MEG Insight into the Spectral Dynamics Underlying Steady Isometric Muscle Contraction

To gain fundamental knowledge on how the brain controls motor actions, we studied in detail the interplay between MEG signals from the primary sensorimotor (SM1) cortex and the contraction force of 17 healthy adult humans (7 females, 10 males). SM1 activity was coherent at ~20 Hz with surface electromyogram (as already extensively reported) but also with contraction force. In both cases, the effective coupling was dominant in the efferent direction. Across subjects, the level of ~20 Hz coherence between cortex and periphery positively correlated with the "burstiness" of ~20 Hz SM1 (Pearson r 0.65) and peripheral fluctuations (r 0.9). Thus, ~20 Hz coherence between cortex and periphery is tightly linked to the presence of ~20 Hz bursts in SM1 and peripheral activity. However, the very high correlation with peripheral fluctuations suggests that the periphery is the limiting factor. At frequencies <3 Hz, both SM1 signals and ~20 Hz SM1 envelope were coherent with both force and its absolute change rate. The effective coupling dominated in the efferent direction between (1) force and the ~20 Hz SM1 envelope and (2) the absolute change rate of the force and SM1 signals. Together, our data favor the view that ~20 Hz coherence between cortex and periphery during isometric contraction builds on the presence of ~20 Hz SM1 oscillations and needs not rely on feedback from the periphery. They also suggest that effective cortical proprioceptive processing operates at <3 Hz frequencies, even during steady isometric contractions.

SIGNIFICANCE STATEMENT Accurate motor actions are made possible by continuous communication between the cortex and spinal motoneurons, but the neurophysiological basis of this communication is poorly understood. Using MEG recordings in humans maintaining steady isometric muscle contractions, we found evidence that the cortex sends population-level motor commands that tend to structure according to the ~20 Hz sensorimotor rhythm, and that it dynamically adapts these commands based on the <3 Hz fluctuations of proprioceptive feedback. To our knowledge, this is the first report to give a comprehensive account of how the human brain dynamically handles the flow of proprioceptive information and converts it into appropriate motor command to keep the contraction force steady.

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