Brain Oscillations Extend Beyond Task-Relevant Motor Neuron Pools and Contribute to Shaping the Functional State of the Motor System
Hug, F.; Dernoncourt, F.; Naveilhan, C.; van den Hoorn, W.
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It remains unknown whether oscillatory brain activity that shapes sensorimotor state is routed selectively to task-relevant muscles or broadcast across the motor system. 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, 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, indicating broad propagation of cortical dynamics to spinal motor neurons. 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 the rapid build-up of motor output following a sudden increase in excitatory drive. These results support a parallel control architecture in which low-frequency drive determines motor output, whereas higher-frequency oscillatory inputs are broadly distributed and shape the functional state of motor neuron pools in preparation for action.
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