The functional role of post-movement beta oscillations in motor termination

Shortly after movement termination, there is a strong increase or resynchronization of the beta rhythm (15–30 Hz) across the sensorimotor network of humans, known as the post-movement beta rebound (PMBR). This response has been associated with active inhibition of the motor network following the completion of a movement, sensory afferentation of the sensorimotor cortices, and other functions. However, studies that have directly probed the role of the PMBR in movement execution have reported mixed results, possibly due to differences in the amount of total motor output and/or movement complexity. Herein, we used magnetoencephalography during an isometric-force control task to examine whether alterations in the timing of motor termination demands modulate the PMBR, independent of differences in the motor output itself. Briefly, we manipulated the amount of time between the cue to initiate the force and the cue to terminate the force, such that participants were either forced to terminate quickly or slowly. We also performed a control experiment to test for temporal predictability effects. Our results indicated that the PMBR was stronger immediately following movement termination in the prefrontal cortices, supplementary motor area, left postcentral gyrus, paracentral lobule, and parietal cortex when participants were forced to terminate more quickly. These results were not attributable to the temporal predictability of each condition. These findings support the notion that the PMBR response at least partially serves motor inhibition, independent of the parameters within the motor output itself, and that particular nodes of the motor network may be differentially modulated by motor termination.

[1]  J. Artieda,et al.  Oscillatory changes related to the forced termination of a movement , 2008, Clinical Neurophysiology.

[2]  Satoru Hayasaka,et al.  Oscillatory MEG Motor Activity Reflects Therapy-Related Plasticity in Stroke Patients , 2011, Neurorehabilitation and neural repair.

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

[4]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

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

[6]  Tony W. Wilson,et al.  Is an absolute level of cortical beta suppression required for proper movement? Magnetoencephalographic evidence from healthy aging , 2016, NeuroImage.

[7]  Michael T. Jurkiewicz,et al.  Post-movement beta rebound is generated in motor cortex: Evidence from neuromagnetic recordings , 2006, NeuroImage.

[8]  Tony W Wilson,et al.  Abnormal Gamma and Beta MEG Activity During Finger Movements in Early-Onset Psychosis , 2011, Developmental neuropsychology.

[9]  William Gaetz,et al.  Localization of sensorimotor cortical rhythms induced by tactile stimulation using spatially filtered MEG , 2006, NeuroImage.

[10]  Juha Virtanen,et al.  Activation of multiple cortical areas in response to somatosensory stimulation: Combined magnetoencephalographic and functional magnetic resonance imaging , 1999, Human brain mapping.

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

[12]  G. Pfurtscheller,et al.  Distinction of different fingers by the frequency of stimulus induced beta oscillations in the human EEG , 2001, Neuroscience Letters.

[13]  P. Derambure,et al.  Relationship between event-related beta synchronization and afferent inputs: Analysis of finger movement and peripheral nerve stimulations , 2006, Clinical Neurophysiology.

[14]  M. Alegre,et al.  Imitating versus non-imitating movements: Differences in frontal electroencephalographic oscillatory activity , 2006, Neuroscience Letters.

[15]  Christa Neuper,et al.  Cue-induced beta rebound during withholding of overt and covert foot movement , 2012, Clinical Neurophysiology.

[16]  R. Ilmoniemi,et al.  Signal-space projection method for separating MEG or EEG into components , 1997, Medical and Biological Engineering and Computing.

[17]  A. Leuthold,et al.  Beta-Band Activity during Motor Planning Reflects Response Uncertainty , 2010, The Journal of Neuroscience.

[18]  Tony W. Wilson,et al.  Cue-related Temporal Factors Modulate Movement-related Beta Oscillatory Activity in the Human Motor Circuit , 2016, Journal of Cognitive Neuroscience.

[19]  Tony W. Wilson,et al.  Functional Brain Abnormalities During Finger-Tapping in HIV-Infected Older Adults: A Magnetoencephalography Study , 2013, Journal of Neuroimmune Pharmacology.

[20]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

[21]  H. Shibasaki,et al.  Movement-related change of electrocorticographic activity in human supplementary motor area proper. , 2000, Brain : a journal of neurology.

[22]  P. Derambure,et al.  Post-movement beta synchronization in subjects presenting with sensory deafferentation , 2008, Clinical Neurophysiology.

[23]  G. Pfurtscheller,et al.  Motor imagery activates primary sensorimotor area in humans , 1997, Neuroscience Letters.

[24]  Donald C. Rojas,et al.  An extended motor network generates beta and gamma oscillatory perturbations during development , 2010, Brain and Cognition.

[25]  R. Hari,et al.  Functional Segregation of Movement-Related Rhythmic Activity in the Human Brain , 1995, NeuroImage.

[26]  Tony W Wilson,et al.  Coding complexity in the human motor circuit , 2015, Human brain mapping.

[27]  M. D. Ernst Permutation Methods: A Basis for Exact Inference , 2004 .

[28]  David G. Norris,et al.  Combining EEG and fMRI to investigate the post-movement beta rebound , 2006, NeuroImage.

[29]  G. Pfurtscheller,et al.  Could the beta rebound in the EEG be suitable to realize a “brain switch”? , 2009, Clinical Neurophysiology.

[30]  P. Derambure,et al.  Basic mechanisms of central rhythms reactivity to preparation and execution of a voluntary movement: a stereoelectroencephalographic study , 2003, Clinical Neurophysiology.

[31]  T. Wilson,et al.  The cortical signature of symptom laterality in Parkinson's disease , 2017, NeuroImage: Clinical.

[32]  A. Labarga,et al.  Frontal and central oscillatory changes related to different aspects of the motor process: a study in go/no-go paradigms , 2004, Experimental Brain Research.

[33]  S. Taulu,et al.  Applications of the signal space separation method , 2005, IEEE Transactions on Signal Processing.

[34]  T. Wilson,et al.  Neuromagnetic Evidence of Abnormal Movement-Related Beta Desynchronization in Parkinson's Disease , 2013, Cerebral cortex.

[35]  D. Cheyne,et al.  Spatiotemporal mapping of cortical activity accompanying voluntary movements using an event‐related beamforming approach , 2006, Human brain mapping.

[36]  P. Derambure,et al.  Does post-movement beta synchronization reflect an idling motor cortex? , 2001, Neuroreport.

[37]  Michael W. Cole,et al.  The Frontoparietal Control System , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[38]  Tony W. Wilson,et al.  Circadian modulation of motor-related beta oscillatory responses , 2014, NeuroImage.

[39]  A. Labarga,et al.  Alpha and beta oscillatory activity during a sequence of two movements , 2004, Clinical Neurophysiology.

[40]  F. L. D. Silva,et al.  Beta rebound after different types of motor imagery in man , 2005, Neuroscience Letters.

[41]  Timothy P. L. Roberts,et al.  Relating MEG measured motor cortical oscillations to resting γ-Aminobutyric acid (GABA) concentration , 2011, NeuroImage.

[42]  G Pfurtscheller,et al.  Mechanical Stimulation of the Fingertip Can Induce Bursts of &bgr; Oscillations in Sensorimotor Areas , 2001, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.