LGN input to simple cells and contrast-invariant orientation tuning: an analysis.

We develop a new analysis of the lateral geniculate nucleus (LGN) input to a cortical simple cell, demonstrating that this input is the sum of two terms, a linear term and a nonlinear term. In response to a drifting grating, the linear term represents the temporal modulation of input, and the nonlinear term represents the mean input. The nonlinear term, which grows with stimulus contrast, has been neglected in many previous models of simple cell response. We then analyze two scenarios by which contrast-invariance of orientation tuning may arise. In the first scenario, at larger contrasts, the nonlinear part of the LGN input, in combination with strong push-pull inhibition, counteracts the nonlinear effects of cortical spike threshold, giving the result that orientation tuning scales with contrast. In the second scenario, at low contrasts, the nonlinear component of LGN input is negligible, and noise smooths the nonlinearity of spike threshold so that the input-output function approximates a power-law function. These scenarios can be combined to yield contrast-invariant tuning over the full range of stimulus contrast. The model clarifies the contribution of LGN nonlinearities to the orientation tuning of simple cells and demonstrates how these nonlinearities may impact different models of contrast-invariant tuning.

[1]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[2]  References , 1971 .

[3]  C. Gilbert.  Laminar differences in receptive field properties of cells in cat primary visual cortex , 1977, The Journal of physiology.

[4]  J. Movshon,et al.  Spatial summation in the receptive fields of simple cells in the cat's striate cortex. , 1978, The Journal of physiology.

[5]  G. Henry,et al.  Laminar distribution of first-order neurons and afferent terminals in cat striate cortex. , 1979, Journal of neurophysiology.

[6]  D. Ferster,et al.  An intracellular analysis of geniculo‐cortical connectivity in area 17 of the cat. , 1983, The Journal of physiology.

[7]  R. L. de Valois,et al.  Relationship between spatial-frequency and orientation tuning of striate-cortex cells. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[8]  D. Ferster.  Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  J. P. Jones,et al.  An evaluation of the two-dimensional Gabor filter model of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[10]  J. P. Jones,et al.  The two-dimensional spatial structure of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[11]  I. Ohzawa,et al.  The effects of contrast on visual orientation and spatial frequency discrimination: a comparison of single cells and behavior. , 1987, Journal of neurophysiology.

[12]  D. Ferster.  Origin of orientation-selective EPSPs in simple cells of cat visual cortex , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  D. Ferster.  Spatially opponent excitation and inhibition in simple cells of the cat visual cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[15]  G. Orban,et al.  How well do response changes of striate neurons signal differences in orientation: a study in the discriminating monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  P. Hammond,et al.  Influence of spatial frequency on tuning and bias for orientation and direction in the cat's striate cortex , 1990, Vision Research.

[17]  D. Amit,et al.  Quantitative study of attractor neural networks retrieving at low spike rates: II. Low-rate retrieval in symmetric networks , 1991 .

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

[19]  Daniel J. Amit,et al.  Quantitative Study of Attractor Neural Network Retrieving at Low Spike Rates: I , 1991 .

[20]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[21]  D. Heeger.  Half-squaring in responses of cat striate cells , 1992, Visual Neuroscience.

[22]  H. Sompolinsky,et al.  Theory of orientation tuning in visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[23]  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.

[24]  R. Reid,et al.  Specificity of monosynaptic connections from thalamus to visual cortex , 1995, Nature.

[25]  S. Nelson,et al.  An emergent model of orientation selectivity in cat visual cortical simple cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  C. Koch,et al.  Recurrent excitation in neocortical circuits , 1995, Science.

[27]  D J Simons,et al.  Spatial gradients and inhibitory summation in the rat whisker barrel system. , 1996, Journal of neurophysiology.

[28]  Christof Koch,et al.  Shunting Inhibition Does Not Have a Divisive Effect on Firing Rates , 1997, Neural Computation.

[29]  R. Reid,et al.  Synaptic Integration in Striate Cortical Simple Cells , 1998, The Journal of Neuroscience.

[30]  Nicholas J. Priebe,et al.  Contrast-Invariant Orientation Tuning in Cat Visual Cortex: Thalamocortical Input Tuning and Correlation-Based Intracortical Connectivity , 1998, The Journal of Neuroscience.

[31]  L. Palmer,et al.  Temporal diversity in the lateral geniculate nucleus of cat , 1998, Visual Neuroscience.

[32]  Y. Frégnac,et al.  Visual input evokes transient and strong shunting inhibition in visual cortical neurons , 1998, Nature.

[33]  Harvey A Swadlow,et al.  Neocortical efferent neurons with very slowly conducting axons: strategies for reliable antidromic identification , 1998, Journal of Neuroscience Methods.

[34]  I. Ohzawa,et al.  Linear and nonlinear contributions to orientation tuning of simple cells in the cat's striate cortex , 1999, Visual Neuroscience.

[35]  D. Ferster,et al.  The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. , 2000, Science.

[36]  M. Carandini,et al.  Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. , 2000, Journal of neurophysiology.

[37]  R. Shapley,et al.  A neuronal network model of macaque primary visual cortex (V1): orientation selectivity and dynamics in the input layer 4Calpha. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[38]  M. Carandini,et al.  Membrane Potential and Firing Rate in Cat Primary Visual Cortex , 2000, The Journal of Neuroscience.

[39]  D. Ferster,et al.  Neural mechanisms of orientation selectivity in the visual cortex. , 2000, Annual review of neuroscience.

[40]  Michael Shelley,et al.  How Simple Cells Are Made in a Nonlinear Network Model of the Visual Cortex , 2001, The Journal of Neuroscience.

[41]  D. Ferster,et al.  Prediction of Orientation Selectivity from Receptive Field Architecture in Simple Cells of Cat Visual Cortex , 2001, Neuron.

[42]  K. Miller,et al.  Neural noise can explain expansive, power-law nonlinearities in neural response functions. , 2002, Journal of neurophysiology.

[43]  R. Freeman,et al.  Orientation selectivity in the cat's striate cortex is invariant with stimulus contrast , 2004, Experimental Brain Research.

[44]  Trichur Raman Vidyasagar,et al.  Relationship between orientation tuning and spatial frequency in neurones of cat area 17 , 2004, Experimental Brain Research.