Direction selectivity of simple cells in the primary visual cortex: Comparison of two alternative mathematical models. I: Response to drifting gratings

Two models of a single hypercolumn in the primary visual cortex are presented, and used for the analysis of direction selectivity in simple cells. The two models differ as to the arrangement of inhibitory connections: in the first ("antiphase model") inhibition is in phase opposition with excitation, but with a similar orientation tuning; in the second ("in-phase model"), inhibition is in phase with excitation, but with broader orientation tuning. Simulation results, performed by using drifting gratings with different orientations, and different spatial and temporal frequencies, show that both models are able to explain the origin of direction preference of simple cells.

[1]  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.

[2]  K. Tanaka.  Cross-correlation analysis of geniculostriate neuronal relationships in cats. , 1983, Journal of neurophysiology.

[3]  Frances S. Chance,et al.  Synaptic Depression and the Temporal Response Characteristics of V1 Cells , 1998, The Journal of Neuroscience.

[4]  Leon N. Cooper,et al.  Formation of Direction Selectivity in Natural Scene Environments , 2000, Neural Computation.

[5]  D N Mastronarde,et al.  Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. , 1987, Journal of neurophysiology.

[6]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Mauro Ursino,et al.  Comparison of different models of orientation selectivity based on distinct intracortical inhibition rules , 2004, Vision Research.

[8]  G. DeAngelis,et al.  Spatiotemporal receptive field organization in the lateral geniculate nucleus of cats and kittens. , 1997, Journal of neurophysiology.

[9]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development. , 1993, Journal of neurophysiology.

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

[11]  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.

[12]  R. L. de Valois,et al.  Inputs to directionally selective simple cells in macaque striate cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[13]  D. Ferster,et al.  Orientation selectivity of thalamic input to simple cells of cat visual cortex , 1996, Nature.

[14]  Russell L. De Valois,et al.  PII: S0042-6989(00)00210-8 , 2000 .

[15]  M. Carandini,et al.  Predictions of a recurrent model of orientation selectivity , 1997, Vision Research.

[16]  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.

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

[18]  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.

[19]  A. L. Humphrey,et al.  Strobe rearing reduces direction selectivity in area 17 by altering spatiotemporal receptive-field structure. , 1998, Journal of neurophysiology.

[20]  A L Humphrey,et al.  Strobe rearing prevents the convergence of inputs with different response timings onto area 17 simple cells. , 1998, Journal of neurophysiology.

[21]  Jose-Manuel Alonso,et al.  Functionally distinct inhibitory neurons at the first stage of visual cortical processing , 2003, Nature Neuroscience.

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

[23]  A L Humphrey,et al.  Laminar differences in the spatiotemporal structure of simple cell receptive fields in cat area 17 , 1997, Visual Neuroscience.

[24]  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.

[25]  Mauro Ursino,et al.  Direction selectivity of simple cells in the primary visual cortex: Comparison of two alternative mathematical models. II: Velocity tuning and response to moving bars , 2007, Comput. Biol. Medicine.

[26]  C. Koch,et al.  Modeling direction selectivity of simple cells in striate visual cortex within the framework of the canonical microcircuit , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  Guy A. Orban,et al.  A Model Circuit for Cortical Temporal Low-Pass Filtering , 1992, Neural Computation.

[28]  R. Douglas,et al.  A functional microcircuit for cat visual cortex. , 1991, The Journal of physiology.

[29]  K. Miller,et al.  Different Roles for Simple-Cell and Complex-Cell Inhibition in V1 , 2003, The Journal of Neuroscience.

[30]  J. Leo van Hemmen,et al.  Development of spatiotemporal receptive fields of simple cells: I. Model formulation , 1997, Biological Cybernetics.

[31]  C. Enroth-Cugell,et al.  Receptive field properties of X and Y cells in the cat retina derived from contrast sensitivity measurements , 1982, Vision Research.

[32]  R E Weller,et al.  Structural correlates of functionally distinct X‐cells in the lateral geniculate nucleus of the cat , 1988, The Journal of comparative neurology.

[33]  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.

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

[36]  R. Shapley,et al.  Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. , 1991, Journal of neurophysiology.

[37]  L. Palmer,et al.  Contribution of linear mechanisms to the specification of local motion by simple cells in areas 17 and 18 of the cat , 1994, Visual Neuroscience.

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

[39]  I. Ohzawa,et al.  Receptive-field dynamics in the central visual pathways , 1995, Trends in Neurosciences.

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

[41]  D. Kleinfeld,et al.  On temporal codes and the spatiotemporal response of neurons in the lateral geniculate nucleus. , 1994, Journal of neurophysiology.

[42]  A. L. Humphrey,et al.  Hebbian learning and the development of direction selectivity: the role of geniculate response timings , 1997 .

[43]  A. L. Humphrey,et al.  Evidence of input from lagged cells in the lateral geniculate nucleus to simple cells in cortical area 17 of the cat. , 1992, Journal of neurophysiology.

[44]  R. Reid,et al.  Rules of Connectivity between Geniculate Cells and Simple Cells in Cat Primary Visual Cortex , 2001, The Journal of Neuroscience.

[45]  D N Mastronarde,et al.  Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive-field properties and classification of cells. , 1987, Journal of neurophysiology.

[46]  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.

[47]  J. Leo van Hemmen,et al.  Development of spatiotemporal receptive fields of simple cells: II. Simulation and analysis , 1997, Biological Cybernetics.