β-Bursts Reveal the Trial-to-Trial Dynamics of Movement Initiation and Cancellation

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 ␤-frequency band (15-29 Hz): in trial-averages, movement initiation is accompanied by ␤-band desynchronization over sensorimotor areas, whereas movement cancellation is accompanied by ␤-power increases over (pre)frontal areas. However, averaging misrepresents the true nature of the ␤-signal. Unaveraged ␤-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 ␤-bursts relate to movement in male and female humans (N ϭ 234), we investigated scalp-recorded ␤-band activity during the stop-signal task, which operationalizes both movement initiation and cancellation. Both processes were indexed by systematic spatiotemporal changes in ␤-burst rates. Before movement initiation, ␤-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 ␤-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 ␤-bursting over fronto-central sites. Such ␤-bursts were followed by shortlatency increases of bilateral sensorimotor ␤-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 ␤-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.

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

“…While several scalp EEG, intracranial EEG, and MEG studies showed increased right frontal beta power for stopping (Castiglione et al, 2019;Schaum et al, 2020;Swann et al, 2009Swann et al, , 2012Wagner et al, 2017), a recent scalp EEG study focused on the spatial and temporal dynamics of beta bursts (Wessel, 2019b). That study saw that burst probability increased for likely dorsomedial frontal cortex (electrode FCz) rather than right frontal cortex, as we do.…”

“…This discrepancy could be explained by our use of a spatial filter approach whereas that study analyzed the data in channel space. A further observation of Wessel (2019b) was that bursts increased over bilateral sensorimotor cortex ~25 ms after the frontal area; and this was interpreted as inhibition of the motor system. This fits our observation of a decrease in corticomotor excitability within ~20 ms of right frontal bursts.…”

Latency and amplitude of the stop-signal P3 event-related potential are related to inhibitory GABAaactivity in primary motor cortex

“…Indeed, EMG and MEP recordings show that the first signs of motor-system inhibition in these measures emerge as early as ∼150ms after the onset of a stop-signal (Jana, Hannah, Muralidharan, & Aron, 2020; Raud & Huster, 2017). In line with this, recent studies have shown that cortical signals that are related to stopping success can also be found in similar time ranges (Huster et al, 2020; Jana et al, 2020; Skippen et al, 2020; Wessel, 2019). Just like the beforementioned EMG and MEP measurements of functional motor inhibition, these cortical signatures often precede both SSRT, as well as the typical onset latency of the fronto-central P3, by several dozens of milliseconds.…”

Taxonomy of neural oscillation events in primate auditory cortex

“…To our knowledge, our is the first study to systematically quantify the full range of physiological oscillations in the auditory cortex, using the novel method of oscillation event analysis. Prior studies have shown that high-power beta rhythms emerge as brief transient events lasting only a few cycles, in somatosensory [20,23] , motor [48][49][50] and frontal cortex [20,51] . In somatosensory cortex, extracranial measurement in humans, and intracranial in mice and NHP [20,23] showed a low rate of beta events comparable to what we observed (1.4-1.6 Hz; Supporting Material Table 1A ).…”