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 {beta}-frequency band (15-29Hz). In trial-averages, movement initiation is indexed by {beta}-band desynchronization over sensorimotor sites, while movement cancellation is signified by {beta}-power increases over (pre)frontal areas. However, averaging misrepresents the true nature of the {beta}-signal. As recent work has highlighted, raw {beta}-band activity is characterized by short-lasting, burst-like events, rather than by steady modulations. To investigate how such {beta}-bursts relate to movement initiation and cancellation in humans, we investigated scalp-recorded {beta}-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 {beta}-bursting. While {beta}-bursting at bilateral sensorimotor sites steadily declined during movement initiation, {beta}-bursting increased at fronto-central sites when Stop-signals instructed movement cancellation. Second, the amount of fronto-central {beta}-bursting clearly distinguished successful from unsuccessful movement cancellation. Third, the emergence of fronto-central {beta}-bursting coincided with the latency of the movement cancellation process, indexed by Stop-signal reaction time. Fourth, individual fronto-central {beta}-bursts during movement cancellation were followed by a low-latency re-instantiation of bilateral sensorimotor {beta}-bursting. These findings suggest that {beta}-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.\n\nSignificance StatementMovement-related {beta}-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 {beta}-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 {beta}-bursting. Movement initiation is characterized by steady reductions of {beta}-bursting over bilateral sensorimotor sites. In contrast, during rapid movement cancellation, {beta}-bursts first emerge over fronto-central sites typically associated with motor control, after which sensorimotor {beta}-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.