Invariant computations in local cortical networks with balanced excitation and inhibition

Cortical computations critically involve local neuronal circuits. The computations are often invariant across a cortical area yet are carried out by networks that can vary widely within an area according to its functional architecture. Here we demonstrate a mechanism by which orientation selectivity is computed invariantly in cat primary visual cortex across an orientation preference map that provides a wide diversity of local circuits. Visually evoked excitatory and inhibitory synaptic conductances are balanced exquisitely in cortical neurons and thus keep the spike response sharply tuned at all map locations. This functional balance derives from spatially isotropic local connectivity of both excitatory and inhibitory cells. Modeling results demonstrate that such covariation is a signature of recurrent rather than purely feed-forward processing and that the observed isotropic local circuit is sufficient to generate invariant spike tuning.

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

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

[3]  H. Sompolinsky,et al.  Theory of orientation tuning in visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[4]  C. Koch,et al.  Modeling direction selectivity of simple cells in striate visual cortex within the framework of the canonical microcircuit , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[6]  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.

[7]  T Bonhoeffer,et al.  Orientation selectivity in pinwheel centers in cat striate cortex. , 1997, Science.

[8]  U. Eysel,et al.  GABA-induced inactivation of functionally characterized sites in cat striate cortex: Effects on orientation tuning and direction selectivity , 1997, Visual Neuroscience.

[9]  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.

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

[11]  Nicholas J. Priebe,et al.  Contrast-Invariant Orientation Tuning in Cat Visual Cortex: Thalamocortical Input Tuning and Correlation-Based Intracortical Connectivity , 1998, The Journal of Neuroscience.

[12]  Y. Frégnac,et al.  Visual input evokes transient and strong shunting inhibition in visual cortical neurons , 1998, Nature.

[13]  C. Gilbert,et al.  Topography of contextual modulations mediated by short-range interactions in primary visual cortex , 1999, Nature.

[14]  M. Carandini,et al.  Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. , 2000, Journal of neurophysiology.

[15]  R. Shapley,et al.  A neuronal network model of macaque primary visual cortex (V1): orientation selectivity and dynamics in the input layer 4Calpha. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[16]  M. Carandini,et al.  Membrane Potential and Firing Rate in Cat Primary Visual Cortex , 2000, The Journal of Neuroscience.

[17]  M. Volgushev,et al.  Comparison of the selectivity of postsynaptic potentials and spike responses in cat visual cortex , 2000, The European journal of neuroscience.

[18]  D. Ferster,et al.  Neural mechanisms of orientation selectivity in the visual cortex. , 2000, Annual review of neuroscience.

[19]  Y. Dan,et al.  Stimulus Timing-Dependent Plasticity in Cortical Processing of Orientation , 2001, Neuron.

[20]  T. Sejnowski,et al.  Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons , 2001, Neuroscience.

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

[22]  Michael Shelley,et al.  How Simple Cells Are Made in a Nonlinear Network Model of the Visual Cortex , 2001, The Journal of Neuroscience.

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

[24]  D. Ferster,et al.  Prediction of Orientation Selectivity from Receptive Field Architecture in Simple Cells of Cat Visual Cortex , 2001, Neuron.

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

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

[27]  P. H. Schiller,et al.  Spatial frequency and orientation tuning dynamics in area V1 , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[28]  R Clay Reid,et al.  Laminar processing of stimulus orientation in cat visual cortex , 2002, The Journal of physiology.

[29]  R. Shapley,et al.  Suppression of neural responses to nonoptimal stimuli correlates with tuning selectivity in macaque V1. , 2002, Journal of neurophysiology.

[30]  Niraj S. Desai,et al.  Critical periods for experience-dependent synaptic scaling in visual cortex , 2002, Nature Neuroscience.

[31]  A. Grinvald,et al.  Dynamics and Constancy in Cortical Spatiotemporal Patterns of Orientation Processing , 2002, Science.

[32]  Luis M Martinez,et al.  Synaptic physiology of the flow of information in the cat's visual cortex in vivo , 2002, The Journal of physiology.

[33]  B. Roerig,et al.  Relationships of local inhibitory and excitatory circuits to orientation preference maps in ferret visual cortex. , 2002, Cerebral cortex.

[34]  K. Martin.  Microcircuits in visual cortex , 2002, Current Opinion in Neurobiology.

[35]  E. Miller,et al.  Dynamics of neuronal sensitivity in visual cortex and local feature discrimination , 2002, Nature Neuroscience.

[36]  K. Miller,et al.  Different Roles for Simple-Cell and Complex-Cell Inhibition in V1 , 2003, The Journal of Neuroscience.

[37]  Li I. Zhang,et al.  Topography and synaptic shaping of direction selectivity in primary auditory cortex , 2003, Nature.

[38]  Lyle J. Graham,et al.  Orientation and Direction Selectivity of Synaptic Inputs in Visual Cortical Neurons A Diversity of Combinations Produces Spike Tuning , 2003, Neuron.

[39]  A. Zador,et al.  Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex , 2003, Nature.

[40]  Maxim Volgushev,et al.  γ‐Frequency fluctuations of the membrane potential and response selectivity in visual cortical neurons , 2003, The European journal of neuroscience.

[41]  C. Gray,et al.  Adaptive Coincidence Detection and Dynamic Gain Control in Visual Cortical Neurons In Vivo , 2003, Neuron.

[42]  R. Shapley,et al.  Dynamics of Orientation Selectivity in the Primary Visual Cortex and the Importance of Cortical Inhibition , 2003, Neuron.

[43]  Jose-Manuel Alonso,et al.  Functionally distinct inhibitory neurons at the first stage of visual cortical processing , 2003, Nature Neuroscience.

[44]  M. Fagiolini,et al.  Excitatory-Inhibitory Balance Controls Critical Period Plasticity , 2003 .

[45]  Guosong Liu,et al.  Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites , 2004, Nature Neuroscience.

[46]  David Fitzpatrick,et al.  A morphological basis for orientation tuning in primary visual cortex , 2004, Nature Neuroscience.

[47]  S. Nelson,et al.  Homeostatic plasticity in the developing nervous system , 2004, Nature Reviews Neuroscience.

[48]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[49]  Mriganka Sur,et al.  PLASTICITY OF ORIENTATION PROCESSING IN ADULT VISUAL CORTEX , 2004 .

[50]  Stephen R. Williams,et al.  Spatial compartmentalization and functional impact of conductance in pyramidal neurons , 2004, Nature Neuroscience.