Neuromotor modules revealed by direct electrical stimulation of the human primary motor cortex

Muscle synergies extracted from multimuscle electromyographic (EMG) signals are widely interpreted as fundamental building blocks of motor control that coordinate groups of muscles during movement. Whether EMG-derived muscle synergies represent genuine neurally encoded modules or motor regularities arising from task or biomechanical constraints has been hotly debated because neurophysiological data that definitively demonstrate the neural basis of muscle synergies in humans have been lacking. Here, we seek to validate the potential neural origin of upper limb muscle synergies by exploiting direct electrical stimulation (DES) of the primary motor cortex (M1) routinely delivered by neurosurgeons during awake craniotomy surgery for glioma excision. Across 13 patients, 69% of the muscle synergies observed during preoperative voluntary behaviors could be matched to DES-evoked muscle synergies or their combination. Analysis of the synergies' cortical activity maps further revealed that the cortical representations of the sparser muscle synergies were more anterior and distributed, and those of the nonsparse synergies, more posterior and localized. Our results not only provide direct causal evidence arguing for the neural origin of most behavioral muscle synergies in humans but also demonstrate the potential existence of two M1 subdivisions with distinct patterns of muscle synergy organization.