Membrane Potential Dynamics of Spontaneous and Visually Evoked Gamma Activity in V1 of Awake Mice

Cortical gamma activity (30–80 Hz) is believed to play important functions in neural computation and arises from the interplay of parvalbumin-expressing interneurons (PV) and pyramidal cells (PYRs). However, the subthreshold dynamics underlying its emergence in the cortex of awake animals remain unclear. Here, we characterized the intracellular dynamics of PVs and PYRs during spontaneous and visually evoked gamma activity in layers 2/3 of V1 of awake mice using targeted patch-clamp recordings and synchronous local field potentials (LFPs). Strong gamma activity patterned in short bouts (one to three cycles), occurred when PVs and PYRs were depolarizing and entrained their membrane potential dynamics regardless of the presence of visual stimulation. PV firing phase locked unconditionally to gamma activity. However, PYRs only phase locked to visually evoked gamma bouts. Taken together, our results indicate that gamma activity corresponds to short pulses of correlated background synaptic activity synchronizing the output of cortical neurons depending on external sensory drive.

[1]  T. Harkany,et al.  Pyramidal cell communication within local networks in layer 2/3 of rat neocortex , 2003, The Journal of physiology.

[2]  R. Metherate,et al.  Ionic flux contributions to neocortical slow waves and nucleus basalis- mediated activation: whole-cell recordings in vivo , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  D. McCormick,et al.  Rapid Neocortical Dynamics: Cellular and Network Mechanisms , 2009, Neuron.

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

[5]  Simon J. Mitchell,et al.  Direct measurement of somatic voltage clamp errors in central neurons , 2008, Nature Neuroscience.

[6]  Moritz Helmstaedter,et al.  Efficient Recruitment of Layer 2/3 Interneurons by Layer 4 Input in Single Columns of Rat Somatosensory Cortex , 2008, The Journal of Neuroscience.

[7]  Kenneth D. Harris,et al.  Laminar-dependent effects of cortical state on auditory cortical spontaneous activity , 2012, Front. Neural Circuits.

[8]  Alain Destexhe,et al.  Neuronal Computations with Stochastic Network States , 2006, Science.

[9]  H. Kennedy,et al.  Visual Areas Exert Feedforward and Feedback Influences through Distinct Frequency Channels , 2014, Neuron.

[10]  Martin Vinck,et al.  Improved measures of phase-coupling between spikes and the Local Field Potential , 2011, Journal of Computational Neuroscience.

[11]  M. Steriade,et al.  A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  T. Sejnowski,et al.  Cortical Enlightenment: Are Attentional Gamma Oscillations Driven by ING or PING? , 2009, Neuron.

[13]  R. Desimone,et al.  Laminar differences in gamma and alpha coherence in the ventral stream , 2011, Proceedings of the National Academy of Sciences.

[14]  M. Carandini,et al.  Parvalbumin-Expressing Interneurons Linearly Transform Cortical Responses to Visual Stimuli , 2012, Neuron.

[15]  C. Pennartz,et al.  Functions of gamma‐band synchronization in cognition: from single circuits to functional diversity across cortical and subcortical systems , 2014, The European journal of neuroscience.

[16]  David A. Lewis,et al.  Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia , 2012, Trends in Neurosciences.

[17]  Maria V. Sanchez-Vives,et al.  Lack of orientation and direction selectivity in a subgroup of fast-spiking inhibitory interneurons: cellular and synaptic mechanisms and comparison with other electrophysiological cell types. , 2008, Cerebral cortex.

[18]  J. Poulet,et al.  Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice , 2008, Nature.

[19]  C. Petersen,et al.  Membrane Potential Dynamics of GABAergic Neurons in the Barrel Cortex of Behaving Mice , 2010, Neuron.

[20]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[21]  H. Adesnik,et al.  Input normalization by global feedforward inhibition expands cortical dynamic range , 2009, Nature Neuroscience.

[22]  P. Roelfsema,et al.  Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex , 2014, Proceedings of the National Academy of Sciences.

[23]  R. Sherwin,et al.  From artificial cerebro-spinal fluid (aCSF) to artificial extracellular fluid (aECF): microdialysis perfusate composition effects on in vivo brain ECF glucose measurements , 2004, Journal of Neuroscience Methods.

[24]  Jason C. Wester,et al.  Columnar Interactions Determine Horizontal Propagation of Recurrent Network Activity in Neocortex , 2012, The Journal of Neuroscience.

[25]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[26]  Ulf Knoblich,et al.  What do We Gain from Gamma? Local Dynamic Gain Modulation Drives Enhanced Efficacy and Efficiency of Signal Transmission , 2010, Front. Hum. Neurosci..

[27]  Martin Vinck,et al.  The pairwise phase consistency: A bias-free measure of rhythmic neuronal synchronization , 2010, NeuroImage.

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

[29]  Dominique L. Pritchett,et al.  For things needing your attention: the role of neocortical gamma in sensory perception , 2015, Current Opinion in Neurobiology.

[30]  Maria V. Sanchez-Vives,et al.  Cellular and network mechanisms of rhythmic recurrent activity in neocortex , 2000, Nature Neuroscience.

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

[32]  A. Kohn,et al.  Gamma and the Coordination of Spiking Activity in Early Visual Cortex , 2013, Neuron.

[33]  M. Scanziani,et al.  Equalizing Excitation-Inhibition Ratios across Visual Cortical Neurons , 2014, Nature.

[34]  R. Douglas,et al.  A Quantitative Map of the Circuit of Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.

[35]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[36]  R. Reid,et al.  Broadly Tuned Response Properties of Diverse Inhibitory Neuron Subtypes in Mouse Visual Cortex , 2010, Neuron.

[37]  C. Petersen,et al.  The Excitatory Neuronal Network of the C2 Barrel Column in Mouse Primary Somatosensory Cortex , 2009, Neuron.

[38]  Alison L. Barth,et al.  An Embedded Subnetwork of Highly Active Neurons in the Neocortex , 2010, Neuron.

[39]  A. Bruns.  Fourier-, Hilbert- and wavelet-based signal analysis: are they really different approaches? , 2004, Journal of Neuroscience Methods.

[40]  R. Shapley,et al.  Is Gamma-Band Activity in the Local Field Potential of V1 Cortex a “Clock” or Filtered Noise? , 2011, The Journal of Neuroscience.

[41]  J. Maunsell,et al.  Do gamma oscillations play a role in cerebral cortex? , 2015, Trends in Cognitive Sciences.

[42]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.

[43]  M. Steriade,et al.  Natural waking and sleep states: a view from inside neocortical neurons. , 2001, Journal of neurophysiology.

[44]  C. Gray,et al.  Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Martin Vinck,et al.  Attentional Modulation of Cell-Class-Specific Gamma-Band Synchronization in Awake Monkey Area V4 , 2013, Neuron.

[46]  W. Singer,et al.  Orientation selectivity and noise correlation in awake monkey area V1 are modulated by the gamma cycle , 2012, Proceedings of the National Academy of Sciences.

[47]  J. Shao,et al.  A General Theory for Jackknife Variance Estimation , 1989 .

[48]  T. Womelsdorf,et al.  Attentional Stimulus Selection through Selective Synchronization between Monkey Visual Areas , 2012, Neuron.

[49]  P. Fries.  Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[50]  R. Nieuwenhuys.  The neocortex , 1994, Anatomy and Embryology.

[51]  Sylvain Crochet,et al.  Synaptic Computation and Sensory Processing in Neocortical Layer 2/3 , 2013, Neuron.

[52]  David Ferster,et al.  Membrane Potential Synchrony in Primary Visual Cortex during Sensory Stimulation , 2010, Neuron.

[53]  Dominique L. Pritchett,et al.  Gamma-range synchronization of fast-spiking interneurons can enhance detection of tactile stimuli , 2014, Nature Neuroscience.

[54]  D. McCormick,et al.  Inhibitory Postsynaptic Potentials Carry Synchronized Frequency Information in Active Cortical Networks , 2005, Neuron.

[55]  Fiona E. N. LeBeau,et al.  Multiple origins of the cortical gamma rhythm , 2011, Developmental neurobiology.

[56]  Pieter M. Goltstein,et al.  Effects of Isoflurane Anesthesia on Ensemble Patterns of Ca2+ Activity in Mouse V1: Reduced Direction Selectivity Independent of Increased Correlations in Cellular Activity , 2015, PloS one.

[57]  R. Shapley,et al.  Stochastic Generation of Gamma-Band Activity in Primary Visual Cortex of Awake and Anesthetized Monkeys , 2012, The Journal of Neuroscience.

[58]  C. Pennartz,et al.  UvA-DARE ( Digital Academic Repository ) Membrane Potential Dynamics of Spontaneous and Visually Evoked Gamma Activity in V 1 of Awake Mice , 2016 .

[59]  R. Knight,et al.  The functional role of cross-frequency coupling , 2010, Trends in Cognitive Sciences.

[60]  M. Stryker,et al.  Modulation of Visual Responses by Behavioral State in Mouse Visual Cortex , 2010, Neuron.

[61]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

[62]  H. Adesnik,et al.  A neural circuit for spatial summation in visual cortex , 2012, Nature.

[63]  M. Carandini,et al.  Inhibition dominates sensory responses in awake cortex , 2012, Nature.

[64]  W. Singer,et al.  Relation between oscillatory activity and long-range synchronization in cat visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[65]  Martin Vinck,et al.  Arousal and Locomotion Make Distinct Contributions to Cortical Activity Patterns and Visual Encoding , 2014, Neuron.

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

[67]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[68]  M. Scanziani,et al.  Inhibition of Inhibition in Visual Cortex: The Logic of Connections Between Molecularly Distinct Interneurons , 2013, Nature Neuroscience.

[69]  Wolf Singer,et al.  Distributed processing and temporal codes in neuronal networks , 2009, Cognitive Neurodynamics.

[70]  Roger D. Traub,et al.  Dual Gamma Rhythm Generators Control Interlaminar Synchrony in Auditory Cortex , 2011, The Journal of Neuroscience.

[71]  P. Golshani,et al.  Cellular mechanisms of brain-state-dependent gain modulation in visual cortex , 2013, Nature Neuroscience.

[72]  J. Lynch,et al.  Liquid junction potentials and small cell effects in patch-clamp analysis , 1991, The Journal of Membrane Biology.

[73]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .