Origins of feature selectivities and maps in the mammalian primary visual cortex

A common feature of the mammalian striate cortex is the arrangement of 'orientation domains' containing neurons preferring similar stimulus orientations. They are arranged as spokes of a pinwheel that converge at singularities known as 'pinwheel centers'. We propose that a cortical network of feedforward and intracortical lateral connections elaborates a full set of optimum orientations from geniculate inputs that show a bias to stimulus orientation and form a set of two or a small number of 'Cartesian' coordinates. Because each geniculate afferent carries signals only from one eye and its receptive field (RF) is either ON or OFF center, the network constructs also ocular dominance columns and a quasi-segregation of ON and OFF responses across the horizontal extent of the striate cortex.

[1]  J D Schall,et al.  Retinal constraints on orientation specificity in cat visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  P. Adorján,et al.  Axonal topography of cortical basket cells in relation to orientation, direction, and ocular dominance maps , 2001, The Journal of comparative neurology.

[3]  K. Albus 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.

[4]  Trichur Raman Vidyasagar,et al.  Receptive field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  Levin Kuhlmann,et al.  A Computational Study of How Orientation Bias in the Lateral Geniculate Nucleus Can Give Rise to Orientation Selectivity in Primary Visual Cortex , 2011, Front. Syst. Neurosci..

[6]  Nuno Maçarico da Costa,et al.  The proportion of synapses formed by the axons of the lateral geniculate nucleus in layer 4 of area 17 of the cat , 2009, The Journal of comparative neurology.

[7]  D. Hubel,et al.  Ferrier lecture - Functional architecture of macaque monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[8]  H Sherk,et al.  Receptive field properties in the cat's area 17 in the absence of on- center geniculate input , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  John H. R. Maunsell,et al.  Functions of the ON and OFF channels of the visual system , 1986, Nature.

[10]  A. Grinvald,et al.  Relationships between orientation-preference pinwheels, cytochrome oxidase blobs, and ocular-dominance columns in primate striate cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Teuvo Kohonen,et al.  Self-organized formation of topologically correct feature maps , 2004, Biological Cybernetics.

[12]  P. Lennie,et al.  Chromatic mechanisms in striate cortex of macaque , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  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.

[14]  P. O. Bishop,et al.  Spatial summation of responses in receptive fields of single cells in cat striate cortex , 1978, Experimental Brain Research.

[15]  Trichur Raman Vidyasagar,et al.  Subcortical orientation biases explain orientation selectivity of visual cortical cells , 2015, Physiological reports.

[16]  M. Sur,et al.  Foci of orientation plasticity in visual cortex , 2001, Nature.

[17]  A. Leventhal,et al.  Relationship between preferred orientation and receptive field position of neurons in cat striate cortex , 1983, The Journal of comparative neurology.

[18]  A. Sillito,et al.  A re-evaluation of the mechanisms underlying simple cell orientation selectivity , 1980, Brain Research.

[19]  M. J. Friedlander,et al.  Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. , 1981, Journal of neurophysiology.

[20]  E J Chichilnisky,et al.  Behavioral / Systems / Cognitive Identification and Characterization of a Y-Like Primate Retinal Ganglion Cell Type , 2007 .

[21]  U. Eysel,et al.  Evidence for a contribution of lateral inhibition to orientation tuning and direction selectivity in cat visual cortex: reversible inactivation of functionally characterized sites combined with neuroanatomical tracing techniques , 1998, The European journal of neuroscience.

[22]  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.

[23]  F. Wörgötter,et al.  Topographical Aspects of Intracortical Excitation and Inhibition Contributing to Orientation Specificity in Area 17 of the Cat Visual Cortex , 1991, The European journal of neuroscience.

[24]  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.

[25]  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.

[26]  Trichur Raman Vidyasagar,et al.  Sparseness of coding in area 17 of the cat visual cortex: A comparison between pinwheel centres and orientation domains , 2012, Neuroscience.

[27]  M. Stryker,et al.  Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  Klaus Obermayer,et al.  The operating regime of local computations in primary visual cortex. , 2009, Cerebral cortex.

[29]  Chun-I Yeh,et al.  On and off domains of geniculate afferents in cat primary visual cortex , 2008, Nature Neuroscience.

[30]  N. Swindale How different feature spaces may be represented in cortical maps , 2004 .

[31]  Trichur Raman Vidyasagar,et al.  Contrast invariance of orientation tuning in the lateral geniculate nucleus of the feline visual system , 2015, The European journal of neuroscience.

[32]  T. Bonhoeffer,et al.  Overrepresentation of horizontal and vertical orientation preferences in developing ferret area 17. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[33]  P. Heggelund Receptive field organization of complex cells in cat striate cortex , 2004, Experimental Brain Research.

[34]  Alessandra Angelucci,et al.  Contribution of feedforward thalamic afferents and corticogeniculate feedback to the spatial summation area of macaque V1 and LGN , 2006, The Journal of comparative neurology.

[35]  O. Creutzfeldt,et al.  An intracellular analysis of visual cortical neurones to moving stimuli: Responses in a co-operative neuronal network , 2004, Experimental Brain Research.

[36]  J. Stone,et al.  The number and distribution of ganglion cells in the cat's retina , 1978, The Journal of comparative neurology.

[37]  W. Levick,et al.  Orientation bias of cat retinal ganglion cells , 1980, Nature.

[38]  Fred Wolf,et al.  Can Retinal Ganglion Cell Dipoles Seed Iso-Orientation Domains in the Visual Cortex? , 2013, PloS one.

[39]  R. Soodak The retinal ganglion cell mosaic defines orientation columns in striate cortex. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Stephen J Eglen,et al.  Parasol cell mosaics are unlikely to drive the formation of structured orientation maps in primary visual cortex. , 2012, Visual neuroscience.

[41]  Sooyoung Chung,et al.  Highly ordered arrangement of single neurons in orientation pinwheels , 2006, Nature.

[42]  P. Heggelund Quantitative studies of enhancement and suppression zones in the receptive field of simple cells in cat striate cortex. , 1986, The Journal of physiology.

[43]  R. Reid,et al.  The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[44]  B. B. Lee,et al.  The retinal input to cells in area 17 of the cat's cortex , 1977, Experimental Brain Research.

[45]  M. Carandini,et al.  Neuronal Selectivity and Local Map Structure in Visual Cortex , 2008, Neuron.

[46]  Fred Wolf,et al.  The pattern of ocular dominance columns in cat primary visual cortex: intra‐ and interindividual variability of column spacing and its dependence on genetic background , 2003, The European journal of neuroscience.

[47]  P. O. Bishop,et al.  Responses to visual contours: spatio‐temporal aspects of excitation in the receptive fields of simple striate neurones , 1971, The Journal of physiology.

[48]  D. Whitteridge,et al.  Innervation of cat visual areas 17 and 18 by physiologically identified X‐ and Y‐ type thalamic afferents. II. Identification of postsynaptic targets by GABA immunocytochemistry and Golgi impregnation , 1985, The Journal of comparative neurology.

[49]  Paul R. Martin,et al.  Cortical-Like Receptive Fields in the Lateral Geniculate Nucleus of Marmoset Monkeys , 2013, The Journal of Neuroscience.

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

[51]  B. Dreher,et al.  Geniculate input to cat visual cortex: a comparison of area 19 with areas 17 and 18. , 1980, Journal of neurophysiology.

[52]  Nicholas J. Priebe,et al.  Orientation Selectivity of Synaptic Input to Neurons in Mouse and Cat Primary Visual Cortex , 2011, The Journal of Neuroscience.

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

[54]  J. Bolz,et al.  Functional specificity of a long-range horizontal connection in cat visual cortex: a cross-correlation study , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  A. B. Bonds,et al.  Are primate lateral geniculate nucleus (LGN) cells really sensitive to orientation or direction? , 2002, Visual Neuroscience.

[56]  A. Leventhal,et al.  Structural basis of orientation sensitivity of cat retinal ganglion cells , 1983, The Journal of comparative neurology.

[57]  R. Douglas,et al.  Stereotypical Bouton Clustering of Individual Neurons in Cat Primary Visual Cortex , 2007, The Journal of Neuroscience.

[58]  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.

[59]  Julie H. Culp,et al.  Transformation of Receptive Field Properties from Lateral Geniculate Nucleus to Superficial V1 in the Tree Shrew , 2013, The Journal of Neuroscience.

[60]  Mriganka Sur,et al.  Synaptic Integration by V1 Neurons Depends on Location within the Orientation Map , 2002, Neuron.

[61]  G. Goodhill Contributions of Theoretical Modeling to the Understanding of Neural Map Development , 2007, Neuron.

[62]  T R Vidyasagar,et al.  Relationship between preferred orientation and ordinal position in neurones of cat striate cortex , 1990, Visual Neuroscience.

[63]  N. Swindale,et al.  How different feature spaces may be represented in cortical maps , 2004, Network.

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

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

[66]  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.

[67]  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.

[68]  Trichur R Vidyasagar,et al.  Role of feedforward geniculate inputs in the generation of orientation selectivity in the cat's primary visual cortex , 2011, The Journal of physiology.

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

[70]  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.

[71]  C. von der Malsburg,et al.  Establishment of a Scaffold for Orientation Maps in Primary Visual Cortex of Higher Mammals , 2008, The Journal of Neuroscience.

[72]  W. Singer,et al.  Development of Orientation Preference Maps in Area 18 of Kitten Visual Cortex , 1997, The European journal of neuroscience.

[73]  M. Sur,et al.  Optically imaged maps of orientation preference in primary visual cortex of cats and ferrets , 1997, The Journal of comparative neurology.

[74]  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.

[75]  Trichur Raman Vidyasagar,et al.  A model of striate response properties based on geniculate anisotropies , 2004, Biological Cybernetics.

[76]  Hongbo Yu,et al.  Global evaluation of contributions of GABAA, AMPA and NMDA receptors to orientation maps in cat's visual cortex , 2008, NeuroImage.

[77]  D. Rose Responses of single units in cat visual cortex to moving bars of light as a function of bar length , 1977, The Journal of physiology.

[78]  Christopher L Passaglia,et al.  Orientation sensitivity of ganglion cells in primate retina , 2002, Vision Research.

[79]  Nicholas J. Priebe,et al.  Mechanisms of Neuronal Computation in Mammalian Visual Cortex , 2012, Neuron.

[80]  Nicholas J. Priebe,et al.  The Emergence of Contrast-Invariant Orientation Tuning in Simple Cells of Cat Visual Cortex , 2007, Neuron.

[81]  U. Eysel,et al.  GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex , 2004, Experimental Brain Research.

[82]  Li I. Zhang,et al.  Linear Transformation of Thalamocortical input by Intracortical Excitation , 2013, Nature Neuroscience.

[83]  Trichur Raman Vidyasagar,et al.  Geniculate orientation biases as cartesian coordinates for cortical orientation detectors. , 1985 .

[84]  D. Ringach,et al.  Retinal origin of orientation maps in visual cortex , 2011, Nature Neuroscience.

[85]  J. Alonso,et al.  COLUMNAR ORGANIZATION OF SPATIAL PHASE IN VISUAL CORTEX , 2014, Nature Neuroscience.

[86]  Trichur Raman Vidyasagar Subcortical mechanisms in orientation sensitivity of cat visual cortical cells , 1992, Neuroreport.

[87]  D. Whitteridge,et al.  An intracellular analysis of the visual responses of neurones in cat visual cortex. , 1991, The Journal of physiology.

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

[89]  Sooyoung Chung,et al.  Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex , 2005, Nature.

[90]  D. Hubel,et al.  Uniformity of monkey striate cortex: A parallel relationship between field size, scatter, and magnification factor , 1974, The Journal of comparative neurology.

[91]  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.

[92]  Peter M. Kaskan,et al.  Intrinsic-Signal Optical Imaging Reveals Cryptic Ocular Dominance Columns in Primary Visual Cortex of New World Owl Monkeys , 2007, Front. Neurosci..

[93]  Edward M. Callaway,et al.  A dedicated circuit linking direction selective retinal ganglion cells to primary visual cortex , 2014, Nature.

[94]  A. Grinvald,et al.  Spatial Relationships among Three Columnar Systems in Cat Area 17 , 1997, The Journal of Neuroscience.

[95]  J. Alonso,et al.  Population receptive fields of ON and OFF thalamic inputs to an orientation column in visual cortex , 2011, Nature Neuroscience.

[96]  J D Schall,et al.  Morphology, central projections, and dendritic field orientation of retinal ganglion cells in the ferret , 1985, The Journal of comparative neurology.

[97]  R. Shapley,et al.  New perspectives on the mechanisms for orientation selectivity , 1997, Current Opinion in Neurobiology.

[98]  U. Eysel,et al.  Orientation-specific relationship between populations of excitatory and inhibitory lateral connections in the visual cortex of the cat. , 1997, Cerebral cortex.

[99]  D. Coppola,et al.  Universality in the Evolution of Orientation Columns in the Visual Cortex , 2010, Science.

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

[101]  K. Albus,et al.  Early post‐natal development of neuronal function in the kitten's visual cortex: a laminar analysis. , 1984, The Journal of physiology.