Cortico-cerebellar beta-band dynamics predict flexible motor timing

Abstract

Flexible motor control requires that movements adapt to changing temporal contexts. Here, we test whether flexible timing is driven by context-dependent encoding across cortico-cerebellar circuits and how neural dynamics within these circuits enable accurate performance. To overcome the signal-to-noise limitations of conventional electro- and magnetoencephalography, we recorded whole-head neural dynamics using optically pumped magnetometer arrays (OPM-MEG). Participants learned a context-dependent task, executing manual button presses at time intervals 800 ms (T1) and 1,600 ms (T2), respectively, to avoid a periocular air puff, which was associated with an implicit conditioned eyeblink. We found that the motor cortex contralateral to the hand and bilateral cerebellar lobule VI dynamically encoded these intervals through beta-band (13-30 Hz) event-related desynchronisation (ERD) that precisely scaled with T1 and T2. The cerebellar trial-by-trial latency of the beta-band ERD predicted the timing of explicit manual actions. Finally, partial directed coherence revealed that baseline bidirectional beta-band coupling across the network transiently weakened from the ipsilateral cerebellum to the contralateral motor cortex during finger movement execution. Our findings show that cortico-cerebellar coupling functions as a gating mechanism and suggest that cerebellar circuits modulate cortical motor activity for flexible, accurate motor timing. Significance statement How human cortico-cerebellar networks flexibly encode context-dependent timing remains poorly understood due to signal-to-noise constraints in non-invasive neural recordings. By combining a task coupling explicit manual and implicit eyeblink responses with wearable optically pumped magnetometers (OPM-MEG), we overcame these depth-sensitivity constraints to resolve human cortico-cerebellar dynamics. Beta-band (13-30 Hz) event-related desynchronisation in the contralateral cortical motor and bilateral cerebellar lobule VI was scaled to the anticipated response timings, with single-trial cerebellar latencies predicting explicit manual response timing. Crucially, directional functional coupling analysis revealed that bidirectional beta-band coupling transiently reduces from cerebellum to motor cortex during movement execution. This approach establishes a blueprint for non-invasively mapping cortico-cerebellar network dynamics, providing a framework to study circuit-level dysfunctions in disorders affecting the cerebellum.