Functional properties of human primary motor cortex gamma oscillations.

Gamma oscillations in human primary motor cortex (M1) have been described in human electrocorticographic and noninvasive magnetoencephalographic (MEG)/electroencephalographic recordings, yet their functional significance within the sensorimotor system remains unknown. In a set of four MEG experiments described here a number of properties of these oscillations are elucidated. First, gamma oscillations were reliably localized by MEG in M1 and reached peak amplitude 137 ms after electromyographic onset and were not affected by whether movements were cued or self-paced. Gamma oscillations were found to be stronger for larger movements but were absent during the sustained part of isometric movements, with no finger movement or muscle shortening. During repetitive movement sequences gamma oscillations were greater for the first movement of a sequence. Finally, gamma oscillations were absent during passive shortening of the finger compared with active contractions sharing similar kinematic properties demonstrating that M1 oscillations are not simply related to somatosensory feedback. This combined pattern of results is consistent with gamma oscillations playing a role in a relatively late stage of motor control, encoding information related to limb movement rather than to muscle contraction.

[1]  Marie-Claude Hepp-Reymond,et al.  Corticomuscular synchronization with small and large dynamic force output , 2007, BMC Neuroscience.

[2]  W. Singer,et al.  Temporal binding and the neural correlates of sensory awareness , 2001, Trends in Cognitive Sciences.

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

[4]  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.

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

[6]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

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

[8]  T. Kammer,et al.  Phosphene thresholds evoked with single and double TMS pulses , 2010, Clinical Neurophysiology.

[9]  Rajesh P. N. Rao,et al.  Cortical activity during motor execution, motor imagery, and imagery-based online feedback , 2010, Proceedings of the National Academy of Sciences.

[10]  J. Pernier,et al.  Oscillatory γ-Band (30–70 Hz) Activity Induced by a Visual Search Task in Humans , 1997, The Journal of Neuroscience.

[11]  Rajesh P. N. Rao,et al.  Spectral Changes in Cortical Surface Potentials during Motor Movement , 2007, The Journal of Neuroscience.

[12]  Paolo Maria Rossini,et al.  High-gamma band activity of primary hand cortical areas: A sensorimotor feedback efficiency index , 2008, NeuroImage.

[13]  S. P. Levine,et al.  Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement , 2003, Clinical Neurophysiology.

[14]  D. Cheyne,et al.  Three-dimensional localization of SMA activity preceding voluntary movement , 2004, Experimental Brain Research.

[15]  Philippe Kahane,et al.  High gamma frequency oscillatory activity dissociates attention from intention in the human premotor cortex , 2005, NeuroImage.

[16]  Tomoyuki Akiyama,et al.  Cortical gamma‐oscillations modulated by auditory–motor tasks‐intracranial recording in patients with epilepsy , 2010, Human brain mapping.

[17]  Krish D. Singh,et al.  Spatiotemporal frequency tuning of BOLD and gamma band MEG responses compared in primary visual cortex , 2008, NeuroImage.

[18]  C. G. Phillips,et al.  Projection from low-threshold muscle afferents of hand and forearm to area 3a of baboon's cortex. , 1971, The Journal of physiology.

[19]  M. Hallett,et al.  Cerebral structures participating in motor preparation in humans: a positron emission tomography study. , 1996, Journal of neurophysiology.

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

[21]  Andreas Schulze-Bonhage,et al.  Movement related activity in the high gamma range of the human EEG , 2008, NeuroImage.

[22]  Karl J. Friston,et al.  Cortical areas and the selection of movement: a study with positron emission tomography , 1991, Experimental Brain Research.

[23]  G. Barnes,et al.  Statistical flattening of MEG beamformer images , 2003, Human brain mapping.

[24]  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.

[25]  P. Viviani,et al.  Internally driven vs. externally cued movement selection: a study on the timing of brain activity. , 2000, Brain research. Cognitive brain research.

[26]  François Mauguière,et al.  Intracerebral study of gamma rhythm reactivity in the sensorimotor cortex , 2005, The European journal of neuroscience.

[27]  Krish D. Singh,et al.  Functional decoupling of BOLD and gamma‐band amplitudes in human primary visual cortex , 2009, Human brain mapping.

[28]  J. Martinerie,et al.  Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony , 2001, Journal of Neuroscience Methods.

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

[30]  F. Varela,et al.  Neuromagnetic imaging of cortical oscillations accompanying tactile stimulation. , 2003, Brain research. Cognitive brain research.

[31]  William Gaetz,et al.  Neuromagnetic imaging of movement-related cortical oscillations in children and adults: Age predicts post-movement beta rebound , 2010, NeuroImage.

[32]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[33]  A. Engel,et al.  High-frequency activity in human visual cortex is modulated by visual motion strength. , 2007, Cerebral cortex.

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

[35]  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.

[36]  Xiaolin Huo,et al.  Gamma oscillations in the primary motor cortex studied with MEG , 2010, Brain and Development.

[37]  R. N. Lemon,et al.  Short-latency peripheral inputs to thalamic neurones projecting to the motor cortex in the monkey , 1979, Experimental Brain Research.

[38]  Rajesh P. N. Rao,et al.  High gamma mapping using EEG , 2010, NeuroImage.

[39]  Gareth R. Barnes,et al.  Group imaging of task-related changes in cortical synchronisation using nonparametric permutation testing , 2003, NeuroImage.

[40]  Andreas K. Engel,et al.  Buildup of Choice-Predictive Activity in Human Motor Cortex during Perceptual Decision Making , 2009, Current Biology.

[41]  Paul Ferrari,et al.  Self-paced movements induce high-frequency gamma oscillations in primary motor cortex , 2008, NeuroImage.

[42]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[43]  G. Barnes,et al.  Distinct contrast response functions in striate and extra-striate regions of visual cortex revealed with magnetoencephalography (MEG) , 2005, Clinical Neurophysiology.

[44]  Eishi Asano,et al.  Somatosensory-related gamma-, beta- and alpha-augmentation precedes alpha- and beta-attenuation in humans , 2010, Clinical Neurophysiology.

[45]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[46]  François Mauguière,et al.  Relationship between intracerebral gamma oscillations and slow potentials in the human sensorimotor cortex , 2006, The European journal of neuroscience.

[47]  Robert Oostenveld,et al.  Proprioception-Related Evoked Potentials: Origin and Sensitivity to Movement Parameters , 2002, NeuroImage.

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

[49]  D. Cheyne,et al.  Localization of human somatosensory cortex using spatially filtered magnetoencephalography , 2003, Neuroscience Letters.

[50]  E. Fetz,et al.  Decoupling the Cortical Power Spectrum Reveals Real-Time Representation of Individual Finger Movements in Humans , 2009, The Journal of Neuroscience.

[51]  C. Braun,et al.  Hand Movement Direction Decoded from MEG and EEG , 2008, The Journal of Neuroscience.

[52]  萩原 綱一 Oscillatory gamma synchronization binds the primary and secondary somatosensory areas in humans , 2010 .

[53]  William A. MacKay,et al.  Synchronized neuronal oscillations and their role in motor processes , 1997, Trends in Cognitive Sciences.

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

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