Journal article
β-Bursts Reveal the Trial-to-Trial Dynamics of Movement Initiation and Cancellation
The Journal of neuroscience, Vol.40(2), pp.411-423
01/08/2020
DOI: 10.1523/JNEUROSCI.1887-19.2019
PMCID: PMC6948942
PMID: 31748375
Abstract
The neurophysiological basis of motor control is of substantial interest to basic researchers and clinicians alike. Motor processes are accompanied by prominent field potential changes in the β-frequency band (15-29 Hz): in trial-averages, movement initiation is accompanied by β-band desynchronization over sensorimotor areas, whereas movement cancellation is accompanied by β-power increases over (pre)frontal areas. However, averaging misrepresents the true nature of the β-signal. Unaveraged β-band activity is characterized by short-lasting, burst-like events, rather than by steady modulations. Therefore, averaging-based quantifications may miss important brain-behavior relationships. To investigate how β-bursts relate to movement in male and female humans (
= 234), we investigated scalp-recorded β-band activity during the stop-signal task, which operationalizes both movement initiation and cancellation. Both processes were indexed by systematic spatiotemporal changes in β-burst rates. Before movement initiation, β-bursting was prominent at bilateral sensorimotor sites. These burst-rates predicted reaction time (a relationship that was absent in trial-average data), suggesting that sensorimotor β-bursting signifies an inhibited motor system, which has to be overcome to initiate movements. Indeed, during movement initiation, sensorimotor burst-rates steadily decreased, lateralizing just before movement execution. In contrast, successful movement cancellation was signified by increased phasic β-bursting over fronto-central sites. Such β-bursts were followed by short-latency increases of bilateral sensorimotor β-burst rates, suggesting that motor inhibition can be rapidly re-instantiated by frontal areas when movements have to be rapidly cancelled. Together, these findings suggest that β-bursting is a fundamental signature of the motor system, used by both sensorimotor and frontal areas involved in the trial-by-trial control of behavior.
Movement-related β-frequency (15-29 Hz) changes are among the most prominent features of neural recordings across species, scales, and methods. However, standard averaging-based methods obscure the true dynamics of β-band activity, which is dominated by short-lived, burst-like events. Here, we demonstrate that both movement-initiation and cancellation in humans are characterized by unique trial-to-trial patterns of β-bursting. Movement initiation is characterized by steady reductions of β-bursting over bilateral sensorimotor sites. In contrast, during rapid movement cancellation, β-bursts first emerge over fronto-central sites typically associated with motor control, after which sensorimotor β-bursting re-initiates. These findings suggest a fundamentally novel, non-invasive measure of the neural interaction underlying movement-initiation and -cancellation, opening new avenues for the study of motor control in health and disease.
Details
- Title: Subtitle
- β-Bursts Reveal the Trial-to-Trial Dynamics of Movement Initiation and Cancellation
- Creators
- Jan R Wessel - Department of Neurology, University of Iowa Hospital and Clinics, Iowa City, Iowa 52242
- Resource Type
- Journal article
- Publication Details
- The Journal of neuroscience, Vol.40(2), pp.411-423
- Publisher
- United States
- DOI
- 10.1523/JNEUROSCI.1887-19.2019
- PMID
- 31748375
- PMCID
- PMC6948942
- ISSN
- 0270-6474
- eISSN
- 1529-2401
- Grant note
- R01 NS102201 / NINDS NIH HHS
- Language
- English
- Date published
- 01/08/2020
- Academic Unit
- Roy J. Carver Department of Biomedical Engineering; Neurology; Psychological and Brain Sciences; Iowa Neuroscience Institute
- Record Identifier
- 9984063174702771
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