The Cerebellum Implements an Oscillatory Forward Model for Accurate Motor Timing

Abstract

Voluntary movements are composed of small sub-movements generated by pulsatile bursts of muscle activity at 4-10 Hz. These motor intermittencies synchronize with rhythmic brain activity and vary with movement velocity and sensory delays, suggesting they are a signature of a central oscillatory motor control mechanism. We hypothesized that these pulsatile movements arise from a cerebellar clocking mechanism-a neuronal timing process that flexibly adjusts its dynamics to maintain motor precision under temporal uncertainty. If so, cerebellar rhythms should modulate their influence on movement depending on cue predictability. To test this, we used optically pumped magnetoencephalography (OP-MEG), which enables high-quality, movement-tolerant recordings of the brain with dense cerebellar coverage. Six participants performed an auditory-paced finger flexion-extension task at approximately 1 Hz with either regular or irregular cue timing to vary predictability. All participants exhibited clear 4-10 Hz intermittencies in their kinematics, synchronized to neural activity in the cerebellum and the posterior parietal cortex. Our connectivity analysis revealed for the first time, that cerebellar activity at this frequency, predominantly reflects sensory feedback, but during regular, predictable cueing, the cerebellum shifts to exert a greater feedforward influence on movement. Moreover, cerebellar oscillations were most persistently phase-aligned with motor intermittent rhythms during accurately timed actions, an effect that was absent under irregular cueing. These findings support the idea that the cerebellum implements an oscillatory forward model for motor timing and provide novel evidence for its ability to adjusting its role in coordinating sensorimotor integration according to sensory predictability. Motor intermittencies may thus represent the output of a cerebellar timing process that underpins precise voluntary action.