Functional connectivity in neuromuscular system underlying bimanual muscle synergies

Abstract

Neural synchrony has been suggested as mechanism for integrating distributed sensorimotor systems involved in coordinated movement. To test the role of corticomuscular and intermuscular coherence in the formation of bimanual muscle synergies, we experimentally manipulated the degree of coordination between hand muscles by varying the sensitivity of the visual feedback to differences in bilateral force. In 16 healthy participants, cortical activity was measured using 64-channel electroencephalography (EEG) and muscle activity of the flexor pollicis brevis muscle of both hands using 8x8-channel high-density electromyography (HDsEMG). Using the uncontrolled manifold framework, coordination between bilateral forces was quantified by the synergy index RV in the time and frequency domain. Functional connectivity was assed using corticomuscular coherence between muscle activity and cortical source activity and intermuscular coherence between bilateral EMG activity. As expected, bimanual synergies were stronger in the high coordination condition. RV was higher in the high coordination condition in frequencies between 0 and 0.5 Hz, and above 2 Hz. For the 0.5-2 Hz frequency band this pattern was inverted. Corticomuscular coherence in the beta band (16-30 Hz) was maximal in the contralateral motor cortex and was reduced in the high coordination condition. In contrast, intermuscular coherence was observed at 5-12 Hz and increased with bimanual coordination. Within-subject comparisons revealed a negative correlation between RV and corticomuscular coherence and a positive correlation between RV and intermuscular coherence. Our findings suggest two distinct neural pathways: (1) Corticomuscular coherence reflects direct corticospinal projections involved in controlling individual muscles; (2) intermuscular coherence reflects diverging pathways involved in the coordination of multiple muscles.