β-bursts reveal the trial-to-trial dynamics of movement initiation and cancellation

Abstract

The neurophysiological basis of motor processes and their control is of tremendous interest to basic researchers and clinicians alike. Notably, both movement initiation and cancellation are accompanied by prominent field potential changes in the β-frequency band . In trial-averages, movement initiation is indexed by β-band desynchronization over sensorimotor sites, while movement cancellation is signified by β-power increases over (pre)frontal areas. However, averaging misrepresents the true nature of the β-signal. As recent work has highlighted, raw β-band activity is characterized by short-lasting, burst-like events, rather than by steady modulations. To investigate how such β-bursts relate to movement initiation and cancellation in humans, we investigated scalp-recorded β-band activity in 234 healthy subjects performing the Stop-signal task. Four observations were made: First, both movement initiation and cancellation were indexed by systematic, localized changes in β-bursting. While β-bursting at bilateral sensorimotor sites steadily declined during movement initiation, β-bursting increased at fronto-central sites when Stopsignals instructed movement cancellation. Second, the amount of fronto-central β-bursting clearly distinguished successful from unsuccessful movement cancellation. Third, the emergence of fronto-central β-bursting coincided with the latency of the movement cancellation process, indexed by Stop-signal reaction time. Fourth, individual fronto-central β-bursts during movement cancellation were followed by a low-latency re-instantiation of bilateral sensorimotor β-bursting. These findings suggest that β-bursting is a fundamental signature of the motor system, reflecting a steady inhibition of motor cortex that is suppressed during movement initiation, and can be rapidly re-instantiated by frontal areas when movements have to be rapidly cancelled.3 Significance StatementMovement-related β-frequency (15-29Hz) 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.

Neurofeedback-Linked Suppression of Cortical β Bursts Speeds Up Movement Initiation in Healthy Motor Control: A Double-Blind Sham-Controlled Study

“…The changes in the accumulated duration of beta bursts induced by neurofeedback training positively correlated with the shortening of reaction time. These results are consistent with previous studies which demonstrated a positive correlation between beta bursts and reaction time (Little et al, 2019;Wessel 2019), but as we purposefully modulated beta bursting through neurofeedback we also provide evidence in favour of a causal link between transient beta bursts and motor function.…”

“…The timing of beta bursts in the motor cortex prior to movement was related to the duration of motor preparation, with later bursts resulting in delayed response times (Little et al, 2019). Wessel (2019) also found that an increased rate of beta bursts in the contralateral sensorimotor cortex following a Go cue predicted a longer reaction time. However, all these studies are correlational, and it is still not clear whether modulating sensorimotor beta bursts can lead to changes in motor preparation and movement initiation.…”

“…In particular, Kühn et al, (2004) found that the event-related desynchronization (ERD) of beta power in the human subthalamic nucleus correlated with motor performance, with a longer latency ERD associated with longer reaction times in an externally paced voluntary movement. Such movement-related beta power reduction has been suggested to reflect changes in the probability of beta bursts rather than a smooth modulation of sustained beta activity (Feingold et al, 2015), and more recently, it has been emphasized that the beta bursts in the cortical-basal ganglia motor network predict sensorimotor behavior (Feingold et al, 2015;Sherman et al, 2016;Shin et al, 2017;Torrecillos et al, 2018;Little et al, 2019;Wessel 2019) and correlate with motor impairment in patients with Parkinson's disease (Tinkhauser et al, 2017a, b). Indeed, beta bursts in the subthalamic nucleus, a key relay in basal ganglia-cortical circuits, are more predictive of motor impairment than average beta power in patients with Parkinson's disease (Torrecillos et al, 2018;Tinkhauser et al, 2020), and similar observations have been made regarding cortical beta bursts and trialaveraged beta power.…”

Brain Activity Reveals Multiple Motor-Learning Mechanisms in a Real-World Task

“…Recent studies suggest that event-related desynchronizations and synchronizations, such as PMBR, are driven by beta bursts (Little et al, 2019 ; Seedat et al, 2020 ; Wessel, 2020 ) which carry more information than the trial-averaged band oscillation. At the same time, a recent study suggested spatial differences between beta oscillations that reflect implicit and explicit learning (Jahani et al, 2020 ).…”

Temporal cascade of frontal, motor and muscle processes underlying human action-stopping

“…We now measured scalp EEG as well as EMG from the hand, in 11 participants (see Table 1 for behavioral results). We derived beta bursts rather than beta power per se, as bursts have richer features (Shin et al, 2017) [also see (Little et al, 2018;Wessel, 2019a)], such as burst timing and duration. To identify right frontal electrodes of interest in each participant (i.e.…”