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Brain-machine interface in chronic stroke rehabilitation: a controlled study.

ABSTRACT: OBJECTIVE:Chronic stroke patients with severe hand weakness respond poorly to rehabilitation efforts. Here, we evaluated efficacy of daily brain-machine interface (BMI) training to increase the hypothesized beneficial effects of physiotherapy alone in patients with severe paresis in a double-blind sham-controlled design proof of concept study. METHODS:Thirty-two chronic stroke patients with severe hand weakness were randomly assigned to 2 matched groups and participated in 17.8 ± 1.4 days of training rewarding desynchronization of ipsilesional oscillatory sensorimotor rhythms with contingent online movements of hand and arm orthoses (experimental group, n = 16). In the control group (sham group, n = 16), movements of the orthoses occurred randomly. Both groups received identical behavioral physiotherapy immediately following BMI training or the control intervention. Upper limb motor function scores, electromyography from arm and hand muscles, placebo-expectancy effects, and functional magnetic resonance imaging (fMRI) blood oxygenation level-dependent activity were assessed before and after intervention. RESULTS:A significant group × time interaction in upper limb (combined hand and modified arm) Fugl-Meyer assessment (cFMA) motor scores was found. cFMA scores improved more in the experimental than in the control group, presenting a significant improvement of cFMA scores (3.41 ± 0.563-point difference, p = 0.018) reflecting a clinically meaningful change from no activity to some in paretic muscles. cFMA improvements in the experimental group correlated with changes in fMRI laterality index and with paretic hand electromyography activity. Placebo-expectancy scores were comparable for both groups. INTERPRETATION:The addition of BMI training to behaviorally oriented physiotherapy can be used to induce functional improvements in motor function in chronic stroke patients without residual finger movements and may open a new door in stroke neurorehabilitation.

SUBMITTER: Ramos-Murguialday A

PROVIDER: S-EPMC3700597 | biostudies-literature | 2013 Jul

REPOSITORIES: biostudies-literature

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Brain-machine interface in chronic stroke rehabilitation: a controlled study.

Ramos-Murguialday Ander A Broetz Doris D Rea Massimiliano M Läer Leonhard L Yilmaz Ozge O Brasil Fabricio L FL Liberati Giulia G Curado Marco R MR Garcia-Cossio Eliana E Vyziotis Alexandros A Cho Woosang W Agostini Manuel M Soares Ernesto E Soekadar Surjo S Caria Andrea A Cohen Leonardo G LG Birbaumer Niels N

Annals of neurology 20130701 1

<h4>Objective</h4>Chronic stroke patients with severe hand weakness respond poorly to rehabilitation efforts. Here, we evaluated efficacy of daily brain-machine interface (BMI) training to increase the hypothesized beneficial effects of physiotherapy alone in patients with severe paresis in a double-blind sham-controlled design proof of concept study.<h4>Methods</h4>Thirty-two chronic stroke patients with severe hand weakness were randomly assigned to 2 matched groups and participated in 17.8 ± ...[more]

PMID: 23494615

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Project description:The primary goal of this work was to apply data-driven machine learning regression to assess if resting state functional connectivity (rs-FC) could estimate measures of behavioral domains in stroke subjects who completed brain-computer interface (BCI) intervention for motor rehabilitation. The study cohort consisted of 20 chronic-stage stroke subjects exhibiting persistent upper-extremity motor deficits who received the intervention using a closed-loop neurofeedback BCI device. Over the course of this intervention, resting state functional MRI scans were collected at four distinct time points: namely, pre-intervention, mid-intervention, post-intervention and 1-month after completion of intervention. Behavioral assessments were administered outside the scanner at each time-point to collect objective measures such as the Action Research Arm Test, Nine-Hole Peg Test, and Barthel Index as well as subjective measures including the Stroke Impact Scale. The present analysis focused on neuroplasticity and behavioral outcomes measured across pre-intervention, post-intervention and 1-month post-intervention to study immediate and carry-over effects. Rs-FC, changes in rs-FC within the motor network and the behavioral measures at preceding stages were used as input features and behavioral measures and associated changes at succeeding stages were used as outcomes for machine-learning-based support vector regression (SVR) models. Potential clinical confounding factors such as age, gender, lesion hemisphere, and stroke severity were included as additional features in each of the regression models. Sequential forward feature selection procedure narrowed the search for important correlates. Behavioral outcomes at preceding time-points outperformed rs-FC-based correlates. Rs-FC and changes associated with bilateral primary motor areas were found to be important correlates of across several behavioral outcomes and were stable upon inclusion of clinical variables as well. NIH Stroke Scale and motor impairment severity were the most influential clinical variables. Comparatively, linear SVR models aided in evaluation of contribution of individual correlates and seed regions while non-linear SVR models achieved higher performance in prediction of behavioral outcomes.

Project description:Interventional therapy using brain-computer interface (BCI) technology has shown promise in facilitating motor recovery in stroke survivors; however, the impact of this form of intervention on functional networks outside of the motor network specifically is not well-understood. Here, we investigated resting-state functional connectivity (rs-FC) in stroke participants undergoing BCI therapy across stages, namely pre- and post-intervention, to identify discriminative functional changes using a machine learning classifier with the goal of categorizing participants into one of the two therapy stages. Twenty chronic stroke participants with persistent upper-extremity motor impairment received neuromodulatory training using a closed-loop neurofeedback BCI device, and rs-functional MRI (rs-fMRI) scans were collected at four time points: pre-, mid-, post-, and 1 month post-therapy. To evaluate the peak effects of this intervention, rs-FC was analyzed from two specific stages, namely pre- and post-therapy. In total, 236 seeds spanning both motor and non-motor regions of the brain were computed at each stage. A univariate feature selection was applied to reduce the number of features followed by a principal component-based data transformation used by a linear binary support vector machine (SVM) classifier to classify each participant into a therapy stage. The SVM classifier achieved a cross-validation accuracy of 92.5% using a leave-one-out method. Outside of the motor network, seeds from the fronto-parietal task control, default mode, subcortical, and visual networks emerged as important contributors to the classification. Furthermore, a higher number of functional changes were observed to be strengthening from the pre- to post-therapy stage than the ones weakening, both of which involved motor and non-motor regions of the brain. These findings may provide new evidence to support the potential clinical utility of BCI therapy as a form of stroke rehabilitation that not only benefits motor recovery but also facilitates recovery in other brain networks. Moreover, delineation of stronger and weaker changes may inform more optimal designs of BCI interventional therapy so as to facilitate strengthened and suppress weakened changes in the recovery process.

Project description:Stroke is a leading cause of persistent upper extremity (UE) motor disability in adults. Brain-computer interface (BCI) intervention has demonstrated potential as a motor rehabilitation strategy for stroke survivors. This sub-analysis of ongoing clinical trial (NCT02098265) examines rehabilitative efficacy of this BCI design and seeks to identify stroke participant characteristics associated with behavioral improvement. Stroke participants (n = 21) with UE impairment were assessed using Action Research Arm Test (ARAT) and measures of function. Nine participants completed three assessments during the experimental BCI intervention period and at 1-month follow-up. Twelve other participants first completed three assessments over a parallel time-matched control period and then crossed over into the BCI intervention condition 1-month later. Participants who realized positive change (≥1 point) in total ARAT performance of the stroke affected UE between the first and third assessments of the intervention period were dichotomized as "responders" (<1 = "non-responders") and similarly analyzed. Of the 14 participants with room for ARAT improvement, 64% (9/14) showed some positive change at completion and approximately 43% (6/14) of the participants had changes of minimal detectable change (MDC = 3 pts) or minimally clinical important difference (MCID = 5.7 points). Participants with room for improvement in the primary outcome measure made significant mean gains in ARATtotal score at completion (ΔARATtotal = 2, p = 0.028) and 1-month follow-up (ΔARATtotal = 3.4, p = 0.0010), controlling for severity, gender, chronicity, and concordance. Secondary outcome measures, SISmobility, SISadl, SISstrength, and 9HPTaffected, also showed significant improvement over time during intervention. Participants in intervention through follow-up showed a significantly increased improvement rate in SISstrength compared to controls (p = 0.0117), controlling for severity, chronicity, gender, as well as the individual effects of time and intervention type. Participants who best responded to BCI intervention, as evaluated by ARAT score improvement, showed significantly increased outcome values through completion and follow-up for SISmobility (p = 0.0002, p = 0.002) and SISstrength (p = 0.04995, p = 0.0483). These findings may suggest possible secondary outcome measure patterns indicative of increased improvement resulting from this BCI intervention regimen as well as demonstrating primary efficacy of this BCI design for treatment of UE impairment in stroke survivors. Clinical Trial Registration: ClinicalTrials.gov, NCT02098265.

Project description:Brain-computer interfaces (BCIs) are an emerging novel technology for stroke rehabilitation. Little is known about how dose-response relationships for BCI therapies affect brain and behavior changes. We report preliminary results on stroke patients (n = 16, 11 M) with persistent upper extremity motor impairment who received therapy using a BCI system with functional electrical stimulation of the hand and tongue stimulation. We collected MRI scans and behavioral data using the Action Research Arm Test (ARAT), 9-Hole Peg Test (9-HPT), and Stroke Impact Scale (SIS) before, during, and after the therapy period. Using anatomical and functional MRI, we computed Laterality Index (LI) for brain activity in the motor network during impaired hand finger tapping. Changes from baseline LI and behavioral scores were assessed for relationships with dose, intensity, and frequency of BCI therapy. We found that gains in SIS Strength were directly responsive to BCI therapy: therapy dose and intensity correlated positively with increased SIS Strength (p ≤ 0.05), although no direct relationships were identified with ARAT or 9-HPT scores. We found behavioral measures that were not directly sensitive to differences in BCI therapy administration but were associated with concurrent brain changes correlated with BCI therapy administration parameters: therapy dose and intensity showed significant (p ≤ 0.05) or trending (0.05 < p < 0.1) negative correlations with LI changes, while therapy frequency did not affect LI. Reductions in LI were then correlated (p ≤ 0.05) with increased SIS Activities of Daily Living scores and improved 9-HPT performance. Therefore, some behavioral changes may be reflected by brain changes sensitive to differences in BCI therapy administration, while others such as SIS Strength may be directly responsive to BCI therapy administration. Data preliminarily suggest that when using BCI in stroke rehabilitation, therapy frequency may be less important than dose and intensity.

Project description:BackgroundWe developed a brain-machine interface (BMI) system for poststroke patients with severe hemiplegia to detect event-related desynchronization (ERD) on scalp electroencephalogram (EEG) and to operate a motor-driven hand orthosis combined with neuromuscular electrical stimulation. ERD arises when the excitability of the ipsi-lesional sensorimotor cortex increases.ObjectiveThe aim of this study was to evaluate our hypothesis that motor training using this BMI system could improve severe hemiparesis that is resistant to improvement by conventional rehabilitation. We, therefore, planned and implemented a randomized controlled clinical trial (RCT) to evaluate the effectiveness and safety of intensive rehabilitation using the BMI system.MethodsWe conducted a single blind, multicenter RCT and recruited chronic poststroke patients with severe hemiparesis more than 90 days after onset (N=40). Participants were randomly allocated to the BMI group (n=20) or the control group (n=20). Patients in the BMI group repeated 10-second motor attempts to operate EEG-BMI 40 min every day followed by 40 min of conventional occupational therapy. The interventions were repeated 10 times in 2 weeks. Control participants performed a simple motor imagery without servo-action of the orthosis, and electrostimulation was given for 10 seconds for 40 min, similar to the BMI intervention. Overall, 40 min of conventional occupational therapy was also given every day after the control intervention, which was also repeated 10 times in 2 weeks. Motor functions and electrophysiological phenotypes of the paretic hands were characterized before (baseline), immediately after (post), and 4 weeks after (follow-up) the intervention. Improvement in the upper extremity score of the Fugl-Meyer assessment between baseline and follow-up was the main outcome of this study.ResultsRecruitment started in March 2017 and ended in July 2018. This trial is currently in the data correcting phase. This RCT is expected to be completed by October 31, 2018.ConclusionsNo widely accepted intervention has been established to improve finger function of chronic poststroke patients with severe hemiparesis. The results of this study will provide clinical data for regulatory approval and novel, important understanding of the role of sensory-motor feedback based on BMI to induce neural plasticity and motor recovery.Trial registrationUMIN Clinical Trials Registry UMIN000026372; https://upload.umin.ac.jp/cgi-open-bin/ctr_e/ctr_view.cgi? recptno=R000030299 (Archived by WebCite at http://www.webcitation.org/743zBJj3D).International registered report identifier (irrid)DERR1-10.2196/12339.

Project description:Repeated use of brain-computer interfaces (BCIs) providing contingent sensory feedback of brain activity was recently proposed as a rehabilitation approach to restore motor function after stroke or spinal cord lesions. However, there are only a few clinical studies that investigate feasibility and effectiveness of such an approach. Here we report on a placebo-controlled, multicenter clinical trial that investigated whether stroke survivors with severe upper limb (UL) paralysis benefit from 10 BCI training sessions each lasting up to 40 min. A total of 74 patients participated: median time since stroke is 8 months, 25 and 75% quartiles [3.0; 13.0]; median severity of UL paralysis is 4.5 points [0.0; 30.0] as measured by the Action Research Arm Test, ARAT, and 19.5 points [11.0; 40.0] as measured by the Fugl-Meyer Motor Assessment, FMMA. Patients in the BCI group (n = 55) performed motor imagery of opening their affected hand. Motor imagery-related brain electroencephalographic activity was translated into contingent hand exoskeleton-driven opening movements of the affected hand. In a control group (n = 19), hand exoskeleton-driven opening movements of the affected hand were independent of brain electroencephalographic activity. Evaluation of the UL clinical assessments indicated that both groups improved, but only the BCI group showed an improvement in the ARAT's grasp score from 0 [0.0; 14.0] to 3.0 [0.0; 15.0] points (p < 0.01) and pinch scores from 0.0 [0.0; 7.0] to 1.0 [0.0; 12.0] points (p < 0.01). Upon training completion, 21.8% and 36.4% of the patients in the BCI group improved their ARAT and FMMA scores respectively. The corresponding numbers for the control group were 5.1% (ARAT) and 15.8% (FMMA). These results suggests that adding BCI control to exoskeleton-assisted physical therapy can improve post-stroke rehabilitation outcomes. Both maximum and mean values of the percentage of successfully decoded imagery-related EEG activity, were higher than chance level. A correlation between the classification accuracy and the improvement in the upper extremity function was found. An improvement of motor function was found for patients with different duration, severity and location of the stroke.

Dataset Information

Brain-machine interface in chronic stroke rehabilitation: a controlled study.

Publications

Brain-machine interface in chronic stroke rehabilitation: a controlled study.

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