The properties of induced gamma oscillations in human visual cortex show individual variability in their dependence on stimulus size

The role of gamma-band (typically 30-100 Hz) oscillations in visual processing is a topic of increasing interest. One hypothesis is that gamma oscillations reflect the action of GABAergic inhibitory processes in the visual cortex responsible for surround-suppression. Evidence from primate neurophysiology [Gieselmann & Thiele, A., 2008. European Journal of Neuroscience 28, 447-459.] suggests that the amplitude of the gamma-band response increases as a visual grating stimulus expands outside of the classical receptive field into the inhibitory surround; with the amplitude of the response increasing, and the frequency of the response decreasing, monotonically with stimulus size. In this study, we tested the relationship between the gamma-band response and the size of visual grating stimuli in humans using MEG. In two initial experiments we found that, while the absolute magnitude of the gamma-band response varied considerably across participants, in all cases the amplitude of the response had a monotonically increasing relationship with size. In contrast, we did not find any relationship between the frequency of the response and the size of the stimulus. Previously, the frequency of the visual gamma-band response has been found to correlate across individuals with the surface area of cortical area V1 [Schwarzkopf et al., 2012. Journal of Neuroscience 32, 1507-12.] We, however, were unable to find any correlation between the frequency or the magnitude of the gamma-band response and the dimensions of V1 cortical gray matter as measured from participants' MR images. Consistent with a saturation of the gamma-band response found for some individuals in the first two experiments, in a third experiment we found that the magnitude of the response to our largest stimulus (8°) was less than that predicted from the response to the stimulus' parts.

[1]  Derek K. Jones,et al.  Visual gamma oscillations and evoked responses: Variability, repeatability and structural MRI correlates , 2010, NeuroImage.

[2]  R. Daroff,et al.  Management of Epilepsy , 1997, Neurology.

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

[4]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[5]  Krish D. Singh,et al.  Visual gamma oscillations: The effects of stimulus type, visual field coverage and stimulus motion on MEG and EEG recordings , 2013, NeuroImage.

[6]  Nicolas Brunel,et al.  Author's Personal Copy Understanding the Relationships between Spike Rate and Delta/gamma Frequency Bands of Lfps and Eegs Using a Local Cortical Network Model , 2022 .

[7]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[8]  Se Robinson,et al.  Functional neuroimaging by Synthetic Aperture Magnetometry (SAM) , 1999 .

[9]  D. Schwarzkopf,et al.  The Frequency of Visually Induced Gamma-Band Oscillations Depends on the Size of Early Human Visual Cortex , 2012, The Journal of Neuroscience.

[10]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[11]  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.

[12]  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.

[13]  G. Barnes,et al.  Identifying spatially overlapping local cortical networks with MEG , 2009, Human brain mapping.

[14]  Krish D. Singh,et al.  Orientation Discrimination Performance Is Predicted by GABA Concentration and Gamma Oscillation Frequency in Human Primary Visual Cortex , 2009, The Journal of Neuroscience.

[15]  Anina N. Rich,et al.  Induced and evoked neural correlates of orientation selectivity in human visual cortex , 2011, NeuroImage.

[16]  Suresh D Muthukumaraswamy,et al.  Functional properties of human primary motor cortex gamma oscillations. , 2010, Journal of neurophysiology.

[17]  J. Vrba,et al.  Signal processing in magnetoencephalography. , 2001, Methods.

[18]  R M Leahy,et al.  A sensor-weighted overlapping-sphere head model and exhaustive head model comparison for MEG. , 1999, Physics in medicine and biology.

[19]  M. A. Smith,et al.  Stimulus Selectivity and Spatial Coherence of Gamma Components of the Local Field Potential , 2011, The Journal of Neuroscience.

[20]  K. D. Singh,et al.  Spectral properties of induced and evoked gamma oscillations in human early visual cortex to moving and stationary stimuli. , 2009, Journal of neurophysiology.

[21]  Krish D. Singh,et al.  A new approach to neuroimaging with magnetoencephalography , 2005, Human brain mapping.

[22]  R. Oostenveld,et al.  Neuronal Dynamics Underlying High- and Low-Frequency EEG Oscillations Contribute Independently to the Human BOLD Signal , 2011, Neuron.

[23]  Gareth R. Barnes,et al.  Stimuli of varying spatial scale induce gamma activity with distinct temporal characteristics in human visual cortex , 2007, NeuroImage.

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

[25]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[26]  Gareth R. Barnes,et al.  The missing link: analogous human and primate cortical gamma oscillations , 2005, NeuroImage.

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

[28]  Stefan Debener,et al.  Size matters: effects of stimulus size, duration and eccentricity on the visual gamma-band response , 2004, Clinical Neurophysiology.

[29]  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.

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

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

[32]  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.

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

[34]  Lawrence L. Wald,et al.  Accurate prediction of V1 location from cortical folds in a surface coordinate system , 2008, NeuroImage.

[35]  Arjan Hillebrand,et al.  Retinotopic mapping of the primary visual cortex – a challenge for MEG imaging of the human cortex , 2011, The European journal of neuroscience.

[36]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[37]  J. Bullier,et al.  Cortical mapping of gamma oscillations in areas V1 and V4 of the macaque monkey , 2001, Visual Neuroscience.

[38]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[39]  Krish D. Singh,et al.  Induced visual illusions and gamma oscillations in human primary visual cortex , 2004, The European journal of neuroscience.

[40]  A. Hyvärinen,et al.  Spatial frequency tuning in human retinotopic visual areas. , 2008, Journal of vision.