Plasticity of premotor cortico-muscular coherence in severely impaired stroke patients with hand paralysis

Abstract

Motor recovery in severely impaired stroke patients is often very limited. To refine therapeutic interventions for regaining motor control in this patient group, the functionally relevant mechanisms of neuronal plasticity need to be detected. Cortico-muscular coherence (CMC) may provide physiological and topographic insights to achieve this goal. Synchronizing limb movements to motor-related brain activation is hypothesized to reestablish cortico-motor control indexed by CMC. In the present study, right-handed, chronic stroke patients with right-hemispheric lesions and left hand paralysis participated in a four-week training for their left upper extremity. A brain-robot interface turned event-related beta-band desynchronization of the lesioned sensorimotor cortex during kinesthetic motor-imagery into the opening of the paralyzed hand by a robotic orthosis. Simultaneous MEG/EMG recordings and individual models from MRIs were used for CMC detection and source reconstruction of cortico-muscular connectivity to the affected finger extensors before and after the training program. The upper extremity-FMA of the patients improved significantly from 16.23 ± 6.79 to 19.52 ± 7.91 (p = 0.0015). All patients showed significantly increased CMC in the beta frequency-band, with a distributed, bi-hemispheric pattern and considerable inter-individual variability. The location of CMC changes was not correlated to the severity of the motor impairment, the motor improvement or the lesion volume. Group analysis of the cortical overlap revealed a common feature in all patients following the intervention: a significantly increased level of ipsilesional premotor CMC that extended from the superior to the middle and inferior frontal gyrus, along with a confined area of increased CMC in the contralesional premotor cortex. In conclusion, functionally relevant modulations of CMC can be detected in patients with long-term, severe motor deficits after a brain-robot assisted rehabilitation training. Premotor beta-band CMC may serve as a biomarker and therapeutic target for novel treatment approaches in this patient group.

Keywords: Brain-computer interface; Brain-machine interface; Brain-robot interface; Cortical reorganization; Cortico-spinal coherence; Functional restoration; Hemiparesis.

Fig. 1

Histograms of individual (A) and mean (B) Fugl-Meyer Score values pre- and post-training.

Fig. 2

Sensor level plots for each single patient. In the upper row of each panel, CMC spectra for pre (light blue, dashed curve) and post-training (deep blue solid curve) are shown. The spectra result from the average of coherence between channel signals covering the bi-hemispheric sensorimotor system and the EMG signal. In the middle row, topoplots of significant beta coherence in the pre and post condition are shown. In the lower panel EMG signals are plotted in the time domain for the entire duration of the motor task.

Fig. 3

Single patient's positive (increase) and negative (decrease) clusters after the training (Pat. 1–9, upper panel) and respective brain structural damage (lower panel, MR images). t-Statistic maps of the CMC post-training vs pre-training differences. Colored areas show significant changes post vs pre. Red and blue represent increase and decrease in connectivity, respectively. For further details, see Material and methods.

Fig. 4

Union of statistical cluster maps on a standard brain surface. Overlaid positive clusters are shown in (A). The negative clusters were detected in 3 patients only, in 2 of whom overlapping was also observed (B).