Pinwheel-dipole configuration in cat early visual cortex

In the early visual cortex, information is processed within functional maps whose layouts are thought to underlie visual perception. However, the precise organization of these functional maps as well as their interrelationships remains largely unknown. Here, we show that spatial frequency representation in cat early visual cortex exhibits singularities around which the map organizes like an electric dipole potential. These singularities are precisely co-located with singularities of the orientation map: the pinwheel centers. To show this, we used high resolution intrinsic optical imaging in cat areas 17 and 18. First, we show that a majority of pinwheel centers exhibit in their neighborhood both semi-global maximum and minimum in the spatial frequency map, contradicting pioneering studies suggesting that pinwheel centers are placed at the locus of a single spatial frequency extremum. Based on an analogy with electromagnetism, we proposed a mathematical model for a dipolar structure, accurately fitting optical imaging data. We conclude that a majority of orientation pinwheel centers form spatial frequency dipoles in cat early visual cortex. Given the functional specificities of neurons at singularities in the visual cortex, it is argued that the dipolar organization of spatial frequency around pinwheel centers could be fundamental for visual processing. ABBREVIATIONS OR Orientation SF Spatial frequency PC Pinwheel center A17 Area 17 A18 Area 18

[1]  Xin Chen,et al.  Functional organization of temporal frequency selectivity in primate visual cortex. , 2008, Cerebral cortex.

[2]  M. Stryker,et al.  Relationship between the Ocular Dominance and Orientation Maps in Visual Cortex of Monocularly Deprived Cats , 1997, Neuron.

[3]  P. O. Bishop,et al.  Some quantitative aspects of the cat's eye: axis and plane of reference, visual field co‐ordinates and optics , 1962, The Journal of physiology.

[4]  Y Matsuda,et al.  Arrangement of orientation pinwheel centers around area 17/18 transition zone in cat visual cortex. , 2000, Cerebral cortex.

[5]  Michael P. Stryker,et al.  New Paradigm for Optical Imaging Temporally Encoded Maps of Intrinsic Signal , 2003, Neuron.

[6]  Ian Nauhaus,et al.  Orthogonal micro-organization of orientation and spatial frequency in primate primary visual cortex , 2012, Nature Neuroscience.

[7]  Nicholas V. Swindale,et al.  Coverage and the design of striate cortex , 1991, Biological Cybernetics.

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

[9]  Klaus Obermayer,et al.  Dynamics of Orientation Tuning in Cat V1 Neurons Depend on Location Within Layers and Orientation Maps , 2007, Front. Neurosci..

[10]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[11]  A. Grinvald,et al.  Optical Imaging of the Layout of Functional Domains in Area 17 and Across the Area 17/18 Border in Cat Visual Cortex , 1995, The European journal of neuroscience.

[12]  I. Ohzawa,et al.  Functional Micro-Organization of Primary Visual Cortex: Receptive Field Analysis of Nearby Neurons , 1999, The Journal of Neuroscience.

[13]  Dezhe Z. Jin,et al.  The Coordinated Mapping of Visual Space and Response Features in Visual Cortex , 2005, Neuron.

[14]  C. Casanova,et al.  Modular organization in area 21a of the cat revealed by optical imaging: comparison with the primary visual cortex , 2009, Neuroscience.

[15]  R. L. de Valois,et al.  Relationship between spatial-frequency and orientation tuning of striate-cortex cells. , 1985, Journal of the Optical Society of America. A, Optics and image science.

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

[17]  A. Grinvald,et al.  Spatio–temporal frequency domains and their relation to cytochrome oxidase staining in cat visual cortex , 1997, Nature.

[18]  M. Stryker,et al.  Spatial Frequency Maps in Cat Visual Cortex , 2000, The Journal of Neuroscience.

[19]  Kenneth D. Miller,et al.  Adaptive filtering enhances information transmission in visual cortex , 2006, Nature.

[20]  Ari Rosenberg,et al.  Models and measurements of functional maps in V1. , 2008, Journal of neurophysiology.

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

[22]  Frédéric Lesage,et al.  Bimodal modulation and continuous stimulation in optical imaging to map direction selectivity , 2010, NeuroImage.

[23]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. , 1978, The Journal of physiology.

[24]  M. Stryker,et al.  The role of visual experience in the development of columns in cat visual cortex. , 1998, Science.

[25]  N. Swindale,et al.  Receptive field and orientation scatter studied by tetrode recordings in cat area 17 , 1999, Visual Neuroscience.

[26]  E. Schwartz,et al.  Physical limits to spatial resolution of optical recording: clarifying the spatial structure of cortical hypercolumns. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Jérôme Ribot,et al.  Parallel development of orientation maps and spatial frequency selectivity in cat visual cortex , 2012, The European journal of neuroscience.

[28]  Jérôme Ribot,et al.  Organization and Origin of Spatial Frequency Maps in Cat Visual Cortex , 2013, The Journal of Neuroscience.

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

[30]  Gopathy Purushothaman,et al.  Quantification of optical images of cortical responses for inferring functional maps. , 2009, Journal of neurophysiology.

[31]  Kai Licha,et al.  Optical imaging. , 2013, Recent results in cancer research. Fortschritte der Krebsforschung. Progres dans les recherches sur le cancer.

[32]  L. Sirovich,et al.  An Optimization Approach to Signal Extraction from Noisy Multivariate Data , 2001, NeuroImage.

[33]  Jonathan Touboul,et al.  Parsimony, Exhaustivity and Balanced Detection in Neocortex , 2014, PLoS Comput. Biol..

[34]  L. Cohen,et al.  Optical monitoring of activity from many areas of the in vitro and in vivo salamander olfactory bulb: a new method for studying functional organization in the vertebrate central nervous system , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  Hirokazu Tanaka,et al.  Online analysis method for intrinsic signal optical imaging , 2006, Journal of Neuroscience Methods.

[36]  M. Volgushev,et al.  Independence of visuotopic representation and orientation map in the visual cortex of the cat , 2003, The European journal of neuroscience.

[37]  Xiangmin Xu,et al.  How do functional maps in primary visual cortex vary with eccentricity? , 2007, The Journal of comparative neurology.

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

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