A neural network model for the development of simple and complex cell receptive fields within cortical maps of orientation and ocular dominance

Prenatal development of the primary visual cortex leads to simple cells with spatially distinct and oriented ON and OFF subregions. These simple cells are organized into spatial maps of orientation and ocular dominance that exhibit singularities, fractures, and linear zones. On a finer spatial scale, simple cells occur that are sensitive to similar orientations but opposite contrast polarities, and exhibit both even-symmetric and odd-symmetric receptive fields. Pooling of outputs from oppositely polarized simple cells leads to complex cells that respond to both contrast polarities. A neural network model is described which simulates how simple and complex cells self-organize starting from unsegregated and unoriented geniculocortical inputs during prenatal development. Neighboring simple cells that are sensitive to opposite contrast polarities develop from a combination of spatially short-range inhibition and high-gain recurrent habituative excitation between cells that obey membrane equations. Habituation, or depression, of synapses controls reset of cell activations both through enhanced ON responses and OFF antagonistic rebounds. Orientation and ocular dominance maps form when high-gain medium-range recurrent excitation and long-range inhibition interact with the short-range mechanisms. The resulting structure clarifies how simple and complex cells contribute to perceptual processes such as texture segregation and perceptual grouping.

[1]  KD Miller A model for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between ON- and OFF-center inputs , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  W. Levick,et al.  Sustained and transient neurones in the cat's retina and lateral geniculate nucleus , 1971, The Journal of physiology.

[3]  S. Grossberg,et al.  Self-Organization of Binocular Disparity Tuning by Reciprocal Corticogeniculate Interactions , 1998, Journal of Cognitive Neuroscience.

[4]  William H. Press,et al.  Numerical Recipes in Fortran 77: The Art of Scientific Computing 2nd Editionn - Volume 1 of Fortran Numerical Recipes , 1992 .

[5]  G. T. Ladd President's address before the New York Meeting of the American Psychological Association. , 1894 .

[6]  田中 啓治 Organization of Geniculate Inputs to Visual Cortical Cells in the Cat , 1986 .

[7]  S. Grossberg Cortical dynamics of three-dimensional form, color, and brightness perception: I. Monocular theory , 1987, Perception & psychophysics.

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

[9]  G. Blasdel,et al.  Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  G. Blasdel,et al.  Voltage-sensitive dyes reveal a modular organization in monkey striate cortex , 1986, Nature.

[11]  P. Schiller,et al.  Quantitative studies of single-cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance. , 1976, Journal of neurophysiology.

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

[13]  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.

[14]  S. Grossberg On the production and release of chemical transmitters and related topics in cellular control. , 1969, Journal of theoretical biology.

[15]  S Grossberg,et al.  Cortical dynamics of three-dimensional form, color, and brightness perception: II. Binocular theory , 1988, Perception & psychophysics.

[16]  R Linsker,et al.  From basic network principles to neural architecture: emergence of spatial-opponent cells. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[17]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[18]  Teuvo Kohonen,et al.  Self-organization and associative memory: 3rd edition , 1989 .

[19]  D Debanne,et al.  Cortical convergence of ON- and OFF-pathways and functional adaptation of receptive field organization in cat area 17. , 1993, Progress in brain research.

[20]  S. Grossberg,et al.  How does a brain build a cognitive code? , 1980, Psychological review.

[21]  C. Koch,et al.  Recurrent excitation in neocortical cells , 1995 .

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

[23]  S. Grossberg Cortical dynamics of three-dimensional figure-ground perception of two-dimensional pictures. , 1997, Psychological review.

[24]  R. Linsker,et al.  From basic network principles to neural architecture , 1986 .

[25]  D. D. Michaels Ocular dominance. , 1972, Survey of ophthalmology.

[26]  William H. Press,et al.  Numerical Recipes in C, 2nd Edition , 1992 .

[27]  GrossbergS. Adaptive pattern classification and universal recoding , 1976 .

[28]  Stephen Grossberg,et al.  Rules for the cortical map of ocular dominance and orientation columns , 1994, Neural Networks.

[29]  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.

[30]  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.

[31]  S. Grossberg,et al.  Cortical dynamics of feature binding and reset: Control of visual persistence , 1994, Vision Research.

[32]  S. Nelson,et al.  Orientation selectivity of cortical neurons during intracellular blockade of inhibition. , 1994, Science.

[33]  S Grossberg,et al.  3-D vision and figure-ground separation by visual cortex , 2010, Perception & psychophysics.

[34]  K. Obermayer,et al.  Statistical-mechanical analysis of self-organization and pattern formation during the development of visual maps. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[35]  M. Stryker,et al.  Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  C. Malsburg,et al.  How patterned neural connections can be set up by self-organization , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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

[39]  Peter H. Schiller,et al.  The ON and OFF channels of the visual system , 1992, Trends in Neurosciences.

[40]  N. Swindale A model for the formation of ocular dominance stripes , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[41]  Richard Durbin,et al.  A dimension reduction framework for understanding cortical maps , 1990, Nature.

[42]  Teuvo Kohonen,et al.  Self-Organization and Associative Memory , 1988 .

[43]  S. Grossberg,et al.  Neural dynamics of form perception: boundary completion, illusory figures, and neon color spreading. , 1985, Psychological review.

[44]  Stephen Grossberg,et al.  Cortical Dynamics of 3-D Figure-Ground Perception of 2-D Pictures , 1995 .

[45]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1990 .

[46]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[47]  D. Hubel,et al.  Shape and arrangement of columns in cat's striate cortex , 1963, The Journal of physiology.

[48]  Amiram Grinvald,et al.  Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns , 1991, Nature.

[49]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[50]  H. Ritter,et al.  A principle for the formation of the spatial structure of cortical feature maps. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Lowell D. Jacobson,et al.  Structural testing of multi-input linear—nonlinear cascade models for cells in macaque striate cortex , 1993, Vision Research.

[52]  R. L. Valois,et al.  The orientation and direction selectivity of cells in macaque visual cortex , 1982, Vision Research.

[53]  G. Blasdel,et al.  Orientation selectivity, preference, and continuity in monkey striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  A. Sillito The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. , 1975, The Journal of physiology.

[55]  C. von der Malsburg Self-organization of orientation sensitive cells in the striate cortex. , 1973, Kybernetik.

[56]  A. Sillito,et al.  Modulatory and inhibitory processes in the visual cortex , 1985, Vision Research.

[57]  Roman Bek,et al.  Discourse on one way in which a quantum-mechanics language on the classical logical base can be built up , 1978, Kybernetika.

[58]  I. Ohzawa,et al.  Local intracortical connections in the cat's visual cortex: postnatal development and plasticity. , 1994, Journal of neurophysiology.

[59]  L. Palmer,et al.  Receptive-field structure in cat striate cortex. , 1981, Journal of neurophysiology.

[60]  D. Hubel,et al.  The pattern of ocular dominance columns in macaque visual cortex revealed by a reduced silver stain , 1975, The Journal of comparative neurology.

[61]  E. Callaway,et al.  Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[62]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[63]  田中 啓治,et al.  Cross-correlation analysis of geniculostriate neuronal relationships in cats , 1983 .

[64]  Gregory C. DeAngelis,et al.  Depth is encoded in the visual cortex by a specialized receptive field structure , 1991, Nature.

[65]  K. Miller,et al.  Ocular dominance column development: analysis and simulation. , 1989, Science.

[66]  S. Levay,et al.  Ocular dominance columns and their development in layer IV of the cat's visual cortex: A quantitative study , 1978, The Journal of comparative neurology.

[67]  N. Swindale,et al.  A model for the formation of orientation columns , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[68]  A. Sillito Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. , 1979, The Journal of physiology.

[69]  T. Wiesel,et al.  Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  K. Miller Development of orientation columns via competition between ON- and OFF-center inputs. , 1992, Neuroreport.

[71]  W. Singer Neuronal Activity as a Shaping Factor in the Self-Organization of Neuron Assemblies , 1983 .

[72]  G. Francis Cortical dynamics of visual persistence and temporal integration , 1996, Perception & psychophysics.

[73]  E. Callaway,et al.  Emergence and refinement of clustered horizontal connections in cat striate cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[75]  D. Hubel,et al.  Plasticity of ocular dominance columns in monkey striate cortex. , 1977, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[76]  S. Grossberg,et al.  Texture segregation, surface representation and figure–ground separation , 1998, Vision Research.

[77]  H. Spitzer,et al.  A complex-cell receptive-field model. , 1985, Journal of neurophysiology.

[78]  Ennio Mingolla,et al.  Neural dynamics of perceptual grouping: Textures, boundaries, and emergent segmentations , 1985 .

[79]  D. Hubel,et al.  Sequence regularity and geometry of orientation columns in the monkey striate cortex , 1974, The Journal of comparative neurology.

[80]  S. Grossberg,et al.  Cortical dynamics of form and motion integration: Persistence, apparent motion, and illusory contours , 1996, Vision Research.

[81]  G. Francis Cortical dynamics of lateral inhibition: Visual persistence and ISI , 1996, Perception & psychophysics.

[82]  D. Pollen,et al.  Phase relationships between adjacent simple cells in the visual cortex. , 1981, Science.

[83]  R. C. Van Sluyters,et al.  The overall pattern of ocular dominance bands in cat visual cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[84]  D. Hubel,et al.  Anatomical demonstration of orientation columns in macaque monkey , 1978, The Journal of comparative neurology.

[85]  S. Grossberg,et al.  Cortical Dynamics of Boundary Segmentation and Reset: Persistence, Afterimages, and Residual Traces , 1996, Perception.

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

[87]  Alan N. Gove,et al.  Brightness perception, illusory contours, and corticogeniculate feedback , 1995, Visual Neuroscience.

[88]  K. Obermayer,et al.  Geometry of orientation and ocular dominance columns in monkey striate cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[89]  J. Stone,et al.  Conduction velocity of afferents to cat visual cortex: a correlation with cortical receptive field properties. , 1971, Brain research.

[90]  E. L. Schwartz,et al.  A parametric model for synthesis of cortical column patterns , 1989, International 1989 Joint Conference on Neural Networks.

[91]  S. Grossberg Contour Enhancement , Short Term Memory , and Constancies in Reverberating Neural Networks , 1973 .

[92]  P. H. Schiller Central connections of the retinal ON and OFF pathways , 1982, Nature.

[93]  T. Kohonen Self-organized formation of topographically correct feature maps , 1982 .

[94]  Trichur Raman Vidyasagar,et al.  Excitation and inhibition in orientation selectivity of cat visual cortex neurons revealed by whole-cell recordings in vivo , 1993, Visual Neuroscience.

[95]  D. Hocking,et al.  An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[96]  D. Pollen,et al.  Interneuronal interaction between members of quadrature phase and anti-phase pairs in the cat's visual cortex , 1992, Vision Research.

[97]  R Linsker,et al.  From basic network principles to neural architecture: emergence of orientation-selective cells. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[98]  J. Beck,et al.  Contrast and spatial variables in texture segregation: Testing a simple spatial-frequency channels model , 1989, Perception & psychophysics.

[99]  S. Levay,et al.  The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[100]  G Sperling,et al.  Two motion perception mechanisms revealed through distance-driven reversal of apparent motion. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[101]  R Linsker,et al.  From basic network principles to neural architecture: emergence of orientation columns. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[102]  Stephen Grossberg,et al.  A Neural Theory of Punishment and Avoidance, II: Quantitative Theory , 1972 .

[103]  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.