Objective: If M1 generates final motor outputs and cerebellar temporal kinematic information must pass through M1, then M1 should relay cerebellar frequency codes to the spinal cord. Accordingly, perturbations of M1 activity would be expected to disrupt motor kinematics.

Background: The classic view of motor control holds that the primary motor cortex (M1) encodes detailed motor commands transmitted to the spinal cord. However, emerging evidence, including M1 lesioning studies, challenges its foundational role in real-time kinematic control. Recent discoveries show that the cerebellum governs movement timing by linearly encoding instantaneous motor frequencies with equation-level precision. These advances prompt re-examination of how cerebellar kinematic codes reach spinal motor neurons.

Method: To test this prediction, we used optogenetic manipulation of M1 and the cerebellum combined with single-unit recordings and motion tracking in awake mice. In humans performing rhythmic tapping, whole-brain EEG tracked frequency propagation and quantified frequency-dependent coherence between neural activity and muscles. Kinematic performance was further examined in essential tremor patients undergoing thalamic deep-brain stimulation (DBS), which disrupts cerebellar-thalamo-M1 transmission.

Results: In mice, stimulation or silencing of the deep cerebellar nucleus (DCN) perturbed rhythmic, patterned, and skilled movements, whereas M1 manipulation did not affect motor kinematics. Coherence analyses confirmed that cerebellar frequency codes were transmitted independently of M1. Tractography revealed DCN innervation of spinal motor neurons. Stimulation of DCN spinal terminals elicited movements matching designed frequency patterns, indicating that cerebellar spinal pathways govern temporal motion dynamics independent of M1. In humans, whole-brain frequency mapping and brain-muscle coherence analyses showed that the cerebellum, but not M1, encodes temporal kinematics. Patients receiving thalamic DBS provided causal evidence that voluntary kinematic control remains intact despite disruption of cerebellum-to-M1 transmission.

Conclusion: The cerebellum encodes temporal kinematics through cerebellar spinal pathways, whereas M1 lacks this capacity. This shifts motor kinematic output from the corticospinal to the cerebellar spinal axis, reshaping motor control theory and frameworks for movement disorders.

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MDS Abstracts - https://www.mdsabstracts.org/abstract/cerebellar-cortical-spinal-information-flow-for-motor-kinematic-control/