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      Human motor cortical beta bursts relate to movement planning and response errors

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          Abstract

          Motor cortical beta activity (13–30 Hz) is a hallmark signature of healthy and pathological movement, but its behavioural relevance remains unclear. Using high-precision magnetoencephalography (MEG), we show that during the classical event-related desynchronisation (ERD) and event-related synchronisation (ERS) periods, motor cortical beta activity in individual trials ( n > 12,000) is dominated by high amplitude, transient, and infrequent bursts. Beta burst probability closely matched the trial-averaged beta amplitude in both the pre- and post-movement periods, but individual bursts were spatially more focal than the classical ERS peak. Furthermore, prior to movement (ERD period), beta burst timing was related to the degree of motor preparation, with later bursts resulting in delayed response times. Following movement (ERS period), the first beta burst was delayed by approximately 100 milliseconds when an incorrect response was made. Overall, beta burst timing was a stronger predictor of single trial behaviour than beta burst rate or single trial beta amplitude. This transient nature of motor cortical beta provides new constraints for theories of its role in information processing within and across cortical circuits, and its functional relevance for behaviour in both healthy and pathological movement.

          Abstract

          The dominant cortical signal before and after movement is the beta oscillations over sensorimotor cortex, which are thought to slowly modulate around movement. This study shows that trial-by-trial beta signals are highly dynamic and dominated by short, high-power bursts, whose precise timing is linked to motor behavior.

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          Most cited references62

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          Post-movement beta synchronization. A correlate of an idling motor area?

          Post-movement beta (around 20 Hz) synchronization was investigated in 2 experiments with self-paced finger extension and flexion and externally paced wrist movement. The electrodes were fixed over the sensorimotor area in distances of 2.5 cm. It was found that after a brisk finger movement the desynchronized beta rhythm displayed a fast recovery and a short-lasting synchronization within 1 sec. This post-movement beta synchronization was maximal over the contralateral hemisphere and localized slightly more anterior to the maximal desynchronization of the hand area mu rhythm. The post-movement beta synchronization is interpreted as a correlate of "idling" motor cortex neurons.
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            Beyond the Status Quo: A Role for Beta Oscillations in Endogenous Content (Re)Activation

            Abstract Among the rhythms of the brain, oscillations in the beta frequency range (∼13–30 Hz) have been considered the most enigmatic. Traditionally associated with sensorimotor functions, beta oscillations have recently become more broadly implicated in top-down processing, long-range communication, and preservation of the current brain state. Here, we extend and refine these views based on accumulating new findings of content-specific beta-synchronization during endogenous information processing in working memory (WM) and decision making. We characterize such content-specific beta activity as short-lived, flexible network dynamics supporting the endogenous (re)activation of cortical representations. Specifically, we suggest that beta-mediated ensemble formation within and between cortical areas may awake, rather than merely preserve, an endogenous cognitive set in the service of current task demands. This proposal accommodates key aspects of content-specific beta modulations in monkeys and humans, integrates with timely computational models, and outlines a functional role for beta that fits its transient temporal characteristics.
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              Propagating waves mediate information transfer in the motor cortex.

              High-frequency oscillations in the beta range (10-45 Hz) are most active in motor cortex during motor preparation and are postulated to reflect the steady postural state or global attentive state of the animal. By simultaneously recording multiple local field potential signals across the primary motor and dorsal premotor cortices of monkeys (Macaca mulatta) trained to perform an instructed-delay reaching task, we found that these oscillations propagated as waves across the surface of the motor cortex along dominant spatial axes characteristic of the local circuitry of the motor cortex. Moreover, we found that information about the visual target to be reached was encoded in terms of both latency and amplitude of evoked waves at a time when the field phase-locked with respect to the target onset. These findings suggest that high-frequency oscillations may subserve intra- and inter-cortical information transfer during movement preparation and execution.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: Project administrationRole: SoftwareRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Resources
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                4 October 2019
                October 2019
                4 October 2019
                : 17
                : 10
                : e3000479
                Affiliations
                [1 ] Department of Clinical and Movement Neuroscience, UCL Queen Square Institute of Neurology, London, United Kingdom
                [2 ] Department of Neurology, University of San Francisco, California, United States of America
                [3 ] Wellcome Centre for Human Neuroimaging, UCL Queen Square Institute of Neurology, London, United Kingdom
                [4 ] Institut des Sciences Cognitives Marc Jeannerod, CNRS UMR 5229, Bron, France
                [5 ] Université Claude Bernard Lyon I, Lyon, France
                UCSF, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-9165-4082
                http://orcid.org/0000-0002-5396-7712
                http://orcid.org/0000-0002-6867-9545
                Article
                PBIOLOGY-D-19-00935
                10.1371/journal.pbio.3000479
                6795457
                31584933
                252fd70b-1f3f-42a7-b5e7-6c65a4f2dfc0
                © 2019 Little et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 2 April 2019
                : 10 September 2019
                Page count
                Figures: 8, Tables: 0, Pages: 30
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 105804/Z/14/Z
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BB/M009645/1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 203147/Z/16/Z
                SL was funded by a clinical research training grant from the Wellcome Trust (105804/Z/14/Z). JB was funded by a BBSRC research grant (BB/M009645/1). The Wellcome Centre for Human Neuroimaging is supported by core funding from the Wellcome trust (203147/Z/16/Z). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Psychology
                Behavior
                Social Sciences
                Psychology
                Behavior
                Biology and Life Sciences
                Neuroscience
                Brain Mapping
                Magnetoencephalography
                Research and Analysis Methods
                Imaging Techniques
                Neuroimaging
                Magnetoencephalography
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                Magnetoencephalography
                Biology and Life Sciences
                Anatomy
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                Motor Cortex
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                Biology and Life Sciences
                Anatomy
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                Medicine and Health Sciences
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                Biology and Life Sciences
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                Custom metadata
                vor-update-to-uncorrected-proof
                2019-10-16
                Data are available via the Open Science Framework (OSF) at https://osf.io/eu6nx. Data are also archived at the Open MEG Archive (OMEGA; Niso et al., 2016 [ 102]) and may be accessed via http://dx.doi.org/10.23686/0015896 (Niso et al., 2018 [ 103]) after registration at https://www.mcgill.ca/bic/resources/omega.

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