Beta-Band Cortico-Muscular Phase Coherence in Hemiparetic Stroke

Abstract

Following a stroke, compensation for the loss of ipsilesional corticospinal and corticobulbar projections, results in increased reliance on contralesional motor pathways during paretic arm movement. Better understanding outcomes of post-stroke contralesional cortical adaptation outcomes may benefit more targeted post-stroke motor rehabilitation interventions. This proof-of-concept study involves eight healthy controls and ten post-stroke participants. Electroencephalographic (EEG) and deltoid electromyographic (EMG) data were collected during an upper-limb task. Phase coupling between beta-band motor cortex EEG and deltoid EMG was assessed using the Multi-Phase Locking Value (M-PLV) method. Different from classic cortico-muscular coherence, M-PLV allows for the calculation of dynamic phase coherence and delays, and is not affected by the non-stationary nature of EEG/EMG signals. Nerve conduction delay from the contralateral motor cortex to the deltoid muscle of the paretic arm was estimated. Our results show the ipsilateral (contralesional) motor cortex beta-band phase coherence behavior is altered in stroke participants, with significant differences in ipsilateral EEG-EMG coherence values, ipsilateral time course percentage above the significance threshold, and ipsilateral time course area above the significance threshold. M-PLV phase coherence analysis provides evidence for post-stroke contralesional motor adaptation, highlighting its increased role in the paretic shoulder abduction task. Nerve conduction delay between the motor cortices and deltoid muscle is significantly higher in stroke participants. Beta-band M-PLV phase coherence analysis shows greater phase-coherence distribution convergence between the ipsilateral (contralesional) and contralateral (ipsilesional) motor cortices in stroke participants, which is interpretable as evidence of maladaptive neural adaptation resulting from a greater reliance on the contralesional motor cortices.

Keywords: beta-band phase coherence; electroencephalography; electromyography; multimodal corticomuscular connectivity; phase coherence analysis; post-stroke neuroadaptation.

Figure 1:

Typical experimental subject setup and positioning for the shoulder movement task: The study participant is seated in the Biodex 3 chair, with the arm securely fastened to the Biodex pedestal via a custom cast with Delrim cuff, weight-support platform, and load cell. A 32 EEG cap is mounted on the participant’s head, as well as several pairs of EMG electrodes, on the biceps, triceps, and intermediate deltoid muscles. Not all installed electrodes are visible, due to photographic angle limitations.

Figure 2:

M-PLV CV time course for a stroke participant, paretic arm EMG vs. contralateral (ipsilesional) motor cortex, $\mathrm{\tau }=89.84\mathrm{m}\mathrm{s}$, 95% significance threshold = 0.0634 (red line), average timecourse CV = 0.0666.

Figure 3:

Optimal delay value ($\mathrm{\tau }$) calculation for a control subject, showing an optimal delay value (peak) of 42.97 ms with a 1-second average contralateral beta-band CV of 0.063 across 250 abduction trials.

Figure 4:

Figure 4a (left) showing the EEG-EMG time course-averaged CV data for the tested arm and contralateral motor cortex (ipsilesional for stroke participants). The stroke (red) and control (blue) participant distributions are not significantly different, with the median CV shown as the line inside the box, and the upper and lower quartiles as box edges, and the range given as the lines above and below the box (p=0.24). Figure 4b (right) shows the differing nerve conduction (NC) time-delay values (left) of control (blue) and stroke (red) participants between the tested arm and contralateral motor cortex (ipsilesional for stroke participants). The stroke and control NC delay values in figure 4b represent two statistically different population distributions, with the median delay shown as the line inside the box, and the upper and lower quartiles as box edges, and the range given as the lines above and below the box (p<0.001, right).

Figure 5:

Control (blue) vs. Stroke (red) population distributions. The median value for each distribution is shown as the central line inside the box plot, with the upper and lower quartiles as box edges, and the range given as the lines above and below the box. Outlier values are shown as circles above and below the range demarcations. Figure 5a (upper left) shows the laterality index distributions of stroke and control populations. These distributions are significantly different between the two populations with 95% or higher confidence (p=0.27). Figure 5b (upper right) shows the coherence-time course average value of the EEG/EMG data ipsilateral to the abducted arm (contralesional for stroke participants). The stroke and control average CV distributions are also statistically significantly different between the two populations (p=0.032). Figure 5c (lower left) shows the percentage of the 1-second EEG-EMG M-PLV time course data (similar to the example in [figure 2]) ipsilateral to the abducted arm (contralesional for stroke participants) that was determined to be above the 95% significance threshold calculated via Monte-Carlo simulation. The stroke and control average CV distributions are statistically significantly different between the two populations (p=0.0017). Figure 5d (lower right) shows the total area of the 1-second EEG-EMG M-PLV time course data (similar to the example in [figure 2]) ipsilateral to the abducted arm (contralesional for stroke participants) that was determined to be above the 95% significance threshold calculated via Monte-Carlo simulation. The stroke and control average CV distributions are statistically significantly different (p=0.026).

Figure 6:

Percentage of the 1-second EEG-EMG M-PLV CV time course determined to be above the 95% significance threshold (%AT, calculated via Monte-Carlo simulation) in control participants. The blue population represents the per-subject average CV data from the deltoid EMG electrodes and the central motor cortex EEG electrode ipsilateral to the tested arm, while the red population represents the per-subject average CV data from the deltoid EMG electrodes and the central motor cortex EEG electrode contralateral to the tested arm. The median value for each distribution is shown as the central line inside the box plot, with the upper and lower quartiles as box edges, and the range given as the lines above and below the box. The blue circle above the upper range demarcation for the ipsilateral population represents an outlier value. In control participants, the ipsilateral and contralateral %AT value distributions represent two statistically different population distributions (p=0.019). This data shows that the contralateral motor cortex experiencing significant beta-band EEG-EMG coherence for a longer period of the abduction task than the ipsilateral motor cortex. This is indicative of the differing responsibilities of the two motor cortexes during a normal-function single-arm abduction task.