Spatiotemporal organization of human sensorimotor beta burst activity
- University College London, United Kingdom
- University of Oxford, United Kingdom
- Institut des Sciences Cognitives Marc Jeannerod, France
Abstract
Beta oscillations in human sensorimotor cortex are hallmark signatures of healthy and pathological movement. In single trials, beta oscillations include bursts of intermittent, transient periods of high-power activity. These burst events have been linked to a range of sensory and motor processes, but their precise spatial, spectral, and temporal structure remains unclear. Specifically, a role for beta burst activity in information coding and communication suggests spatiotemporal patterns, or travelling wave activity, along specific anatomical gradients. We here show in human magnetoencephalography recordings that burst activity in sensorimotor cortex occurs in planar spatiotemporal wave-like patterns that dominate along two axes either parallel or perpendicular to the central sulcus. Moreover, we find that the two propagation directions are characterised by distinct anatomical and physiological features. Finally, our results suggest that sensorimotor beta bursts occurring before and after a movement can be distinguished by their anatomical, spectral and spatiotemporal characteristics, indicating distinct functional roles.
Data availability
Data are available via the Open Science Framework (OSF) at https://osf. io/eu6nx. Data are also archived at the Open MEG Archive (OMEGA; Nisoetal.,2016) and may be accessed via http://dx .doi.org/10.23686/ 0015896 (Niso et al.,2018) after registration at https:// www.mcgill.ca/bic/resources/omega.
Article and author information
Author details
Funding
Brain Research UK (201718-13)
- Catharina Zich
Brain Research UK (201617-03)
- Catharina Zich
Wellcome Trust (098369/Z/12/Z)
- Andrew J Quinn
Engineering and Physical Sciences Research Council (EP/T001046/1)
- George O'Neill
Medical Research Council (MR/N013867/1)
- Lydia C Mardell
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: The study protocol was in full accordance with the Declaration of Helsinki, and all participants gave written informed consent after being fully informed about the purpose of the study. The study protocol, participant information, and form of consent, were approved by the UCL Research Ethics Committee (reference number 5833/001).
Copyright
© 2023, Zich et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Spatiotemporal organization of human sensorimotor beta burst activity
eLife 12:e80160.
https://doi.org/10.7554/eLife.80160
Further reading
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- Neuroscience
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.
