Ipsilateral EEG mu rhythm reflects the excitability of uncrossed pathways projecting to shoulder muscles

Abstract

Background: Motor planning, imagery or execution is associated with event-related desynchronization (ERD) of mu rhythm oscillations (8-13 Hz) recordable over sensorimotor areas using electroencephalography (EEG). It was shown that motor imagery involving distal muscles, e.g. finger movements, results in contralateral ERD correlating with increased excitability of the contralateral corticospinal tract (c-CST). Following the rationale that purposefully increasing c-CST excitability might facilitate motor recovery after stroke, ERD recently became an attractive target for brain-computer interface (BCI)-based neurorehabilitation training. It was unclear, however, whether ERD would also reflect excitability of the ipsilateral corticospinal tract (i-CST) that mainly innervates proximal muscles involved in e.g. shoulder movements. Such knowledge would be important to optimize and extend ERD-based BCI neurorehabilitation protocols, e.g. to restore shoulder movements after stroke. Here we used single-pulse transcranial magnetic stimulation (TMS) targeting the ipsilateral primary motor cortex to elicit motor evoked potentials (MEPs) of the trapezius muscle. To assess whether ERD reflects excitability of the i-CST, a correlation analysis between between MEP amplitudes and ipsilateral ERD was performed.

Methods: Experiment 1 consisted of a motor execution task during which 10 healthy volunteers performed elevations of the shoulder girdle or finger pinching while a 128-channel EEG was recorded. Experiment 2 consisted of a motor imagery task during which 16 healthy volunteers imagined shoulder girdle elevations or finger pinching while an EEG was recorded; the participants simultaneously received randomly timed, single-pulse TMS to the ipsilateral primary motor cortex. The spatial pattern and amplitude of ERD and the amplitude of the agonist muscle's TMS-induced MEPs were analyzed.

Results: ERDs occurred bilaterally during both execution and imagery of shoulder girdle elevations, but were lateralized to the contralateral hemisphere during finger pinching. We found that trapezius MEPs increased during motor imagery of shoulder elevations and correlated with ipsilateral ERD amplitudes.

Conclusions: Ipsilateral ERD during execution and imagery of shoulder girdle elevations appears to reflect the excitability of uncrossed pathways projecting to the shoulder muscles. As such, ipsilateral ERD could be used for neurofeedback training of shoulder movement, aiming at reanimation of the i-CST.

Keywords: Brain-computer interface; Electroencephalography; Event-related desynchronization; Stroke rehabilitation.

Fig. 1

A schematic representation of the experimental protocols. Rest: rest period, Prep: preparation period, Task: task period (motor execution, motor imagery, or relax). a Experiment 1 in which participants performed movement execution (finger pinching or elevation of the shoulder girdle) during the task period. When the word ‘Go’ was presented on the computer monitor, participants executed a movement that was specified during the preparation period. b Experiment 2 in which participants performed motor imagery (finger pinching or elevation of the shoulder girdle) or remained relaxed without any imagery during the task period. When participants performed imagery of movements, the magnitude of ERD was fed-back on the computer monitor

Fig. 2

a Event-related desynchronization (ERD) topography during motor execution in a representative participant. Black dots indicate electroencephalogram (EEG) channel location. Left panel, finger motor execution; Right panel, shoulder motor execution. b Laterality index (LI) for finger and shoulder motor execution. An asterisk denotes statistical significance (p < 0.05)

Fig. 3

a Event-related desynchronization (ERD) topography during motor imagery in a representative participant; Black dots indicate electroencephalogram (EEG) channel location. Left panel, finger motor imagery; Right panel, shoulder motor imagery; b Laterality index (LI) for finger and shoulder motor imagery. An asterisk denotes statistical significance (p < 0.05)

Fig. 4

Motor-evoked potential (MEP) amplitude during motor imagery of elevation of the shoulder girdle and the rest period. Each line indicates data from an individual participant. An asterisk denotes statistical significance (p < 0.05)

Fig. 5

Relationship between event-related desynchronization (ERD) and motor-evoked potential (MEP) amplitude during shoulder motor imagery in a representative participant. Each diamond indicates a single trial