On the operating point of cortical computation

In this paper, we consider a class of network models of Hodgkin-Huxley type neurons arranged according to a biologically plausible two-dimensional topographic orientation preference map, as found in primary visual cortex (V1). We systematically vary the strength of the recurrent excitation and inhibition relative to the strength of the afferent input in order to characterize different operating regimes of the network. We then compare the map-location dependence of the tuning in the networks with different parametrizations with the neuronal tuning measured in cat V1 in vivo. By considering the tuning of neuronal dynamic and state variables, conductances and membrane potential respectively, our quantitative analysis is able to constrain the operating regime of V1: The data provide strong evidence for a network, in which the afferent input is dominated by strong, balanced contributions of recurrent excitation and inhibition, operating in vivo. Interestingly, this recurrent regime is close to a regime of "instability", characterized by strong, self-sustained activity. The firing rate of neurons in the best-fitting model network is therefore particularly sensitive to small modulations of model parameters, possibly one of the functional benefits of this particular operating regime.

[1]  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.

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

[3]  Nicholas V. Swindale,et al.  Orientation tuning curves: empirical description and estimation of parameters , 1998, Biological Cybernetics.

[4]  Nils Bertschinger,et al.  Real-Time Computation at the Edge of Chaos in Recurrent Neural Networks , 2004, Neural Computation.

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

[6]  K. Obermayer,et al.  The Role of Feedback in Shaping the Extra-Classical Receptive Field of Cortical Neurons: A Recurrent Network Model , 2006, The Journal of Neuroscience.

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

[8]  P. Dayan,et al.  Space and time in visual context , 2007, Nature Reviews Neuroscience.

[9]  Ning Qian,et al.  Comparison among some models of orientation selectivity. , 2006, Journal of neurophysiology.

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

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

[12]  Carrie J. McAdams,et al.  Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4 , 1999, The Journal of Neuroscience.

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

[14]  O. Kinouchi,et al.  Optimal dynamical range of excitable networks at criticality , 2006, q-bio/0601037.

[15]  A. Destexhe,et al.  Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. , 1999, Journal of neurophysiology.

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

[17]  Christopher G. Langton,et al.  Computation at the edge of chaos: Phase transitions and emergent computation , 1990 .

[18]  H. Sompolinsky,et al.  Mexican hats and pinwheels in visual cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[19]  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.

[20]  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.

[21]  M. Sur,et al.  Invariant computations in local cortical networks with balanced excitation and inhibition , 2005, Nature Neuroscience.

[22]  C. Koch,et al.  Recurrent excitation in neocortical circuits , 1995, Science.

[23]  D. McCormick,et al.  Neocortical Network Activity In Vivo Is Generated through a Dynamic Balance of Excitation and Inhibition , 2006, The Journal of Neuroscience.

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

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

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