Visual Cortical Gamma-Band Activity During Free Viewing of Natural Images

Gamma-band activity in visual cortex has been implicated in several cognitive operations, like perceptual grouping and attentional selection. So far, it has been studied primarily under well-controlled visual fixation conditions and using well-controlled stimuli, like isolated bars or patches of grating. If gamma-band activity is to subserve its purported functions outside of the laboratory, it should be present during natural viewing conditions. We recorded neuronal activity with a 252-channel electrocorticographic (ECoG) grid covering large parts of the left hemisphere of 2 macaque monkeys, while they freely viewed natural images. We found that natural viewing led to pronounced gamma-band activity in the visual cortex. In area V1, gamma-band activity during natural viewing showed a clear spectral peak indicative of oscillatory activity between 50 and 80 Hz and was highly significant for each of 65 natural images. Across the ECoG grid, gamma-band activity during natural viewing was present over most of the recorded visual cortex and absent over most remaining cortex. After saccades, the gamma peak frequency slid down to 30–40 Hz at around 80 ms postsaccade, after which the sustained 50- to 80-Hz gamma-band activity resumed. We propose that gamma-band activity plays an important role during natural viewing.

[1]  Robert Oostenveld,et al.  Visually induced gamma-band activity predicts speed of change detection in humans , 2010, NeuroImage.

[2]  R Eckhorn,et al.  Inhibition of sustained gamma oscillations (35-80 Hz) by fast transient responses in cat visual cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[3]  W. Singer,et al.  Gamma-Phase Shifting in Awake Monkey Visual Cortex , 2010, The Journal of Neuroscience.

[4]  M. Livingstone Oscillatory firing and interneuronal correlations in squirrel monkey striate cortex. , 1996, Journal of neurophysiology.

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

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

[7]  Robert Desimone,et al.  Parallel and Serial Neural Mechanisms for Visual Search in Macaque Area V4 , 2005, Science.

[8]  Andreas K. Engel,et al.  Conditions of perceptual selection and suppression during interocular rivalry in strabismic and normal cats , 2001, Vision Research.

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

[10]  W. Singer,et al.  Synchronization Dynamics in Response to Plaid Stimuli in Monkey V1 , 2009, Cerebral cortex.

[11]  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.

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

[13]  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.

[14]  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.

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

[16]  Rodrigo F. Salazar,et al.  Responses to natural scenes in cat V1. , 2003, Journal of neurophysiology.

[17]  Pascal Fries,et al.  A Microsaccadic Rhythm Modulates Gamma-Band Synchronization and Behavior , 2009, The Journal of Neuroscience.

[18]  Jeffrey G. Ojemann,et al.  Power-Law Scaling in the Brain Surface Electric Potential , 2009, PLoS Comput. Biol..

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

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

[21]  David A. Leopold,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

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

[23]  Sunita Mandon,et al.  Switching Neuronal Inputs by Differential Modulations of Gamma-Band Phase-Coherence , 2012, The Journal of Neuroscience.

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

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

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

[27]  A. Thiele,et al.  Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1 , 2008, The European journal of neuroscience.

[28]  R. Oostenveld,et al.  Tactile Spatial Attention Enhances Gamma-Band Activity in Somatosensory Cortex and Reduces Low-Frequency Activity in Parieto-Occipital Areas , 2006, The Journal of Neuroscience.

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

[30]  P. Fries,et al.  Robust Gamma Coherence between Macaque V1 and V2 by Dynamic Frequency Matching , 2013, Neuron.

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

[32]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[33]  Chun-I Yeh,et al.  Laminar analysis of visually evoked activity in the primary visual cortex , 2012, Proceedings of the National Academy of Sciences.

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

[35]  W. Singer,et al.  Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  Wolf Singer,et al.  Features of neuronal synchrony in mouse visual cortex. , 2003, Journal of neurophysiology.

[37]  W. Singer,et al.  Oscillatory Neuronal Synchronization in Primary Visual Cortex as a Correlate of Stimulus Selection , 2002, The Journal of Neuroscience.

[38]  R. Eckhorn,et al.  Contour decouples gamma activity across texture representation in monkey striate cortex. , 2000, Cerebral cortex.

[39]  Sonja Grün,et al.  Saccade-Related Modulations of Neuronal Excitability Support Synchrony of Visually Elicited Spikes , 2011, Cerebral cortex.

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

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

[42]  W. Singer,et al.  Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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