Contralesional Brain-Computer Interface Control of a Powered Exoskeleton for Motor Recovery in Chronic Stroke Survivors

Abstract

Background and purpose: There are few effective therapies to achieve functional recovery from motor-related disabilities affecting the upper limb after stroke. This feasibility study tested whether a powered exoskeleton driven by a brain-computer interface (BCI), using neural activity from the unaffected cortical hemisphere, could affect motor recovery in chronic hemiparetic stroke survivors. This novel system was designed and configured for a home-based setting to test the feasibility of BCI-driven neurorehabilitation in outpatient environments.

Methods: Ten chronic hemiparetic stroke survivors with moderate-to-severe upper-limb motor impairment (mean Action Research Arm Test=13.4) used a powered exoskeleton that opened and closed the affected hand using spectral power from electroencephalographic signals from the unaffected hemisphere associated with imagined hand movements of the paretic limb. Patients used the system at home for 12 weeks. Motor function was evaluated before, during, and after the treatment.

Results: Across patients, our BCI-driven approach resulted in a statistically significant average increase of 6.2 points in the Action Research Arm Test. This behavioral improvement significantly correlated with improvements in BCI control. Secondary outcomes of grasp strength, Motricity Index, and the Canadian Occupational Performance Measure also significantly improved.

Conclusions: The findings demonstrate the therapeutic potential of a BCI-driven neurorehabilitation approach using the unaffected hemisphere in this uncontrolled sample of chronic stroke survivors. They also demonstrate that BCI-driven neurorehabilitation can be effectively delivered in the home environment, thus increasing the probability of future clinical translation.

Clinical trial registration: URL: http://www.clinicaltrials.gov. Unique identifier: NCT02552368.

Keywords: arm; brain-computer interface; hand; rehabilitation; stroke.

Figure 1.

Study methodology. A, The exoskeleton used attached to a patient’s affected hand via straps on the forearm, palm of the hand, and intermediate phalanges of the index and middle finger, whereas the thumb was held stationary. The exoskeleton was controlled by a microprocessor in the forearm assembly that processed electroencephalographic (EEG) signals. A linear actuator drove hand movements in a 3-finger pinch grip based on the decoded EEG. B, The study tested whether training with the brain–computer interface (BCI)–controlled exoskeleton would lead to functional improvements. Patients that met the inclusion criteria completed 3 EEG screenings. Patients with consistent movement-related EEG activations then completed baseline motor evaluations and BCI system training. Finally, patients completed a 12-wk home-based BCI protocol with follow-up motor evaluations at 2-wk intervals.

Figure 2.

Exemplar electroencephalographic (EEG) activity and brain–computer interface (BCI) control. A, During an exemplar laboratory-based screening session, the patient (patient 10, left affected) demonstrated significant decreases in μ- and β-band spectral power bilaterally. The color scale shows signed r² values indicating increases (positive values) and decreases (negative values) in spectral power during motor imagery. A BCI control feature (red box) ipsilateral to the affected hand was chosen (contact C3). B, During a home-based BCI control session, a similar spatiospectral pattern of movement-related EEG activity was observed. C, The mean (±SE) of the hand position in movement and rest trials shows that the patient achieved a high level of BCI control (0% fully closed, 100% fully open).

Figure 3.

Improvement in motor function. A, Each line shows the change in Action Research Arm Test (ARAT) during the study. At completion, 6 of 10 patients had ARAT increases surpassing the minimal clinically important difference (MCID; 5.7 points). B, ARAT increases were related to the rate of change in brain–computer interface (BCI) accuracy (Spearman r=0.75, P=0.013). C, ARAT increases were not related to the time of device use (Spearman r=0.47, P=0.17).

Figure 4.

Summary of outcome measures. Each box shows the distribution of each outcome measurement at baseline and study completion. Boxes show the 25th percentile, median, and 75th percentile; bars indicate the range of values; and outliers >2.7 SDs from the mean are marked with a +. Measures with statistically significant (P<0.05) changes are indicated with an *. ARAT indicates Action Research Arm Test; and COPM, Canadian Occupational Performance Measure.

Figure 5.

Relationship between changes in electroencephalographic (EEG) activity and Action Research Arm Test (ARAT) improvements. Ranked changes in motor function (ARAT) and changes in EEG activations (r² value) per brain–computer interface (BCI) run are shown. A, Analyses were performed using EEG activity at the site and frequency used for BCI control, at the frequency used for BCI control but an electrode in the contralateral hemisphere, at the frequency used for BCI control but an electrode in the frontal lobe (F3; serving as a spatial control), and at the site used for BCI control but at 50 Hz (serving as a spectral control). B, There was a positive relationship that trended toward significance at both the BCI control feature (top left) and in the contralateral motor cortex (top right) but not at a location outside the motor cortex (bottom left) or a task-irrelevant frequency (bottom right).