Different Faces of Medial Beta-Band Activity Reflect Distinct Visuomotor Feedback Signals.

Beta-band (13-35 Hz) modulations following reward, task outcome feedback, and error have been described in cognitive and/or motor adaptation tasks. Observations from different studies are, however, difficult to conciliate. Among the studies that used cognitive response selection tasks, several reported an increase in beta-band activity following reward, whereas others observed increased beta power after negative feedback. Moreover, in motor adaptation tasks, an attenuation of the postmovement beta rebound follows a movement execution error induced by visual or mechanical perturbations. Given that kinematic error typically leads to negative task-outcome feedback (e.g., target missed), one may wonder how contradictory modulations, beta power decrease with movement error versus beta power increase with negative feedback, may coexist. We designed a motor adaptation task in which female and male participants experience varied feedbacks-binary success/failure feedback, kinematic error, and sensory-prediction error-and demonstrate that beta-band modulations in opposite directions coexist at different spatial locations, time windows, and frequency ranges. First, high beta power in the medial frontal cortex showed opposite modulations well separated in time when compared in success and failure trials; that is, power was higher in success trials just after the binary success feedback, whereas it was lower in the postmovement period compared with failure trials. Second, although medial frontal high-beta activity was sensitive to task outcome, low-beta power in the medial parietal cortex was strongly attenuated following movement execution error but was not affected by either the outcome of the task or sensory-prediction error. These findings suggest that medial beta activity in different spatio-temporal-spectral configurations play a multifaceted role in encoding qualitatively distinct feedback signals.SIGNIFICANCE STATEMENT Beta-band activity reflects neural processes well beyond sensorimotor functions, including cognition and motivation. By disentangling alternative spatio-temporal-spectral patterns of possible beta-oscillatory activity, we reconcile a seemingly discrepant literature. First, high-beta power in the medial frontal cortex showed opposite modulations separated in time in success and failure trials; power was higher in success trials just after success feedback and lower in the postmovement period compared with failure trials. Second, although medial frontal high-beta activity was sensitive to task outcome, low-beta power in the medial parietal cortex was strongly attenuated following movement execution error but was not affected by the task outcome or the sensory-prediction error. We propose that medial beta activity reflects distinct feedback signals depending on its anatomic location, time window, and frequency range.

Spatially Distinct Beta-Band Activities Reflect Implicit Sensorimotor Adaptation and Explicit Re-aiming Strategy.

Previous research suggests that so-called implicit and explicit processes of motor adaptation are implemented by distinct neural structures. Here we tested whether implicit sensorimotor adaptation and strategic re-aiming used to reduce movement error are reflected by spatially distinct EEG oscillatory components. We analyzed beta-band oscillations (∼13-30 Hz), which have long been linked to sensorimotor functions, at the time when these adaptive processes intervene for movement planning. We hypothesized that beta-band activity within sensorimotor regions relates to implicit adaptive processes, whereas beta-band activity within medial motor areas reflects deliberate re-aiming. In female and male human volunteers, we recorded EEG in a motor adaptation task in which a visual rotation was introduced in short series of trials separated by unperturbed trials. Participants were instructed in advance about the nature of the visual perturbation and trained to counter it by strategically re-aiming at a neighboring target. Consistent with our hypothesis, we found that preparatory beta-band activities within the two regions exhibited different patterns of modulation. Beta power in lateral central regions was attenuated when a change in the visual condition rendered internal-model predictions uncertain. In contrast, beta power in medial frontal regions was selectively decreased when participants strategically re-aimed their reaches. We propose that the reduction in lateral central beta power reflects an increased weighting of peripheral sensory information implicitly triggered when an adaptive change in the sensorimotor mapping is required, whereas the reduction in medial frontal beta-band activity relates to the inhibition of automatic motor responses in favor of cognitively controlled movements.SIGNIFICANCE STATEMENT Behavioral and modeling studies have proposed that so-called implicit and explicit components of motor adaptation recruit different neural circuits. Here, we investigated whether these different processes are reflected by spatially distinct beta-band activities. Analyzing EEG signals at the time they influence movement planning, during the foreperiod, we found that beta power within lateral central regions was decreased when a change in visual conditions required implicit sensorimotor remapping, which may reflect enhanced sensory processing when internal-model predictions are rendered uncertain. In contrast, beta-band power within medial frontal areas was selectively attenuated when participants deliberately re-aimed their movements to improve task performance, which may be associated with the inhibition of automatic motor responses in favor of cognitively controlled movements.