Switching Neuronal Inputs by Differential Modulations of Gamma-Band Phase-Coherence

Receptive fields (RFs) of cortical sensory neurons increase in size along consecutive processing stages. When multiple stimuli are present in a large visual RF, a neuron typically responds to an attended stimulus as if only that stimulus were present. However, the mechanism by which a neuron selectively responds to a subset of its inputs while discarding all others is unknown. Here, we show that neurons can switch between subsets of their afferent inputs by highly specific modulations of interareal gamma-band phase-coherence (PC). We measured local field potentials, single- and multi-unit activity in two male macaque monkeys (Macaca mulatta) performing an attention task. Two small stimuli were placed on a screen; the stimuli were driving separate local V1 populations, while both were driving the same local V4 population. In each trial, we cued one of the two stimuli to be attended. We found that gamma-band PC of the local V4 population with multiple subpopulations of its V1 input was differentially modulated. It was high with the input subpopulation representing the attended stimulus, while simultaneously it was very low between the same V4 population and the other input-providing subpopulation representing the irrelevant stimulus. These differential modulations, which depend on stimulus relevance, were also found in the locking of spikes from V4 neurons to the gamma-band oscillations of the V1 input subpopulations. This rapid, highly specific interareal locking provides neurons with a powerful dynamic routing mechanism to select and process only the currently relevant signals.

[1]  T. Womelsdorf,et al.  Dynamic shifts of visual receptive fields in cortical area MT by spatial attention , 2006, Nature Neuroscience.

[2]  John F. Kalaska,et al.  Faculty Opinions recommendation of Neuronal correlates of a perceptual decision in ventral premotor cortex. , 2004 .

[3]  Stephanie Westendorff,et al.  The Cortical Timeline for Deciding on Reach Motor Goals , 2010, The Journal of Neuroscience.

[4]  W. Singer,et al.  Phase Sensitivity of Synaptic Modifications in Oscillating Cells of Rat Visual Cortex , 2004, The Journal of Neuroscience.

[5]  Bijan Pesaran,et al.  Free choice activates a decision circuit between frontal and parietal cortex , 2008, Nature.

[6]  Annette Witt,et al.  Dynamic Effective Connectivity of Inter-Areal Brain Circuits , 2011, PLoS Comput. Biol..

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

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

[9]  J. Maunsell,et al.  Differences in Gamma Frequencies across Visual Cortex Restrict Their Possible Use in Computation , 2010, Neuron.

[10]  K. Moxon,et al.  Correcting the bias of spike field coherence estimators due to a finite number of spikes. , 2010, Journal of neurophysiology.

[11]  How far can a random walker go , 1992 .

[12]  R. Romo,et al.  Neuronal Correlates of a Perceptual Decision in Ventral Premotor Cortex , 2004, Neuron.

[13]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[14]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[15]  R. Oostenveld,et al.  A MEMS-based flexible multichannel ECoG-electrode array , 2009, Journal of neural engineering.

[16]  D. Tucker,et al.  EEG coherency. I: Statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales. , 1997, Electroencephalography and clinical neurophysiology.

[17]  Andreas K. Kreiter,et al.  How do we model attention-dependent signal routing? , 2006, Neural Networks.

[18]  P. Dayan,et al.  Matching storage and recall: hippocampal spike timing–dependent plasticity and phase response curves , 2005, Nature Neuroscience.

[19]  Robert Desimone,et al.  Cortical connections of area V4 in the macaque. , 2000, Cerebral cortex.

[20]  P König,et al.  Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[21]  W. Freiwald,et al.  Coherent oscillatory activity in monkey area v4 predicts successful allocation of attention. , 2005, Cerebral cortex.

[22]  E. Miller,et al.  Task-specific neural activity in the primate prefrontal cortex. , 2000, Journal of neurophysiology.

[23]  Naoki Masuda,et al.  Selective Population Rate Coding: A Possible Computational Role of Gamma Oscillations in Selective Attention , 2009, Neural Computation.

[24]  M. Abeles,et al.  Multispike train analysis , 1977, Proceedings of the IEEE.

[25]  Nikola T. Markov,et al.  Weight Consistency Specifies Regularities of Macaque Cortical Networks , 2010, Cerebral cortex.

[26]  John H. R. Maunsell,et al.  Attentional modulation of visual motion processing in cortical areas MT and MST , 1996, Nature.

[27]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[28]  Terrence J. Sejnowski,et al.  Mechanisms for Phase Shifting in Cortical Networks and their Role in Communication through Coherence , 2010, Front. Hum. Neurosci..

[29]  I. Lampl,et al.  Subthreshold oscillations of the membrane potential: a functional synchronizing and timing device. , 1993, Journal of neurophysiology.

[30]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[31]  Robert Oostenveld,et al.  Neural Mechanisms of Visual Attention : How Top-Down Feedback Highlights Relevant Locations , 2007 .

[32]  R. Desimone,et al.  Responses of Neurons in Inferior Temporal Cortex during Memory- Guided Visual Search , 1998 .

[33]  R. Eckhorn,et al.  Stimulus-specific fast oscillations at zero phase between visual areas V1 and V2 of awake monkey. , 1994, Neuroreport.

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

[35]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[36]  R. Gattass,et al.  Cortical visual areas in monkeys: location, topography, connections, columns, plasticity and cortical dynamics , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[38]  Louise S. Delicato,et al.  Attention Reduces Stimulus-Driven Gamma Frequency Oscillations and Spike Field Coherence in V1 , 2010, Neuron.

[39]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.