Stimulus competition by inhibitory interference

When two stimuli are present in the receptive field of a V4 neuron, the firing rate response is between the weakest and strongest response elicited by each of the stimuli alone. When attention is directed towards the stimulus eliciting the strongest response (preferred stimulus), the response to the pair is increased, whereas the response decreases when attention is directed to the poor stimulus. We reproduced these results in a V4 model neuron. The model suggests that top-down attention biases the competition between V2 columns for control of V4 neurons by changing the relative timing of inhibition rather than by changes in synchrony of interneuron networks.

[1]  勇一 作村,et al.  Biophysics of Computation , 2001 .

[2]  B. Grothe,et al.  Precise inhibition is essential for microsecond interaural time difference coding , 2002, Nature.

[3]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[4]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[5]  J. Tepper,et al.  Inhibitory control of neostriatal projection neurons by GABAergic interneurons , 1999, Nature Neuroscience.

[6]  Wulfram Gerstner,et al.  Population Dynamics of Spiking Neurons: Fast Transients, Asynchronous States, and Locking , 2000, Neural Computation.

[7]  R. Desimone,et al.  Interacting Roles of Attention and Visual Salience in V4 , 2003, Neuron.

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

[9]  T. Moore,et al.  Microstimulation of the frontal eye field and its effects on covert spatial attention. , 2004, Journal of neurophysiology.

[10]  Carson C. Chow,et al.  Synchronization and Oscillatory Dynamics in Heterogeneous, Mutually Inhibited Neurons , 1998, Journal of Computational Neuroscience.

[11]  Katherine M. Armstrong,et al.  Visuomotor Origins of Covert Spatial Attention , 2003, Neuron.

[12]  Joachim Gross The role of neural oscillations in attention: Perspectives for computational models , 2006, Neural Networks.

[13]  Bartlett W. Mel,et al.  Dendritic Compartmentalization Could Underlie Competition and Attentional Biasing of Simultaneous Visual Stimuli , 2000, NIPS.

[14]  E. Niebur,et al.  Modeling the Temporal Dynamics of IT Neurons in Visual Search: A Mechanism for Top-Down Selective Attention , 1996, Journal of Cognitive Neuroscience.

[15]  E. Helfand,et al.  Numerical integration of stochastic differential equations — ii , 1979, The Bell System Technical Journal.

[16]  Brent Doiron,et al.  Subtractive and Divisive Inhibition: Effect of Voltage-Dependent Inhibitory Conductances and Noise , 2001, Neural Computation.

[17]  W. Senn,et al.  Neocortical pyramidal cells respond as integrate-and-fire neurons to in vivo-like input currents. , 2003, Journal of neurophysiology.

[18]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[19]  Kresimir Josic,et al.  The Firing of an Excitable Neuron in the Presence of Stochastic Trains of Strong Synaptic Inputs , 2007, Neural Computation.

[20]  J. J. Hopfield,et al.  Pattern recognition computation using action potential timing for stimulus representation , 1995, Nature.

[21]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.

[22]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[23]  P. Mitra,et al.  Analysis of dynamic brain imaging data. , 1998, Biophysical journal.

[24]  G. Buzsáki,et al.  Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks , 1995, Current Opinion in Neurobiology.

[25]  Nancy Kopell,et al.  Synchronization in Networks of Excitatory and Inhibitory Neurons with Sparse, Random Connectivity , 2003, Neural Computation.

[26]  W. Senn,et al.  Top-down dendritic input increases the gain of layer 5 pyramidal neurons. , 2004, Cerebral cortex.

[27]  Ivan Soltesz,et al.  Postsynaptic effects of GABAergic synaptic diversity: regulation of neuronal excitability by changes in IPSC variance , 2002, Neuropharmacology.

[28]  P H Tiesinga,et al.  Robust gamma oscillations in networks of inhibitory hippocampal interneurons , 1999, Network.

[29]  Frances S. Chance,et al.  Gain Modulation from Background Synaptic Input , 2002, Neuron.

[30]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

[31]  T. Sejnowski,et al.  Comparison of current-driven and conductance-driven neocortical model neurons with Hodgkin-Huxley voltage-gated channels. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[32]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Germán Mato,et al.  Synchrony in Heterogeneous Networks of Spiking Neurons , 2000, Neural Computation.

[34]  S. Hestrin,et al.  Spike Transmission and Synchrony Detection in Networks of GABAergic Interneurons , 2001, Science.

[35]  Paul H. E. Tiesinga,et al.  Rapid Temporal Modulation of Synchrony by Competition in Cortical Interneuron Networks , 2004, Neural Computation.

[36]  K. Miller Understanding layer 4 of the cortical circuit: a model based on cat V1. , 2003, Cerebral cortex.

[37]  R. Desimone,et al.  Attention Increases Sensitivity of V4 Neurons , 2000, Neuron.

[38]  R. Desimone Visual attention mediated by biased competition in extrastriate visual cortex. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[39]  S. Prescott,et al.  Gain control of firing rate by shunting inhibition: Roles of synaptic noise and dendritic saturation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Christof Koch,et al.  Shunting Inhibition Does Not Have a Divisive Effect on Firing Rates , 1997, Neural Computation.

[41]  Nancy Kopell,et al.  Gamma Oscillations and Stimulus Selection , 2008, Neural Computation.

[42]  S. Thorpe,et al.  Taking the MAX from neuronal responses , 2003, Trends in Cognitive Sciences.

[43]  R. Desimone,et al.  The Role of Neural Mechanisms of Attention in Solving the Binding Problem , 1999, Neuron.

[44]  G. Deco,et al.  The time course of selective visual attention: theory and experiments , 2002, Vision Research.

[45]  Terrence J. Sejnowski,et al.  Selective attention through phase relationship of excitatory and inhibitory input synchrony in a model cortical neuron , 2006, Neural Networks.

[46]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[47]  M. Frotscher,et al.  Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Jorge V. José,et al.  Inhibitory synchrony as a mechanism for attentional gain modulation , 2004, Journal of Physiology-Paris.

[49]  Katherine M. Armstrong,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2003, Nature.

[50]  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.

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

[52]  John Duncan,et al.  A neural basis for visual search in inferior temporal cortex , 1993, Nature.

[53]  David B. Grayden,et al.  Study of neuronal gain in a conductance-based leaky integrate-and-fire neuron model with balanced excitatory and inhibitory synaptic input , 2003, Biological Cybernetics.

[54]  John H. R. Maunsell,et al.  Attention to both space and feature modulates neuronal responses in macaque area V4. , 2000, Journal of neurophysiology.

[55]  David Golomb,et al.  The Number of Synaptic Inputs and the Synchrony of Large, Sparse Neuronal Networks , 2000, Neural Computation.

[56]  B. Connors,et al.  Synchronous Activity of Inhibitory Networks in Neocortex Requires Electrical Synapses Containing Connexin36 , 2001, Neuron.

[57]  B. Connors,et al.  Two dynamically distinct inhibitory networks in layer 4 of the neocortex. , 2003, Journal of neurophysiology.

[58]  G. Kinney,et al.  Dynamic Influences on Coincidence Detection in Neocortical Pyramidal Neurons , 2004, The Journal of Neuroscience.

[59]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[60]  T. Gawne,et al.  Responses of primate visual cortical V4 neurons to simultaneously presented stimuli. , 2002, Journal of neurophysiology.

[61]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[62]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

[63]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[64]  I. Soltesz,et al.  Modulation of network behaviour by changes in variance in interneuronal properties , 2002, The Journal of physiology.

[65]  J. Movshon,et al.  Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex , 1997, The Journal of Neuroscience.

[66]  R. Silver,et al.  Shunting Inhibition Modulates Neuronal Gain during Synaptic Excitation , 2003, Neuron.

[67]  D. V. van Essen,et al.  Responses in area V4 depend on the spatial relationship between stimulus and attention. , 1996, Journal of neurophysiology.

[68]  Carrie J. McAdams,et al.  Effects of Attention on the Reliability of Individual Neurons in Monkey Visual Cortex , 1999, Neuron.

[69]  P. Tiesinga Stimulus Competition by Inhibitory Interference , 2004, Neural Computation.

[70]  T. Sejnowski,et al.  Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity , 2003, Neuroscience.

[71]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[72]  Jorge V. José,et al.  Synchronization as a mechanism for attentional gain modulation , 2004, Neurocomputing.

[73]  Anthony N. Burkitt Balanced neurons: analysis of leaky integrate-and-fire neurons with reversal potentials , 2001, Biological Cybernetics.

[74]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[75]  T. Sejnowski,et al.  Information transfer in entrained cortical neurons. , 2002, Network.

[76]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[77]  P. Somogyi,et al.  Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons , 2000, Nature Neuroscience.

[78]  Kenneth D Miller,et al.  Multiplicative Gain Changes Are Induced by Excitation or Inhibition Alone , 2003, The Journal of Neuroscience.

[79]  T. Sejnowski,et al.  Impact of Correlated Synaptic Input on Output Firing Rate and Variability in Simple Neuronal Models , 2000, The Journal of Neuroscience.

[80]  Xiao-Jing Wang,et al.  What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. , 2003, Journal of neurophysiology.

[81]  D. Ulrich Differential arithmetic of shunting inhibition for voltage and spike rate in neocortical pyramidal cells , 2003, The European journal of neuroscience.

[82]  B. Connors,et al.  A network of electrically coupled interneurons drives synchronized inhibition in neocortex , 2000, Nature Neuroscience.

[83]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[84]  O. Paulsen,et al.  Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro , 1998, Nature.

[85]  A. Aertsen,et al.  Neuronal Integration of Synaptic Input in the Fluctuation-Driven Regime , 2004, The Journal of Neuroscience.

[86]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.

[87]  Nicolas Brunel,et al.  Dynamics of networks of randomly connected excitatory and inhibitory spiking neurons , 2000, Journal of Physiology-Paris.

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

[89]  Nicolas Brunel,et al.  Dynamics of Sparsely Connected Networks of Excitatory and Inhibitory Spiking Neurons , 2000, Journal of Computational Neuroscience.

[90]  C. Gray,et al.  Stimulus-Dependent Neuronal Oscillations and Local Synchronization in Striate Cortex of the Alert Cat , 1997, The Journal of Neuroscience.