Recruitment of local inhibitory networks by horizontal connections in layer 2/3 of ferret visual cortex.

To investigate how neurons in cortical layer 2/3 integrate horizontal inputs arising from widely distributed sites, we combined intracellular recording and voltage-sensitive dye imaging to visualize the spatiotemporal dynamics of neuronal activity evoked by electrical stimulation of multiple sites in visual cortex. Individual stimuli evoked characteristic patterns of optical activity, while delivering stimuli at multiple sites generated interacting patterns in the regions of overlap. We observed that neurons in overlapping regions received convergent horizontal activation that generated nonlinear responses due to the emergence of large inhibitory potentials. The results indicate that co-activation of multiple sets of horizontal connections recruit strong inhibition from local inhibitory networks, causing marked deviations from simple linear integration.

[1]  P. Schwindt,et al.  Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. , 1985, Journal of neurophysiology.

[2]  A Grinvald,et al.  Optical recording of synaptic potentials from processes of single neurons using intracellular potentiometric dyes. , 1987, Biophysical journal.

[3]  J. Hablitz,et al.  EPSPs in rat neocortical neurons in vitro. II. Involvement of N-methyl-D-aspartate receptors in the generation of EPSPs. , 1989, Journal of neurophysiology.

[4]  M Hines,et al.  A program for simulation of nerve equations with branching geometries. , 1989, International journal of bio-medical computing.

[5]  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.

[6]  W. Singer,et al.  The Involvement of N‐Methyl‐D‐Aspartate Receptors in Induction and Maintenance of Long‐Term Potentiation in Rat Visual Cortex , 1990, The European journal of neuroscience.

[7]  R. Douglas,et al.  A functional microcircuit for cat visual cortex. , 1991, The Journal of physiology.

[8]  C. Gilbert,et al.  Synaptic physiology of horizontal connections in the cat's visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  T. Wiesel,et al.  Targets of horizontal connections in macaque primary visual cortex , 1991, The Journal of comparative neurology.

[10]  C. Gilbert Horizontal integration and cortical dynamics , 1992, Neuron.

[11]  J. Deuchars,et al.  Temporal and spatial properties of local circuits in neocortex , 1994, Trends in Neurosciences.

[12]  Peter Somogyi,et al.  Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites , 1994, Nature.

[13]  D. Fitzpatrick,et al.  Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns , 1995, Neuron.

[14]  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.

[15]  O. Prospero-Garcia,et al.  Reliability of Spike Timing in Neocortical Neurons , 1995 .

[16]  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.

[17]  P. Somogyi,et al.  Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons , 1995, Nature.

[18]  G. Orban,et al.  Model circuit of spiking neurons generating directional selectivity in simple cells. , 1996, Journal of neurophysiology.

[19]  J. Deuchars,et al.  Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. , 1996, The Journal of physiology.

[20]  J. Deuchars,et al.  Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. , 1997, Cerebral cortex.

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

[22]  P. Somogyi,et al.  Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. , 1997, The Journal of physiology.

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

[24]  R. Reid,et al.  Synaptic Integration in Striate Cortical Simple Cells , 1998, The Journal of Neuroscience.

[25]  Paul Mineiro,et al.  Analysis of Direction Selectivity Arising from Recurrent Cortical Interactions , 1998, Neural Computation.

[26]  P. Somogyi,et al.  Differentially Interconnected Networks of GABAergic Interneurons in the Visual Cortex of the Cat , 1998, The Journal of Neuroscience.

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

[28]  E. Todorov,et al.  A local circuit approach to understanding integration of long-range inputs in primary visual cortex. , 1998, Cerebral cortex.

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

[30]  R. Shapley,et al.  Contrast's effect on spatial summation by macaque V1 neurons , 1999, Nature Neuroscience.

[31]  S. Hestrin,et al.  A network of fast-spiking cells in the neocortex connected by electrical synapses , 1999, Nature.

[32]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

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

[34]  H. Markram,et al.  Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. , 2000, Science.

[35]  Y Watanabe,et al.  Properties of Horizontal and Vertical Inputs to Pyramidal Cells in the Superficial Layers of the Cat Visual Cortex , 2000, The Journal of Neuroscience.

[36]  L. C. Katz,et al.  Spatiotemporal patterns of excitation and inhibition evoked by the horizontal network in layer 2/3 of ferret visual cortex. , 2003, Journal of neurophysiology.

[37]  Susan R. Barry Neurons In Action: Computer Simulations with NeuroLab , 2004, Journal of Undergraduate Neuroscience Education.