Brain Oscillations Extend Beyond Task-Relevant Motor Neuron Pools and Contribute to Shaping the Functional State of the Motor System

Abstract

It remains unknown whether oscillatory brain activity associated with sensorimotor behavior is routed selectively to task-relevant muscles or expressed more broadly, including in task-irrelevant muscles. Here we combined electroencephalography with large-scale recordings of spinal motor neurons innervating the tibialis anterior. Participants maintained a submaximal dorsiflexion while performing a Go/No-Go task in which the instructed response was either a ballistic dorsiflexion or a ballistic handgrip contraction, making the tibialis anterior task-relevant or task-irrelevant, respectively. Alpha- and beta-band modulations observed at the cortical level were largely expressed in motor neuron output, including in the task-irrelevant motor neuron pool. The peripheral expression of these modulations differed across frequency bands: alpha was partly effector-dependent, consistent with more selective transmission to the task-relevant pool, whereas beta was largely effector-independent, consistent with broader expression across motor neuron pools. Using simulation-based inference, we found that task-related changes in motor output were best explained by modulations in net excitatory drive, whereas alpha- and beta-band inputs contributed primarily to motor neuron synchronization. A complementary simulation showed that this synchronization may facilitate rapid changes in motor output. These results support a parallel control architecture in which low-frequency drive determines motor output, whereas higher-frequency oscillatory inputs shape synchronization within motor pools more broadly, potentially setting the motor system in a state that favours rapid adjustments in output.