Optogenetic Assessment of Horizontal Interactions in Primary Visual Cortex

Columnar organization of orientation selectivity and clustered horizontal connections linking orientation columns are two of the distinctive organizational features of primary visual cortex in many mammalian species. However, the functional role of these connections has been harder to characterize. Here we examine the extent and nature of horizontal interactions in V1 of the tree shrew using optical imaging of intrinsic signals, optogenetic stimulation, and multi-unit recording. Surprisingly, we find the effects of optogenetic stimulation depend primarily on distance and not on the specific orientation domains or axes in the cortex, which are stimulated. In addition, across a wide range of variation in both visual and optogenetic stimulation we find linear addition of the two inputs. These results emphasize that the cortex provides a rich substrate for functional interactions that are not limited to the orientation-specific interactions predicted by the monosynaptic distribution of horizontal connections.

[1]  B. Zemelman,et al.  The columnar and laminar organization of inhibitory connections to neocortical excitatory cells , 2010, Nature Neuroscience.

[2]  K. Svoboda,et al.  Channelrhodopsin-2–assisted circuit mapping of long-range callosal projections , 2007, Nature Neuroscience.

[3]  D. V. van Essen,et al.  Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. , 1992, Journal of neurophysiology.

[4]  Sean P. MacEvoy,et al.  A precise form of divisive suppression supports population coding in primary visual cortex , 2009, Nature Neuroscience.

[5]  Ian Nauhaus,et al.  Contrast Dependence and Differential Contributions from Somatostatin- and Parvalbumin-Expressing Neurons to Spatial Integration in Mouse V1 , 2013, The Journal of Neuroscience.

[6]  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.

[7]  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.

[8]  K. Svoboda,et al.  The subcellular organization of neocortical excitatory connections , 2009, Nature.

[9]  Heather J. Chisum,et al.  The contribution of vertical and horizontal connections to the receptive field center and surround in V1 , 2004, Neural Networks.

[10]  T. Murphy,et al.  In vivo Large-Scale Cortical Mapping Using Channelrhodopsin-2 Stimulation in Transgenic Mice Reveals Asymmetric and Reciprocal Relationships between Cortical Areas , 2012, Front. Neural Circuits.

[11]  J. Movshon,et al.  Selectivity and spatial distribution of signals from the receptive field surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[12]  E. Callaway.  Local circuits in primary visual cortex of the macaque monkey. , 1998, Annual review of neuroscience.

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

[14]  Shawn R. Olsen,et al.  Gain control by layer six in cortical circuits of vision , 2012, Nature.

[15]  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.

[16]  U. Polat,et al.  The architecture of perceptual spatial interactions , 1994, Vision Research.

[17]  T. Murphy,et al.  Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice , 2009, Nature Methods.

[18]  Jean Bennett,et al.  Lateral Connectivity and Contextual Interactions in Macaque Primary Visual Cortex , 2002, Neuron.

[19]  M. Carandini,et al.  Parvalbumin-Expressing Interneurons Linearly Transform Cortical Responses to Visual Stimuli , 2012, Neuron.

[20]  V. Mountcastle.  The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

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

[22]  J. B. Levitt,et al.  Contrast dependence of contextual effects in primate visual cortex , 1997, nature.

[23]  Ke Chen,et al.  Contrast-dependent variations in the excitatory classical receptive field and suppressive nonclassical receptive field of cat primary visual cortex. , 2013, Cerebral cortex.

[24]  David J. Field,et al.  Contour integration by the human visual system: Evidence for a local “association field” , 1993, Vision Research.

[25]  K. Deisseroth,et al.  Millisecond-timescale, genetically targeted optical control of neural activity , 2005, Nature Neuroscience.

[26]  Cyrille C. Girardin,et al.  Inactivation of lateral connections in cat area 17 , 2009, The European journal of neuroscience.

[27]  T. Wiesel,et al.  Clustered intrinsic connections in cat visual cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  Karl Deisseroth,et al.  Optogenetics in Neural Systems , 2011, Neuron.

[29]  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.

[30]  Lief E. Fenno,et al.  The development and application of optogenetics. , 2011, Annual review of neuroscience.

[31]  U. Polat,et al.  Collinear stimuli regulate visual responses depending on cell's contrast threshold , 1998, Nature.

[32]  J. Movshon,et al.  Time Course and Time-Distance Relationships for Surround Suppression in Macaque V1 Neurons , 2003, The Journal of Neuroscience.

[33]  H. Adesnik,et al.  Lateral competition for cortical space by layer-specific horizontal circuits , 2010, Nature.

[34]  G Westheimer,et al.  Dynamics of spatial summation in primary visual cortex of alert monkeys. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Hamutal Slovin,et al.  Population response to contextual influences in the primary visual cortex. , 2010, Cerebral cortex.

[36]  C. Gilbert,et al.  Improvement in visual sensitivity by changes in local context: Parallel studies in human observers and in V1 of alert monkeys , 1995, Neuron.

[37]  Yoshio Maruyama,et al.  Transcranial optogenetic stimulation for functional mapping of the motor cortex , 2009, Journal of Neuroscience Methods.

[38]  Karl Deisseroth,et al.  Activation of Specific Interneurons Improves V1 Feature Selectivity and Visual Perception , 2012, Nature.

[39]  A. B. Bonds.  Role of Inhibition in the Specification of Orientation Selectivity of Cells in the Cat Striate Cortex , 1989, Visual Neuroscience.

[40]  W H Bosking,et al.  Functional Specificity of Callosal Connections in Tree Shrew Striate Cortex , 2000, The Journal of Neuroscience.

[41]  A. L. Humphrey,et al.  Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis) , 1982, The Journal of comparative neurology.

[42]  Karel Svoboda,et al.  Long-Range Neuronal Circuits Underlying the Interaction between Sensory and Motor Cortex , 2011, Neuron.

[43]  W. C. Hall,et al.  High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice , 2007, Proceedings of the National Academy of Sciences.

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

[45]  D. Burr,et al.  Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[46]  Vernon B Mountcastle,et al.  Introduction. Computation in cortical columns. , 2003, Cerebral cortex.

[47]  L. Martinez,et al.  Circuits that build visual cortical receptive fields , 2006, Trends in Neurosciences.

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

[49]  H. Adesnik,et al.  A neural circuit for spatial summation in visual cortex , 2012, Nature.

[50]  Timothy H. Murphy,et al.  Distinct Cortical Circuit Mechanisms for Complex Forelimb Movement and Motor Map Topography , 2012, Neuron.

[51]  Nathan R. Wilson,et al.  Division and subtraction by distinct cortical inhibitory networks in vivo , 2012, Nature.

[52]  J. Movshon,et al.  Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[53]  Jason C. Wester,et al.  Columnar Interactions Determine Horizontal Propagation of Recurrent Network Activity in Neocortex , 2012, The Journal of Neuroscience.