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Research Articles, Behavioral/Cognitive

Differential beta and gamma activity modulation during unimanual and bimanual motor learning

Min Wu, Marleen J. Schoenfeld, Carl Lindersson, Sven Braeutigam, Catharina Zich and Charlotte J. Stagg
Journal of Neuroscience 29 April 2025, e2187242025; https://doi.org/10.1523/JNEUROSCI.2187-24.2025
Min Wu
1Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, United Kingdom
2Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neuroscience, University of Oxford, United Kingdom
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Marleen J. Schoenfeld
1Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, United Kingdom
2Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neuroscience, University of Oxford, United Kingdom
3Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
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Carl Lindersson
1Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, United Kingdom
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Sven Braeutigam
4Medical Sciences Division, Oxford Centre for Human Brain Activity, University of Oxford, United Kingdom
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Catharina Zich
1Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, United Kingdom
2Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neuroscience, University of Oxford, United Kingdom
5Department of Clinical and Movement Neuroscience, UCL Queen Square Institute of Neurology, London, United Kingdom
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Charlotte J. Stagg
1Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, United Kingdom
2Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neuroscience, University of Oxford, United Kingdom
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Abstract

Movement-related dynamics in the beta and gamma bands have been studied in relation to motor execution and learning during unimanual movements, but their roles in complex bimanual tasks remain largely unexplored. This study aimed to investigate how beta and gamma activity differs between unimanual and bimanual movements, and how these neural signatures evolve during the learning process. Our motor task incorporated varying levels of bimanual interaction: unimanual, bimanual-equal, and bimanual-unequal. Magnetoencephalography data were recorded in healthy participants (N = 43, 27 females) during task performance, and beta and gamma activity was quantified. As expected, increasing task complexity from unimanual to bimanual-equal, and then to bimanual-unequal movements resulted in slower and less accurate performance. Across all conditions, significant beta event-related desynchronization (ERD) and gamma event-related synchronization (ERS) were observed during movement, as well as beta ERS after movement. Bimanual movements exhibited greater beta ERD, beta ERS, and gamma ERS compared to unimanual movements. With practice, participants demonstrated faster and more accurate movements, accompanied by enhanced beta ERS responses. Furthermore, learning-related reductions in errors correlated with increases in beta ERS. These findings suggest the distinct behavioural and neural demands of unimanual versus bimanual movements and highlight the important role of beta activity in motor performance and learning.

Significance statement Bimanual movements, which dominate daily motor behaviours, require finely tuned coordination between the two hands yet remain poorly understood at the neurophysiological level. Using magnetoencephalography, we tested neural responses to a novel movement task incorporating varying levels of bimanual interaction. We demonstrate that greater task complexity elicits enhanced movement-related brain activity in the beta and gamma frequency bands. Motor learning is associated with an increase in beta movement-related synchronization that correlates with improved movement accuracy. This study provides novel insights into how beta and gamma brain activity adapt to increasing movement complexity and motor learning.

Footnotes

  • The authors declare no conflicts of interest.

  • CJS holds a Senior Research Fellowship, funded by the Wellcome Trust (224430/Z/21/Z). MW is funded by the NWO Rubicon grant (04520232310005). The research was supported by the National Institute for Health Research (NIHR) Oxford Biomedical Research Centre. The work was supported by the NIHR Oxford Health Biomedical Research Centre (NIHR203316). The Wellcome Centre for Integrative Neuroimaging is supported by core funding from the Wellcome Trust (203139/Z/16/Z). We thank Ipsita Sarkar and Patricia Cambalova for their help with participant recruitment and data collection.

  • ↵#These authors contributed equally.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Differential beta and gamma activity modulation during unimanual and bimanual motor learning
Min Wu, Marleen J. Schoenfeld, Carl Lindersson, Sven Braeutigam, Catharina Zich, Charlotte J. Stagg
Journal of Neuroscience 29 April 2025, e2187242025; DOI: 10.1523/JNEUROSCI.2187-24.2025

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Differential beta and gamma activity modulation during unimanual and bimanual motor learning
Min Wu, Marleen J. Schoenfeld, Carl Lindersson, Sven Braeutigam, Catharina Zich, Charlotte J. Stagg
Journal of Neuroscience 29 April 2025, e2187242025; DOI: 10.1523/JNEUROSCI.2187-24.2025
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