Transient beta activity and cortico-muscular connectivity during sustained motor behaviour

Irene Echeverria-Altuna; Andrew J. Quinn; Nahid Zokaei; Mark W. Woolrich; Anna C. Nobre; Freek van Ede

doi:10.1016/j.pneurobio.2022.102281

Transient beta activity and cortico-muscular connectivity during sustained motor behaviour

Irene Echeverria-Altuna^*, Andrew J. Quinn, Nahid Zokaei, Mark W. Woolrich, Anna C. Nobre, Freek van Ede

^*Corresponding author for this work

Psychology

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Abstract

Neural oscillations are thought to play a central role in orchestrating activity states between distant neural populations. For example, during isometric contraction, 13–30 Hz beta activity becomes phase coupled between the motor cortex and the contralateral muscle. This and related observations have led to the proposal that beta activity and connectivity sustain stable cognitive and motor states – or the ‘status quo’ – in the brain. Recently, however, beta activity at the single-trial level has been shown to be short-lived – though so far this has been reported for regional beta activity in tasks without sustained motor demands. Here, we measured magnetoencephalography (MEG) and electromyography (EMG) in 18 human participants performing a sustained isometric contraction (gripping) task. If cortico-muscular beta connectivity is directly responsible for sustaining a stable motor state, then beta activity within single trials should be (or become) sustained in this context. In contrast, we found that motor beta activity and connectivity with the downstream muscle were transient. Moreover, we found that sustained motor requirements did not prolong beta-event duration in comparison to rest. These findings suggest that neural synchronisation between the brain and the muscle involves short ‘bursts’ of frequency-specific connectivity, even when task demands – and motor behaviour – are sustained.

Original language	English
Article number	102281
Journal	Progress in neurobiology
Volume	214
DOIs	https://doi.org/10.1016/j.pneurobio.2022.102281
Publication status	Published - 14 May 2022

Bibliographical note

Funding Information:
This research was funded by a Wellcome Trust PhD Studentship ( 102170/Z/13/Z ) I.E.A., a James S. McDonnell Foundation Understanding Human Cognition Collaborative Award (220020448) and a Wellcome Trust Senior Investigator Award (104571/Z/14/Z) to A.C.N, an ERC Starting Grant from the European Research Council (MEMTICIPATION, 850636) to F.v.E., Wellcome Trust grants (106183/Z/14/Z, 215573/Z/19/Z) to M.W.W. and the New Therapeutics in Alzheimer’s Diseases (NTAD) study supported by UK MRC and the Dementia Platform UK to A.C.N. and M.W.W., and by the NIHR Oxford Health Biomedical Research Centre. The Wellcome Centre for Integrative Neuroimaging is supported by core funding from the Wellcome Trust ( 203139/Z/16/Z ). For the purpose of open access, the author has applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission. Figure schematics were created with BioRender.com.

Publisher Copyright:
© 2022 The Authors

Keywords

Beta
Burst
Movement
Neural oscillation
Motor Cortex/physiology
Magnetoencephalography
Humans
Electromyography

ASJC Scopus subject areas

General Neuroscience

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Cite this

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title = "Transient beta activity and cortico-muscular connectivity during sustained motor behaviour",

abstract = "Neural oscillations are thought to play a central role in orchestrating activity states between distant neural populations. For example, during isometric contraction, 13–30 Hz beta activity becomes phase coupled between the motor cortex and the contralateral muscle. This and related observations have led to the proposal that beta activity and connectivity sustain stable cognitive and motor states – or the {\textquoteleft}status quo{\textquoteright} – in the brain. Recently, however, beta activity at the single-trial level has been shown to be short-lived – though so far this has been reported for regional beta activity in tasks without sustained motor demands. Here, we measured magnetoencephalography (MEG) and electromyography (EMG) in 18 human participants performing a sustained isometric contraction (gripping) task. If cortico-muscular beta connectivity is directly responsible for sustaining a stable motor state, then beta activity within single trials should be (or become) sustained in this context. In contrast, we found that motor beta activity and connectivity with the downstream muscle were transient. Moreover, we found that sustained motor requirements did not prolong beta-event duration in comparison to rest. These findings suggest that neural synchronisation between the brain and the muscle involves short {\textquoteleft}bursts{\textquoteright} of frequency-specific connectivity, even when task demands – and motor behaviour – are sustained.",

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note = "Funding Information: This research was funded by a Wellcome Trust PhD Studentship ( 102170/Z/13/Z ) I.E.A., a James S. McDonnell Foundation Understanding Human Cognition Collaborative Award (220020448) and a Wellcome Trust Senior Investigator Award (104571/Z/14/Z) to A.C.N, an ERC Starting Grant from the European Research Council (MEMTICIPATION, 850636) to F.v.E., Wellcome Trust grants (106183/Z/14/Z, 215573/Z/19/Z) to M.W.W. and the New Therapeutics in Alzheimer{\textquoteright}s Diseases (NTAD) study supported by UK MRC and the Dementia Platform UK to A.C.N. and M.W.W., and by the NIHR Oxford Health Biomedical Research Centre. The Wellcome Centre for Integrative Neuroimaging is supported by core funding from the Wellcome Trust ( 203139/Z/16/Z ). For the purpose of open access, the author has applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission. Figure schematics were created with BioRender.com. Publisher Copyright: {\textcopyright} 2022 The Authors",

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Transient beta activity and cortico-muscular connectivity during sustained motor behaviour

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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