Wessel, J. R. | bioRxiv Science

bioRxiv2019

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

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.

neuroscience↗

bioRxiv2019

Frontal cortex tracks surprise separately for different sensory modalities but engages a common inhibitory control mechanism

The brain constantly generates predictions about the environment to guide action. Unexpected events lead to surprise and can necessitate the modification of ongoing behavior. Surprise can occur for any sensory domain, but it is not clear how these separate surprise signals are integrated to affect motor output. By applying a trial-to-trial Bayesian surprise model to human electroencephalography data recorded during a cross-modal oddball task, we tested whether there are separate predictive models for different sensory modalities (visual, auditory), or whether expectations are integrated across modalities such that surprise in one modality decreases surprise for a subsequent unexpected event in the other modality. We found that while surprise was represented in a common frontal signature across sensory modalities (the fronto-central P3 event-related potential), the single-trial amplitudes of this signature more closely conformed to a model with separate surprise terms for each sensory domain. We then investigated whether surprise-related fronto-central P3 activity indexes the rapid inhibitory control of ongoing behavior after surprise, as suggested by recent theories. Confirming this prediction, the fronto-central P3 amplitude after both auditory and visual unexpected events was highly correlated with the fronto-central P3 found after stop-signals (measured in a separate stop-signal task). Moreover, surprise-related and stopping-related activity loaded onto the same component in a cross-task independent components analysis. Together, these findings suggest that medial frontal cortex maintains separate predictive models for different sensory domains, but engages a common mechanism for inhibitory control of behavior regardless of the source of surprise.\n\nAuthor summarySurprise is an elementary cognitive computation that the brain performs to guide behavior. We investigated how the brain tracks surprise across different senses: Do unexpected sounds make subsequent unexpected visual stimuli less surprising? Or does the brain maintain separate expectations of environmental regularities for different senses? We found that the latter is the case. However, even though surprise was separately tracked for auditory and visual events, it elicited a common signature over frontal cortex in both sensory domains. Importantly, we observed the same neural signature when actions had to be stopped after non-surprising stop-signals in a motor inhibition task. This suggests that this signature reflects a rapid interruption of ongoing behavior when our surroundings do not conform to our expectations.

neuroscience↗