Intrinsic connections in tree shrew V1 imply a global to local mapping

The local-global map hypothesis states that locally organized response properties--such as orientation preference--result from visuotopically organized local maps of non-retinotopic response properties. In the tree shrew, the lateral extent of horizontal patchy connections is as much as 80-100% of V1 and is consistent with the length summation property. We argue that neural signals can be transmitted across the entire extent of V1 and this allows the formation of maps at the local scale that are visuotopically organized. We describe mechanisms relevant to the formation of local maps and report modeling results showing the same patterns of horizontal connectivity, and relationships to orientation preference, seen in vivo. The structure of the connectivity that emerges in the simulations reveals a 'hub and spoke' organization. Singularities form the centers of local maps, and linear zones and saddle-points arise as smooth border transitions between maps. These findings are used to present the case for the local-global map hypothesis for tree shrew V1.

[1]  J. B. Levitt,et al.  Relation between patterns of intrinsic lateral connectivity, ocular dominance, and cytochrome oxidase-reactive regions in macaque monkey striate cortex. , 1996, Cerebral cortex.

[2]  T. Wiesel,et al.  Functional architecture of macaque monkey visual cortex , 1977 .

[3]  Geoffrey J. Goodhill,et al.  Topography and ocular dominance: a model exploring positive correlations , 1993, Biological Cybernetics.

[4]  Amiram Grinvald,et al.  Visual cortex maps are optimized for uniform coverage , 2000, Nature Neuroscience.

[5]  Shigeru Tanaka,et al.  Theory of Self-Organization of Cortical Maps , 1988, NIPS.

[6]  Paul D. Bourke,et al.  Synchronous oscillation in the cerebral cortex and object coherence: simulation of basic electrophysiological findings , 2000, Biological Cybernetics.

[7]  G. Blasdel,et al.  Physiological organization of layer 4 in macaque striate cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  C. Malsburg Self-organization of orientation sensitive cells in the striate cortex , 2004, Kybernetik.

[9]  D. Hubel,et al.  Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey , 1981, Nature.

[10]  Prof. Dr. Valentino Braitenberg,et al.  Anatomy of the Cortex , 1991, Studies of Brain Function.

[11]  G. Mitchison,et al.  Long axons within the striate cortex: their distribution, orientation, and patterns of connection. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[12]  G. Orban,et al.  The organization of orientation selectivity throughout macaque visual cortex. , 2002, Cerebral cortex.

[13]  G. Rager,et al.  Synaptogenesis in the primary visual cortex of the tree shrew (Tupaia belangeri) , 1991, The Journal of comparative neurology.

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

[15]  Peter A. Robinson,et al.  Synchronous oscillations in the cerebral cortex , 1998 .

[16]  M. Livingstone Oscillatory firing and interneuronal correlations in squirrel monkey striate cortex. , 1996, Journal of neurophysiology.

[17]  U. Eysel,et al.  Topography of orientation centre connections in the primary visual cortex of the cat , 2001, Neuroreport.

[18]  T. M. Mayhew,et al.  Anatomy of the Cortex: Statistics and Geometry. , 1991 .

[19]  K. Purpura,et al.  Contrast sensitivity and spatial frequency response of primate cortical neurons in and around the cytochrome oxidase blobs , 1995, Vision Research.

[20]  R. Eckhorn,et al.  Functional coupling shows stronger stimulus dependency for fast oscillations than for low‐frequency components in striate cortex of awake monkey , 2000, The European journal of neuroscience.

[21]  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.

[22]  M. Constantine-Paton,et al.  Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. , 1990, Annual review of neuroscience.

[23]  J. Bullier,et al.  Reaching beyond the classical receptive field of V1 neurons: horizontal or feedback axons? , 2003, Journal of Physiology-Paris.

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

[25]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[26]  A. Grinvald,et al.  Long-term voltage-sensitive dye imaging reveals cortical dynamics in behaving monkeys. , 2002, Journal of neurophysiology.

[27]  Vision Research , 1961, Nature.

[28]  G. Blasdel,et al.  Intrinsic connections of macaque striate cortex: axonal projections of cells outside lamina 4C , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  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.

[30]  J. Rauschecker,et al.  Mechanisms of visual plasticity: Hebb synapses, NMDA receptors, and beyond. , 1991, Physiological reviews.

[31]  J. Lund,et al.  Intrinsic laminar lattice connections in primate visual cortex , 1983, The Journal of comparative neurology.

[32]  R. Cans Obituary: Jacques-Yves Cousteau (1910-97) , 1997, Nature.

[33]  V. Bringuier,et al.  Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. , 1999, Science.

[34]  T. Lee Top-down influence in early visual processing: a Bayesian perspective , 2002, Physiology & Behavior.

[35]  D. Fitzpatrick,et al.  Orientation Selectivity and the Arrangement of Horizontal Connections in Tree Shrew Striate Cortex , 1997, The Journal of Neuroscience.

[36]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. III. Color , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  Leonard E. White,et al.  Mapping multiple features in the population response of visual cortex , 2003, Nature.

[38]  W. Singer,et al.  In search of common foundations for cortical computation , 1997, Behavioral and Brain Sciences.

[39]  R. Durbin,et al.  Optimal numberings of an N N array , 1986 .

[40]  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.

[41]  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.

[42]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[43]  G. Innocenti,et al.  The role of pattern vision in the development ofcortico‐cortical connections , 1999, The European journal of neuroscience.

[44]  A. Grinvald,et al.  Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[45]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

[46]  N. Swindale The development of topography in the visual cortex: a review of models. , 1996, Network.

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

[48]  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.

[49]  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.

[50]  Richard Durbin,et al.  An analogue approach to the travelling salesman problem using an elastic net method , 1987, Nature.

[51]  P. Robinson,et al.  Mechanisms of cortical electrical activity and emergence of gamma rhythm. , 2000, Journal of theoretical biology.

[52]  Y. Frégnac,et al.  Temporal covariance of postsynaptic membrane potential and synaptic input--role in synaptic efficacy in visual cortex. , 1993, Progress in brain research.

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

[54]  K. Rockland,et al.  Axon collaterals of meynert cells diverge over large portions of area V1 in the macaque monkey , 2001, The Journal of comparative neurology.

[55]  W. Freeman,et al.  Analysis of spatial patterns of phase in neocortical gamma EEGs in rabbit. , 2000, Journal of neurophysiology.

[56]  R. Eckhorn,et al.  Flexible cortical gamma-band correlations suggest neural principles of visual processing , 2001 .

[57]  James J. Wright EEG simulation: variation of spectral envelope, pulse synchrony and ALMOST EQUAL TO 40 Hz oscillation , 1997, Biol. Cybern..

[58]  J. Lund,et al.  Anatomical substrates for functional columns in macaque monkey primary visual cortex. , 2003, Cerebral cortex.

[59]  Nicholas V. Swindale,et al.  A model for the coordinated development of columnar systems in primate striate cortex , 2004, Biological Cybernetics.

[60]  S. Maier,et al.  Widespread Periodic Intrinsic Connections in the Tree Shrew Visual Cortex , 2005 .

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

[62]  C. L. Chapman,et al.  Toward an integrated continuum model of cerebral dynamics: the cerebral rhythms, synchronous oscillation and cortical stability. , 2001, Bio Systems.

[63]  Eric L. Schwartz,et al.  Computational anatomy and functional architecture of striate cortex: A spatial mapping approach to perceptual coding , 1980, Vision Research.

[64]  D. Fitzpatrick The functional organization of local circuits in visual cortex: insights from the study of tree shrew striate cortex. , 1996, Cerebral cortex.

[65]  M. Stryker,et al.  The Role of Activity in the Development of Long-Range Horizontal Connections in Area 17 of the Ferret , 1996, The Journal of Neuroscience.

[66]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. II. Retinotopic organization , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  James J. Wright,et al.  Spatial eigenmodes and synchronous oscillation: Co-incidence detection in simulated cerebral cortex , 2002, Journal of mathematical biology.

[68]  W. Singer,et al.  Synchronization of oscillatory neuronal responses in cat striate cortex: Temporal properties , 1992, Visual Neuroscience.

[69]  David Fitzpatrick,et al.  Emergent Properties of Layer 2/3 Neurons Reflect the Collinear Arrangement of Horizontal Connections in Tree Shrew Visual Cortex , 2003, The Journal of Neuroscience.

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

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

[72]  J. J. Wright,et al.  EEG simulation: variation of spectral envelope, pulse synchrony and ≈40 Hz oscillation , 1997, Biological Cybernetics.

[73]  Jim Kay,et al.  Activation Functions, Computational Goals, and Learning Rules for Local Processors with Contextual Guidance , 1997, Neural Computation.

[74]  J. Kaas,et al.  Cortical connections of striate and extrastriate visual areas in tree shrews , 1998, The Journal of comparative neurology.

[75]  D. Fitzpatrick,et al.  Spatial coding of position and orientation in primary visual cortex , 2002, Nature Neuroscience.