Gamma-Phase Shifting in Awake Monkey Visual Cortex

Gamma-band synchronization is abundant in nervous systems. Typically, the strength or precision of gamma-band synchronization is studied. However, the precise phase with which individual neurons are synchronized to the gamma-band rhythm might have interesting consequences for their impact on further processing and for spike timing-dependent plasticity. Therefore, we investigated whether the spike times of individual neurons shift systematically in the gamma cycle as a function of the neuronal activation strength. We found that stronger neuronal activation leads to spikes earlier in the gamma cycle, i.e., we observed gamma-phase shifting. Gamma-phase shifting occurred on very rapid timescales. It was particularly pronounced for periods in which gamma-band synchronization was relatively weak and for neurons that were only weakly coupled to the gamma rhythm. We suggest that gamma-phase shifting is brought about by an interplay between overall excitation and gamma-rhythmic synaptic input and has interesting consequences for neuronal coding, competition, and plasticity.

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

[2]  Derek K. Jones,et al.  Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans , 2009, Proceedings of the National Academy of Sciences.

[3]  R. Quiroga,et al.  Extracting information from neuronal populations: information theory and decoding approaches , 2009, Nature Reviews Neuroscience.

[4]  Ernst Niebur,et al.  Effect of Stimulus Intensity on the Spike–Local Field Potential Relationship in the Secondary Somatosensory Cortex , 2008, The Journal of Neuroscience.

[5]  Y. Dan,et al.  Spike timing-dependent plasticity: a Hebbian learning rule. , 2008, Annual review of neuroscience.

[6]  R. Desimone,et al.  The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4 , 2008, The Journal of Neuroscience.

[7]  C. Tallon-Baudry,et al.  Neural Dissociation between Visual Awareness and Spatial Attention , 2008, The Journal of Neuroscience.

[8]  J. O’Neill,et al.  Gamma Oscillatory Firing Reveals Distinct Populations of Pyramidal Cells in the CA1 Region of the Hippocampus , 2008, The Journal of Neuroscience.

[9]  H. Robinson,et al.  Recurrent Synaptic Input and the Timing of Gamma-Frequency-Modulated Firing of Pyramidal Cells during Neocortical “UP” States , 2008, The Journal of Neuroscience.

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

[11]  T. Sejnowski,et al.  Regulation of spike timing in visual cortical circuits , 2008, Nature Reviews Neuroscience.

[12]  W. Singer,et al.  The gamma cycle , 2007, Trends in Neurosciences.

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

[14]  Arne D. Ekstrom,et al.  Brain Oscillations Control Timing of Single-Neuron Activity in Humans , 2007, The Journal of Neuroscience.

[15]  E. Miller,et al.  Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices , 2007, Science.

[16]  Danko Nikolic,et al.  Non-parametric detection of temporal order across pairwise measurements of time delays , 2007, Journal of Computational Neuroscience.

[17]  Danko Nikolic,et al.  Spatiotemporal Structure in Large Neuronal Networks Detected from Cross-Correlation , 2006, Neural Computation.

[18]  Robert Oostenveld,et al.  Localizing human visual gamma-band activity in frequency, time and space , 2006, NeuroImage.

[19]  P. Jonas,et al.  Shunting Inhibition Improves Robustness of Gamma Oscillations in Hippocampal Interneuron Networks by Homogenizing Firing Rates , 2006, Neuron.

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

[21]  S. Epstein,et al.  Background gamma rhythmicity and attention in cortical local circuits: a computational study. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. Schoffelen,et al.  Neuronal Coherence as a Mechanism of Effective Corticospinal Interaction , 2005, Science.

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

[24]  J. Csicsvari,et al.  Mechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat , 2003, Neuron.

[25]  G. Buzsáki,et al.  Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells , 2002, Nature.

[26]  M. R. Mehta,et al.  Role of experience and oscillations in transforming a rate code into a temporal code , 2002, Nature.

[27]  H. Scheich,et al.  Stimulus-related gamma oscillations in primate auditory cortex. , 2002, Journal of neurophysiology.

[28]  G. Buzsáki.  Theta Oscillations in the Hippocampus , 2002, Neuron.

[29]  C. Elger,et al.  Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling , 2001, Nature Neuroscience.

[30]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[31]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[32]  B. Gordon,et al.  Induced electrocorticographic gamma activity during auditory perception , 2001, Clinical Neurophysiology.

[33]  D. Barth,et al.  Cellular mechanisms of thalamically evoked gamma oscillations in auditory cortex. , 2001, Journal of neurophysiology.

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

[35]  C. Gray,et al.  Dynamics of striate cortical activity in the alert macaque: II. Fast time scale synchronization. , 2000, Cerebral cortex.

[36]  C. Gray,et al.  Dynamics of striate cortical activity in the alert macaque: I. Incidence and stimulus-dependence of gamma-band neuronal oscillations. , 2000, Cerebral cortex.

[37]  Christo Pantev,et al.  The perception of coherent and non-coherent auditory objects: a signature in gamma frequency band , 2000, Hearing Research.

[38]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[39]  W. Freeman,et al.  Topographic analysis of epidural pure-tone-evoked potentials in gerbil auditory cortex. , 2000, Journal of neurophysiology.

[40]  Roman Bauer,et al.  Fast oscillations display sharper orientation tuning than slower components of the same recordings in striate cortex of the awake monkey , 2000, The European journal of neuroscience.

[41]  R. Eckhorn,et al.  Functional coupling shows stronger stimulus dependency for fast oscillations than for low‐frequency components in striate cortex of awake monkey , 2000, The European journal of neuroscience.

[42]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[43]  S. Cruikshank,et al.  Thalamocortical inputs trigger a propagating envelope of gamma-band activity in auditory cortex in vitro , 1999, Experimental Brain Research.

[44]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[45]  Christoph Braun,et al.  Coherence of gamma-band EEG activity as a basis for associative learning , 1999, Nature.

[46]  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.

[47]  E. G. Jones,et al.  Tonotopic organization of auditory cortical fields delineated by parvalbumin immunoreactivity in macaque monkeys , 1997, The Journal of comparative neurology.

[48]  M. Steriade,et al.  Instrumental conditioning of fast (20- to 50-Hz) oscillations in corticothalamic networks. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[50]  G. Laurent,et al.  Odour encoding by temporal sequences of firing in oscillating neural assemblies , 1996, Nature.

[51]  D. Barth,et al.  Thalamic modulation of high-frequency oscillating potentials in auditory cortex , 1996, Nature.

[52]  G. Pfurtscheller,et al.  Human cortical 40 Hz rhythm is closely related to EMG rhythmicity , 1996, Neuroscience Letters.

[53]  L. Marshall,et al.  Event-related gamma band activity during passive and active oddball tasks. , 1996, Neuroreport.

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

[55]  Pieter R. Roelfsema,et al.  How Precise is Neuronal Synchronization? , 1995, Neural Computation.

[56]  G. Buzsáki,et al.  Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  R. Eckhorn,et al.  Synchronous High‐frequency Oscillations in Cat Area 18 , 1995, The European journal of neuroscience.

[58]  R. Llinás,et al.  Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[59]  R. Näätänen,et al.  Long-term stimulation attenuates the transient 40-Hz response. , 1994, Neuroreport.

[60]  F. de Ribaupierre,et al.  Changes of single unit activity in the cat's auditory thalamus and cortex associated to different anesthetic conditions , 1994, Neuroscience Research.

[61]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

[62]  K. Reinikainen,et al.  Selective attention enhances the auditory 40-Hz transient response in humans , 1993, Nature.

[63]  R. Llinás,et al.  Coherent 40-Hz oscillation characterizes dream state in humans. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[64]  Alan J. Lee,et al.  Regression Models for an Angular Response , 1992 .

[65]  Gerald Langner,et al.  Periodicity coding in the auditory system , 1992, Hearing Research.

[66]  S Makeig,et al.  Human auditory evoked gamma-band magnetic fields. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[67]  W. Singer,et al.  Stimulus‐Dependent Neuronal Oscillations in Cat Visual Cortex: Inter‐Columnar Interaction as Determined by Cross‐Correlation Analysis , 1990, The European journal of neuroscience.

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

[69]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[70]  S. Makeig,et al.  A 40-Hz auditory potential recorded from the human scalp. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[71]  J. Frost.  Comparison of intracellular potentials and ECoG activity in isolated cerebral cortex. , 1967, Electroencephalography and clinical neurophysiology.

[72]  R. Oostenveld,et al.  Finding Gamma , 2008, Neuron.

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

[74]  G. Buzsáki.  Rhythms of the brain , 2006 .

[75]  C. Pantev.  Evoked and induced gamma-band activity of the human cortex , 2005, Brain Topography.

[76]  Reinhard Eckhorn,et al.  Neural mechanisms of scene segmentation: recordings from the visual cortex suggest basic circuits for linking field models , 1999, IEEE Trans. Neural Networks.

[77]  Wolfgang Maass,et al.  Networks of spiking neurons can emulate arbitrary Hopfield nets in temporal coding , 1997 .

[78]  M Steinschneider,et al.  Localization of ERP generators and identification of underlying neural processes. , 1995, Electroencephalography and clinical neurophysiology. Supplement.

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

[80]  J. R. Rosenberg,et al.  The Fourier approach to the identification of functional coupling between neuronal spike trains. , 1989, Progress in biophysics and molecular biology.

[81]  U. Mitzdorf.  Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[82]  Ch. von der Malsburg,et al.  How are Nervous Structures Organized , 1983 .