Using Transcranial Direct Current Stimulation to Augment the Effect of Motor Imagery-Assisted Brain-Computer Interface Training in Chronic Stroke Patients-Cortical Reorganization Considerations

Effie Chew, Wei-Peng Teo, Ning Tang, Kai Keng Ang, Yee Sien Ng, Juan Helen Zhou, Irvin Teh, Kok Soon Phua, Ling Zhao, Cuntai Guan, Effie Chew, Wei-Peng Teo, Ning Tang, Kai Keng Ang, Yee Sien Ng, Juan Helen Zhou, Irvin Teh, Kok Soon Phua, Ling Zhao, Cuntai Guan

Abstract

Introduction: Transcranial direct current stimulation (tDCS) has been shown to modulate cortical plasticity, enhance motor learning and post-stroke upper extremity motor recovery. It has also been demonstrated to facilitate activation of brain-computer interface (BCI) in stroke patients. We had previously demonstrated that BCI-assisted motor imagery (MI-BCI) can improve upper extremity impairment in chronic stroke participants. This study was carried out to investigate the effects of priming with tDCS prior to MI-BCI training in chronic stroke patients with moderate to severe upper extremity paresis and to investigate the cortical activity changes associated with training. Methods: This is a double-blinded randomized clinical trial. Participants were randomized to receive 10 sessions of 20-min 1 mA tDCS or sham-tDCS before MI-BCI, with the anode applied to the ipsilesional, and the cathode to the contralesional primary motor cortex (M1). Upper extremity sub-scale of the Fugl-Meyer Assessment (UE-FM) and corticospinal excitability measured by transcranial magnetic stimulation (TMS) were assessed before, after and 4 weeks after intervention. Results: Ten participants received real tDCS and nine received sham tDCS. UE-FM improved significantly in both groups after intervention. Of those with unrecordable motor evoked potential (MEP-) to the ipsilesional M1, significant improvement in UE-FM was found in the real-tDCS group, but not in the sham group. Resting motor threshold (RMT) of ipsilesional M1 decreased significantly after intervention in the real-tDCS group. Short intra-cortical inhibition (SICI) in the contralesional M1 was reduced significantly following intervention in the sham group. Correlation was found between baseline UE-FM score and changes in the contralesional SICI for all, as well as between changes in UE-FM and changes in contralesional RMT in the MEP- group. Conclusion: MI-BCI improved the motor function of the stroke-affected arm in chronic stroke patients with moderate to severe impairment. tDCS did not confer overall additional benefit although there was a trend toward greater benefit. Cortical activity changes in the contralesional M1 associated with functional improvement suggests a possible role for the contralesional M1 in stroke recovery in more severely affected patients. This has important implications in designing neuromodulatory interventions for future studies and tailoring treatment. Clinical Trial Registration: The study was registered at https://ichgcp.net/clinical-trials-registry/NCT01897025" title="See in ClinicalTrials.gov">NCT01897025).

Keywords: brain-computer interface; motor imagery; motor recovery; stroke; transcranial direct current stimulation.

Copyright © 2020 Chew, Teo, Tang, Ang, Ng, Zhou, Teh, Phua, Zhao and Guan.

Figures

Figure 1
Figure 1
CONSORT flow diagram. Forty-two participants were screened. Nineteen participants completed the intervention and follow-up evaluation and were included in the final analysis−10 in the real-tDCS group, nine in the sham-tDCS group.
Figure 2
Figure 2
UE-FM score (A) and ΔUE-FM (B) in both groups. (A) Both groups improved significantly in UE-FM at POST2 after intervention (n = 10 for real-tDCS group, n = 9 for sham-tDCS group). Between group difference was not statistically significant. (B) ΔUE-FM (changes in UE-FM score compared to PRE) was significantly higher at POST2, compared to POST1 in the real-tDCS group, not in the sham group. Data shows mean ± SEM.
Figure 3
Figure 3
UE-FM (A) and ΔUE-FM (B) in both groups in MEP- participants. (A) Significant improvement in UE-FM in the real-tDCS group (n = 6), but not the sham-tDCS group (n = 5). (B) No significant difference in ΔUE-FM was shown between groups, or over time. Data shows mean ± SEM.
Figure 4
Figure 4
RMT in the ipsilesional M1 (A) and contralesional M1 (B). (A) Significant reduction in RMT in ipsilesional M1 in real-tDCS (n = 6) group at POST1 and POST2, compared to PRE, but not in sham-tDCS group (n = 5). The overall difference between groups was statistically significant. (B) No significant difference in RMT in contralesional side between two groups (n = 10 for real-tDCS group, n = 9 for sham-tDCS group), or over time. Data shows mean ± SEM.
Figure 5
Figure 5
SICI (ISI 2ms) in contralesional M1 in both groups. The sham-tDCS group (n = 9) had significantly reduced SICI2ms at POST1 and POST2, compared PRE. No difference over time was observed in real-tDCS group (n = 10). Between-group difference was not significant.

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