Preparing to Stop Action Increases Beta Band Power in Contralateral Sensorimotor Cortex

How do we prepare to stop ourselves in the future? Here, we used scalp EEG to test the hypothesis that people prepare to stop by putting parts of their motor system (specifically, here, sensorimotor cortex) into a suppressed state ahead of time. On each trial, participants were cued to prepare to stop one hand and then initiated a bimanual movement. On a minority of trials, participants were instructed to stop the cued hand while continuing quickly with the other. We used a guided multivariate source separation method to examine oscillatory power changes in presumed sensorimotor cortical areas. We observed that, when people prepare to stop a hand, there were above-baseline beta band power increases (12–24 Hz) in contralateral cortex up to a second earlier. This increase in beta band power in the proactive period was functionally relevant because it predicted, trial by trial, the degree of selectivity with which participants subsequently stopped a response but did not relate to movement per se. Thus, preparing to stop particular response channels corresponds to increased beta power from contralateral (sensorimotor) cortex, and this relates specifically to subsequent stopping. These results provide a high temporal resolution and frequency-specific electrophysiological signature of the preparing-to-stop state that is pertinent to future studies of mitigating provocation, including in clinical disorders. The results also highlight the utility of guided multivariate source separation for revealing the cortical dynamics underlying both movement and response suppression.

[1]  René J. Huster,et al.  The Temporal Dynamics of Response Inhibition and their Modulation by Cognitive Control , 2017, Brain Topography.

[2]  W. Byblow,et al.  Selective inhibition of movement. , 2007, Journal of neurophysiology.

[3]  Tipu Z. Aziz,et al.  The role of the subthalamic nucleus in response inhibition: Evidence from local field potential recordings in the human subthalamic nucleus , 2012, NeuroImage.

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

[5]  P. Brown,et al.  New insights into the relationship between dopamine, beta oscillations and motor function , 2011, Trends in Neurosciences.

[6]  J. Piacentini,et al.  Brief Review of Habit Reversal Training for Tourette Syndrome , 2006, Journal of child neurology.

[7]  A. Aron,et al.  Stop the Presses , 2008, Psychological science.

[8]  K.-R. Muller,et al.  Optimizing Spatial filters for Robust EEG Single-Trial Analysis , 2008, IEEE Signal Processing Magazine.

[9]  A. Aron,et al.  Proactive Selective Response Suppression Is Implemented via the Basal Ganglia , 2013, The Journal of Neuroscience.

[10]  M. Hinder,et al.  Distinct modulation of interhemispheric inhibitory mechanisms during movement preparation reveals the influence of cognition on action control , 2018, Cortex.

[11]  Michael X Cohen,et al.  Comparison of linear spatial filters for identifying oscillatory activity in multichannel data , 2016, Journal of Neuroscience Methods.

[12]  Stefan Haufe,et al.  On the interpretation of weight vectors of linear models in multivariate neuroimaging , 2014, NeuroImage.

[13]  Nitin Tandon,et al.  Intracranial electroencephalography reveals different temporal profiles for dorsal- and ventro-lateral prefrontal cortex in preparing to stop action. , 2013, Cerebral cortex.

[14]  G. Logan.  On the ability to inhibit thought and action , 1984 .

[15]  Kozo Funase,et al.  Unilateral imagined movement increases interhemispheric inhibition from the contralateral to ipsilateral motor cortex , 2014, Experimental Brain Research.

[16]  Ulf Ziemann,et al.  Modulation of interhemispheric inhibition by volitional motor activity: an ipsilateral silent period study , 2009, The Journal of physiology.

[17]  Nitin Tandon,et al.  Roles for the pre-supplementary motor area and the right inferior frontal gyrus in stopping action: Electrophysiological responses and functional and structural connectivity , 2012, NeuroImage.

[18]  Hayley J. MacDonald,et al.  Proactive modulation of long-interval intracortical inhibition during response inhibition. , 2016, Journal of neurophysiology.

[19]  Caitlin L. Oldenkamp,et al.  A Proactive Mechanism for Selective Suppression of Response Tendencies , 2011, The Journal of Neuroscience.

[20]  Julien Bastin,et al.  Subthalamic nucleus activity dissociates proactive and reactive inhibition in patients with Parkinson's disease , 2014, NeuroImage.

[21]  Michael A. DiSano,et al.  Intracranial EEG Reveals a Time- and Frequency-Specific Role for the Right Inferior Frontal Gyrus and Primary Motor Cortex in Stopping Initiated Responses , 2009, The Journal of Neuroscience.

[22]  Mark Hallett,et al.  Time course of corticospinal excitability in reaction time and self‐paced movements , 1998, Annals of neurology.

[23]  Lucas C. Parra,et al.  Blind Source Separation via Generalized Eigenvalue Decomposition , 2003, J. Mach. Learn. Res..

[24]  Peter Brown,et al.  Boosting Cortical Activity at Beta-Band Frequencies Slows Movement in Humans , 2009, Current Biology.

[25]  Julie Duque,et al.  Physiological Markers of Motor Inhibition during Human Behavior , 2017, Trends in Neurosciences.

[26]  Jan R. Wessel,et al.  Stop‐related subthalamic beta activity indexes global motor suppression in Parkinson's disease , 2016, Movement disorders : official journal of the Movement Disorder Society.

[27]  P. Brown.  Abnormal oscillatory synchronisation in the motor system leads to impaired movement , 2007, Current Opinion in Neurobiology.

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

[29]  Jan R. Wessel,et al.  Chronometric Electrical Stimulation of Right Inferior Frontal Cortex Increases Motor Braking , 2013, The Journal of Neuroscience.

[30]  A. Riehle,et al.  The ups and downs of beta oscillations in sensorimotor cortex , 2013, Experimental Neurology.

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

[32]  Adam R. Aron,et al.  Establishing a Right Frontal Beta Signature for Stopping Action in Scalp EEG: Implications for Testing Inhibitory Control in Other Task Contexts , 2018, Journal of Cognitive Neuroscience.

[33]  Jobi S. George,et al.  Transcranial magnetic stimulation reveals dissociable mechanisms for global versus selective corticomotor suppression underlying the stopping of action. , 2012, Cerebral cortex.

[34]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[35]  Jose M Carmena,et al.  Beta band oscillations in motor cortex reflect neural population signals that delay movement onset , 2017, eLife.

[36]  R. Dolan,et al.  Preparing for Selective Inhibition within Frontostriatal Loops , 2013, The Journal of Neuroscience.

[37]  Tzyy-Ping Jung,et al.  Independent Component Analysis of Electroencephalographic Data , 1995, NIPS.

[38]  P. Brown.  Oscillatory nature of human basal ganglia activity: Relationship to the pathophysiology of Parkinson's disease , 2003, Movement disorders : official journal of the Movement Disorder Society.

[39]  Zachary M. Westrick,et al.  Selective inhibition of a multicomponent response can be achieved without cost. , 2015, Journal of neurophysiology.

[40]  Frederick Verbruggen,et al.  Having a goal to stop action is associated with advance control of specific motor representations , 2010, Neuropsychologia.

[41]  Christoph S. Herrmann,et al.  When holding your horses meets the deer in the headlights: time-frequency characteristics of global and selective stopping under conditions of proactive and reactive control , 2014, Front. Hum. Neurosci..