  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.

[33]  M. Carandini,et al.  Suppression without Inhibition in Visual Cortex , 2002, Neuron.

[34]  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.

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

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

[37]  Eero P. Simoncelli,et al.  Natural signal statistics and sensory gain control , 2001, Nature Neuroscience.

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

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

[40]  J. Kremers,et al.  Influence of contrast on the responses of marmoset lateral geniculate cells to drifting gratings. , 2001, Journal of neurophysiology.

[41]  E Kaplan,et al.  The dynamics of primate retinal ganglion cells. , 2001, Progress in brain research.

[42]  Ethan A. Benardete,et al.  THE DYNAMICS OF PRIMATE RETINAL GANGLION CELLS PROGRESS IN BRAIN RESEARCH 2001 , 2001 .

[43]  Ethan A. Benardete,et al.  Chapter 2 The dynamics of primate retinal ganglion cells , 2001 .

[44]  D. Pollen,et al.  Striate cortex increases contrast gain of macaque LGN neurons , 2000, Visual Neuroscience.

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

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

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

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

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

[50]  U. Eysel,et al.  Inverse correlation of firing patterns of single topographically matched perigeniculate neurons and cat dorsal lateral geniculate relay cells , 1998, Visual Neuroscience.

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

[52]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[53]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[54]  Y. Zhou,et al.  Adaptation of visually evoked responses of relay cells in the dorsal lateral geniculate nucleus of the cat following prolonged exposure to drifting gratings , 1996, Visual Neuroscience.

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

[56]  Earl L. Smith,et al.  Transfer characteristics of lateral geniculate nucleus X neurons in the cat: effects of spatial frequency and contrast. , 1995, Journal of neurophysiology.

[57]  H. Jones,et al.  The Length – Response Properties of Cells in the Feline Perigeniculate Nucleus , 1994, The European journal of neuroscience.

[58]  P. C. Murphy,et al.  Brain-stem modulation of the response properties of cells in the cat's perigeniculate nucleus , 1994, Visual Neuroscience.

[59]  A. Wróbel,et al.  Visual classification of X and Y perigeniculate neurons of the cat , 1994, Experimental Brain Research.

[60]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. , 1993, Journal of neurophysiology.

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

[62]  A. L. Humphrey,et al.  Temporal-frequency tuning of direction selectivity in cat visual cortex , 1992, Visual Neuroscience.

[63]  H. Jones,et al.  The length‐response properties of cells in the feline dorsal lateral geniculate nucleus. , 1991, The Journal of physiology.

[64]  D. G. Albrecht,et al.  Motion selectivity and the contrast-response function of simple cells in the visual cortex , 1991, Visual Neuroscience.

[65]  A L Humphrey,et al.  Morphology and axonal projection patterns of individual neurons in the cat perigeniculate nucleus. , 1991, Journal of neurophysiology.

[66]  John H. R. Maunsell,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[67]  A. L. Humphrey,et al.  Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. , 1990, Journal of neurophysiology.

[68]  A. Leventhal,et al.  Organized arrangement of orientation-sensitive relay cells in the cat's dorsal lateral geniculate nucleus , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[70]  E Kaplan,et al.  Abnormal orientation bias of LGN neurons in strabismic cats. , 1988, Investigative ophthalmology & visual science.

[71]  M. Dubin,et al.  Retinal Ganglion Cells , 1988 .

[72]  P. C. Murphy,et al.  Corticofugal feedback influences the generation of length tuning in the visual pathway , 1987, Nature.

[73]  E Kaplan,et al.  Contrast affects the transmission of visual information through the mammalian lateral geniculate nucleus. , 1987, The Journal of physiology.

[74]  R. Shapley,et al.  Linear mechanism of orientation tuning in the retina and lateral geniculate nucleus of the cat. , 1987, Journal of neurophysiology.

[75]  J. Victor The dynamics of the cat retinal X cell centre. , 1987, The Journal of physiology.

[76]  B. B. Lee,et al.  A comparison of visual responses of cat lateral geniculate nucleus neurones with those of ganglion cells afferent to them. , 1985, The Journal of physiology.

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

[78]  J. Daugman Uncertainty relation for resolution in space, spatial frequency, and orientation optimized by two-dimensional visual cortical filters. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[79]  R. Shapley,et al.  The receptive field organization of X-cells in the cat: Spatiotemporal coupling and asymmetry , 1984, Vision Research.

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

[81]  B. Cleland,et al.  Response to the length of moving visual stimuli of the brisk classes of ganglion cells in the cat retina. , 1983, The Journal of physiology.

[82]  G. Ahlsén,et al.  Corticofugal projection to perigeniculate neurones in the cat. , 1983, Acta physiologica Scandinavica.

[83]  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.

[84]  D. G. Albrecht,et al.  Striate cortex of monkey and cat: contrast response function. , 1982, Journal of neurophysiology.

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

[86]  R. Shapley,et al.  Spatial tuning of cells in and around lateral geniculate nucleus of the cat: X and Y relay cells and perigeniculate interneurons. , 1981, Journal of neurophysiology.

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

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

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

[90]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. , 1978, The Journal of physiology.

[91]  B. Cleland,et al.  Organization of visual inputs to interneurons of lateral geniculate nucleus of the cat. , 1977, Journal of neurophysiology.

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

[93]  L. Maffei,et al.  The visual cortex as a spatial frequency analyser. , 1973, Vision research.

[94]  The periphery effect and its relation to the receptive field organization of 'transient' retinal ganglion cells. , 1972, The Journal of physiology.

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

[96]  K. Sanderson,et al.  The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat , 1971, The Journal of comparative neurology.

[97]  James T. McIlwain,et al.  Microelectrode Study of Synaptic Excitation and Inhibition in the Lateral Geniculate Nucleus of the Cat , 1967 .

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

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

[100]  W. Levick,et al.  EVIDENCE THAT MCILWAIN'S PERIPHERY EFFECT IS NOT A STRAY LIGHT ARTIFACT. , 1965, Journal of neurophysiology.

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

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