An architectural hypothesis for direction selectivity in the visual cortex: the role of spatially asymmetric intracortical inhibition

Abstract. Within a linear field approach, an architectural model for simple cell direction selectivity in the visual cortex is proposed. The origin of direction selectivity is related to recurrent intracortical interactions with a spatially asymmetric character along the axis of stimulus motion. No explicit asymmetric temporal mechanisms are introduced or adopted. The analytical investigation of network behavior, carried out under the assumption of a linear superposition of geniculate and intracortical contributions, shows that motion sensitivity of the resulting receptive fields emerges as a dynamic property of the cortical network without any feed-forward direction selectivity bias. A detailed analysis of the effects of the architectural characteristics of the cortical network on directionality and velocity-response curves was conducted by systematically varying the model's parameters.

[1]  Kevan A. C. Martin,et al.  A Canonical Microcircuit for Neocortex , 1989, Neural Computation.

[2]  Leo Ganz,et al.  Visual cortical mechanisms responsible for direction selectivity , 1984, Vision Research.

[3]  K. Martin,et al.  Excitatory synaptic inputs to spiny stellate cells in cat visual cortex , 1996, Nature.

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

[5]  L. Palmer,et al.  Contribution of linear spatiotemporal receptive field structure to velocity selectivity of simple cells in area 17 of cat , 1989, Vision Research.

[6]  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.

[7]  A Grinvald,et al.  Coherent spatiotemporal patterns of ongoing activity revealed by real-time optical imaging coupled with single-unit recording in the cat visual cortex. , 1995, Journal of neurophysiology.

[8]  M. Landy,et al.  The Plenoptic Function and the Elements of Early Vision , 1991 .

[9]  D. Heeger.  Modeling simple-cell direction selectivity with normalized, half-squared, linear operators. , 1993, Journal of neurophysiology.

[10]  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.

[11]  A. Sillito.  Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat's visual cortex , 1977, The Journal of physiology.

[12]  C. Koch,et al.  A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  P. Gaudiano.  Simulations of X and Y retinal ganglion cell behavior with a nonlinear push-pull model of spatiotemporal retinal processing , 1994, Vision Research.

[14]  R. C. Emerson.  Quadrature subunits in directionally selective simple cells: Spatiotemporal interactions , 1997, Visual Neuroscience.

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

[16]  Hanspeter A. Mallot,et al.  Population networks: a large-scale framework for modelling cortical neural networks , 1996, Biological Cybernetics.

[17]  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.

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

[19]  W. Singer,et al.  Horizontal Interactions in Cat Striate Cortex: II. A Current Source‐Density Analysis , 1990, The European journal of neuroscience.

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

[21]  A J Ahumada,et al.  Model of human visual-motion sensing. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[22]  Hanspeter A. Mallot,et al.  Neural mapping and space-variant image processing , 1990, 1990 IJCNN International Joint Conference on Neural Networks.

[23]  R. C. Emerson,et al.  Quadrature subunits in directionally selective simple cells: Counterphase and drifting grating responses , 1997, Visual Neuroscience.

[24]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[25]  Hanspeter A. Mallot,et al.  Layered computation in neural networks , 1998 .

[26]  G. Gerstein,et al.  Networks with lateral connectivity. I. dynamic properties mediated by the balance of intrinsic excitation and inhibition. , 1996, Journal of neurophysiology.

[27]  D. G. Albrecht,et al.  Visual cortical receptive fields in monkey and cat: Spatial and temporal phase transfer function , 1989, Vision Research.

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

[29]  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.

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

[31]  C. Koch,et al.  The analysis of visual motion: from computational theory to neuronal mechanisms. , 1986, Annual review of neuroscience.

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

[33]  K. Albus,et al.  A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat , 1975, Experimental Brain Research.

[34]  Professor Dr. Guy A. Orban.  Neuronal Operations in the Visual Cortex , 1983, Studies of Brain Function.

[35]  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.

[36]  E H Adelson,et al.  Spatiotemporal energy models for the perception of motion. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[37]  R. Frostig,et al.  Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  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.

[39]  C. Nicholson,et al.  Theoretical analysis of field potentials in anisotropic ensembles of neuronal elements. , 1973, IEEE transactions on bio-medical engineering.

[40]  D. S. JONES,et al.  Simulation and Analysis , 1968, Nature.

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

[42]  Christof Koch,et al.  Modeling the mammalian visual system , 1989 .

[43]  D. Tolhurst,et al.  Evaluation of a linear model of directional selectivity in simple cells of the cat's striate cortex , 1991, Visual Neuroscience.

[44]  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.

[45]  F. Wörgötter,et al.  Spatiotemporal mechanisms in receptive fields of visual cortical simple cells: a model. , 1991, Journal of neurophysiology.

[46]  H. J. Luhmann,et al.  Horizontal Interactions in Cat Striate Cortex: III. Ectopic Receptive Fields and Transient Exuberance of Tangential Interactions , 1990, The European journal of neuroscience.

[47]  R. Eckhorn,et al.  Visual receptive fields of local intracortical potentials , 1988, Journal of Neuroscience Methods.

[48]  Fabio Solari,et al.  An Architectural Mechanism for Direction-tuned Cortical Simple Cells: The Role of Mutual Inhibition , 1996, NIPS.

[49]  G. Orban,et al.  Model circuit of spiking neurons generating directional selectivity in simple cells. , 1996, Journal of neurophysiology.