Brain-machine interfaces for rehabilitation in stroke: A review

BACKGROUND: Motor paralysis after stroke has devastating consequences for the patients, families and caregivers. Although therapies have improved in the recent years, traditional rehabilitation still fails in patients with severe paralysis. Brain-machine interfaces (BMI) have emerged as a promising tool to guide motor rehabilitation interventions as they can be applied to patients with no residual movement. OBJECTIVE: This paper reviews the efficiency of BMI technologies to facilitate neuroplasticity and motor recovery after stroke. METHODS: We provide an overview of the existing rehabilitation therapies for stroke, the rationale behind the use of BMIs for motor rehabilitation, the current state of the art and the results achieved so far with BMI-based interventions, as well as the future perspectives of neural-machine interfaces. RESULTS: Since the first pilot study by Buch and colleagues in 2008, several controlled clinical studies have been conducted, demonstrating the efficacy of BMIs to facilitate functional recovery in completely paralyzed stroke patients with noninvasive technologies such as the electroencephalogram (EEG). CONCLUSIONS: Despite encouraging results, motor rehabilitation based on BMIs is still in a preliminary stage, and further improvements are required to boost its efficacy. Invasive and hybrid approaches are promising and might set the stage for the next generation of stroke rehabilitation therapies.This study was funded by the Bundesministerium für Bildung und Forschung BMBF MOTORBIC (FKZ13GW0053)andAMORSA(FKZ16SV7754), the Deutsche Forschungsgemeinschaft (DFG), the fortüne-Program of the University of Tübingen (2422-0-0 and 2452-0-0), and the Basque GovernmentScienceProgram(EXOTEK:KK2016/00083). NIL was supported by the Basque Government’s scholarship for predoctoral students

On the design of EEG-based movement decoders for completely paralyzed stroke patients

Background: Brain machine interface (BMI) technology has demonstrated its efficacy for rehabilitation of paralyzed chronic stroke patients. The critical component in BMI-training consists of the associative connection (contingency) between the intention and the feedback provided. However, the relationship between the BMI design and its performance in stroke patients is still an open question. Methods: In this study we compare different methodologies to design a BMI for rehabilitation and evaluate their effects on movement intention decoding performance. We analyze the data of 37 chronic stroke patients who underwent 4 weeks of BMI intervention with different types of association between their brain activity and the proprioceptive feedback. We simulate the pseudo-online performance that a BMI would have under different conditions, varying: (1) the cortical source of activity (i.e., ipsilesional, contralesional, bihemispheric), (2) the type of spatial filter applied, (3) the EEG frequency band, (4) the type of classifier; and also evaluated the use of residual EMG activity to decode the movement intentions. Results: We observed a significant influence of the different BMI designs on the obtained performances. Our results revealed that using bihemispheric beta activity with a common average reference and an adaptive support vector machine led to the best classification results. Furthermore, the decoding results based on brain activity were significantly higher than those based on muscle activity. Conclusions: This paper underscores the relevance of the different parameters used to decode movement, using EEG in severely paralyzed stroke patients. We demonstrated significant differences in performance for the different designs, which supports further research that should elucidate if those approaches leading to higher accuracies also induce higher motor recovery in paralyzed stroke patients.This study was funded by the Baden-Württemberg Stiftung (GRUENS ROB-1), the Deutsche Forschungsgemeinschaft (DFG, Koselleck and Grant SP 1533/2– 1), the Bundesministerium für Bildung und Forschung BMBF: MOTORBIC (FKZ 13GW0053) and AMORSA (FKZ 16SV7754), the fortüne-Program of the University of Tübingen (2422-0-1 and 2452-0-0) and the Basque Government Science Program (EXOTEK: KK 2016/00083)

Event-related desynchronization during movement attempt and execution in severely paralyzed stroke patients: An artifact removal relevance analysis

The electroencephalogram (EEG) constitutes a relevant tool to study neural dynamics and to develop brain-machine interfaces (BMI) for rehabilitation of patients with paralysis due to stroke. However, the EEG is easily contaminated by artifacts of physiological origin, which can pollute the measured cortical activity and bias the interpretations of such data. This is especially relevant when recording EEG of stroke patients while they try to move their paretic limbs, since they generate more artifacts due to compensatory activity. In this paper, we study how physiological artifacts (i.e., eye movements, motion artifacts, muscle artifacts and compensatory movements with the other limb) can affect EEG activity of stroke patients. Data from 31 severely paralyzed stroke patients performing/attempting grasping movements with their healthy/paralyzed hand were analyzed offline. We estimated the cortical activation as the event-related desynchronization (ERD) of sensorimotor rhythms and used it to detect the movements with a pseudo-online simulated BMI. Automated state-of-the-art methods (linear regression to remove ocular contaminations and statistical thresholding to reject the other types of artifacts) were used to minimize the influence of artifacts. The effect of artifact reduction was quantified in terms of ERD and BMI performance. The results reveal a significant contamination affecting the EEG, being involuntary muscle activity the main source of artifacts. Artifact reduction helped extracting the oscillatory signatures of motor tasks, isolating relevant information from noise and revealing a more prominent ERD activity. Lower BMI performances were obtained when artifacts were eliminated from the training datasets. This suggests that artifacts produce an optimistic bias that improves theoretical accuracy but may result in a poor link between task-related oscillatory activity and BMI peripheral feedback. With a clinically relevant dataset of stroke patients, we evidence the need of appropriate methodologies to remove artifacts from EEG datasets to obtain accurate estimations of the motor brain activity.This study was funded by the fortüne-Program of the University of Tübingen (2422-0-1 and 2452-0-0), the Bundesministerium für Bildung und Forschung BMBF MOTORBIC (FKZ 13GW0053) and AMORSA (FKZ 16SV7754), the Deutsche Forschungsgemeinschaft (DFG), the Basque Government Science Program (EXOTEK: KK 2016/00083). The work of A. Insausti-Delgado was supported by the Basque Government's scholarship for predoctoral students

BCI controlled robotic arm as assistance to the rehabilitation of neurologically disabled patients

This presentation summarises the development of a portable and cost-efficient BCI controlled assistive technology using a non-invasive BCI headset 'OpenBCI' and an open source robotic arm, U-Arm, to accomplish tasks related to rehabilitation, such as access to resources, adaptability or home use. The resulting system used a combination of EEG and EMG sensor readings to control the arm, which could perform a number of different tasks such as picking/placing objects or assist users in eating

EEG and ECoG features for Brain Computer Interface in Stroke Rehabilitation

The ability of non-invasive Brain-Computer Interface (BCI) to control an exoskeleton was used for motor rehabilitation in stroke patients or as an assistive device for the paralyzed. However, there is still a need to create a more reliable BCI that could be used to control several degrees of Freedom (DoFs) that could improve rehabilitation results. Decoding different movements from the same limb, high accuracy and reliability are some of the main difficulties when using conventional EEG-based BCIs and the challenges we tackled in this thesis. In this PhD thesis, we investigated that the classification of several functional hand reaching movements from the same limb using EEG is possible with acceptable accuracy. Moreover, we investigated how the recalibration could affect the classification results. For this reason, we tested the recalibration in each multi-class decoding for within session, recalibrated between-sessions, and between sessions. It was shown the great influence of recalibrating the generated classifier with data from the current session to improve stability and reliability of the decoding. Moreover, we used a multiclass extension of the Filter Bank Common Spatial Patterns (FBCSP) to improve the decoding accuracy based on features and compared it to our previous study using CSP. Sensorimotor-rhythm-based BCI systems have been used within the same frequency ranges as a way to influence brain plasticity or controlling external devices. However, neural oscillations have shown to synchronize activity according to motor and cognitive functions. For this reason, the existence of cross-frequency interactions produces oscillations with different frequencies in neural networks. In this PhD, we investigated for the first time the existence of cross-frequency coupling during rest and movement using ECoG in chronic stroke patients. We found that there is an exaggerated phase-amplitude coupling between the phase of alpha frequency and the amplitude of gamma frequency, which can be used as feature or target for neurofeedback interventions using BCIs. This coupling has been also reported in another neurological disorder affecting motor function (Parkinson and dystonia) but, to date, it has not been investigated in stroke patients. This finding might change the future design of assistive or therapeuthic BCI systems for motor restoration in stroke patients

Challenges of neural interfaces for stroke motor rehabilitation

More than 85% of stroke survivors suffer from different degrees of disability for the rest of their lives. They will require support that can vary from occasional to full time assistance. These conditions are also associated to an enormous economic impact for their families and health care systems. Current rehabilitation treatments have limited efficacy and their long-term effect is controversial. Here we review different challenges related to the design and development of neural interfaces for rehabilitative purposes. We analyze current bibliographic evidence of the effect of neuro-feedback in functional motor rehabilitation of stroke patients. We highlight the potential of these systems to reconnect brain and muscles. We also describe all aspects that should be taken into account to restore motor control. Our aim with this work is to help researchers designing interfaces that demonstrate and validate neuromodulation strategies to enforce a contingent and functional neural linkage between the central and the peripheral nervous system. We thus give clues to design systems that can improve or/and re-activate neuroplastic mechanisms and open a new recovery window for stroke patients

Analysis of Human Gait Using Hybrid EEG-fNIRS-Based BCI System: A Review

Human gait is a complex activity that requires high coordination between the central nervous system, the limb, and the musculoskeletal system. More research is needed to understand the latter coordination\u27s complexity in designing better and more effective rehabilitation strategies for gait disorders. Electroencephalogram (EEG) and functional near-infrared spectroscopy (fNIRS) are among the most used technologies for monitoring brain activities due to portability, non-invasiveness, and relatively low cost compared to others. Fusing EEG and fNIRS is a well-known and established methodology proven to enhance brain–computer interface (BCI) performance in terms of classification accuracy, number of control commands, and response time. Although there has been significant research exploring hybrid BCI (hBCI) involving both EEG and fNIRS for different types of tasks and human activities, human gait remains still underinvestigated. In this article, we aim to shed light on the recent development in the analysis of human gait using a hybrid EEG-fNIRS-based BCI system. The current review has followed guidelines of preferred reporting items for systematic reviews and meta-Analyses (PRISMA) during the data collection and selection phase. In this review, we put a particular focus on the commonly used signal processing and machine learning algorithms, as well as survey the potential applications of gait analysis. We distill some of the critical findings of this survey as follows. First, hardware specifications and experimental paradigms should be carefully considered because of their direct impact on the quality of gait assessment. Second, since both modalities, EEG and fNIRS, are sensitive to motion artifacts, instrumental, and physiological noises, there is a quest for more robust and sophisticated signal processing algorithms. Third, hybrid temporal and spatial features, obtained by virtue of fusing EEG and fNIRS and associated with cortical activation, can help better identify the correlation between brain activation and gait. In conclusion, hBCI (EEG + fNIRS) system is not yet much explored for the lower limb due to its complexity compared to the higher limb. Existing BCI systems for gait monitoring tend to only focus on one modality. We foresee a vast potential in adopting hBCI in gait analysis. Imminent technical breakthroughs are expected using hybrid EEG-fNIRS-based BCI for gait to control assistive devices and Monitor neuro-plasticity in neuro-rehabilitation. However, although those hybrid systems perform well in a controlled experimental environment when it comes to adopting them as a certified medical device in real-life clinical applications, there is still a long way to go

Enhancing brain/neural-machine interfaces for upper limb motor restoration in chronic stroke and cervical spinal cord injury

Operation of assistive exoskeletons based on voluntary control of sensorimotor rhythms (SMR, 8-12 Hz) enables intuitive control of finger or arm movements in severe paralysis after chronic stroke or cervical spinal cord injury (SCI). To improve reliability of such systems outside the laboratory, in particular when brain activity is recorded non-invasively with scalp electroencephalography (EEG), a hybrid EEG/electrooculography (EOG) brain/neural-machine interface (B/NMI) was recently introduced. Besides providing assistance, recent studies indicate that repeated use of such systems can trigger neural recovery. However, important prerequisites have to achieved before broader use in clinical settings or everyday life environments is feasible. Current B/NMI systems predominantly restore hand function, but do not allow simultaneous control of more proximal joints for whole-arm motor coordination as required for most stroke survivors suffering from paralysis in the entire upper limb. Besides paralysis, cognitive impairments including post-stroke fatigue due to the brain lesion reduce the capacity to maintain effortful B/NMI control over a longer period of time. This impedes the applicability in daily life assistance and might even limits the efficacy of neurorehabilitation training. In contrast to stroke survivors, tetraplegics due to cervical SCI lack motor function in both hands. Given that most activities of daily living (ADL) involve bimanual manipulation, e.g., to open the lid of a bottle, bilateral exoskeleton control is required but was not shown yet in tetraplegics. To further enhance B/NMI systems, we first investigated whether B/NMI whole-arm exoskeleton control in hemiplegia after chronic stroke is feasible and safe. In contrast to simple grasping, control of more complex tasks involving the entire upper limb was not feasible with established B/NMIs because high- dimensionality of such multiple joint systems exceeds the bandwidth of these interfaces. Thus, we blended B/NMI control with vision-guidance to receive a semiautonomous whole-arm exoskeleton control. Such setup allowed to divide ADL tasks into a sequence of EEG/EOG-triggered sub-tasks reducing complexity for the user. While, for instance, a drinking task was resolved into EOG-induced reaching, lifting and placing back the cup, grasping and releasing movements were based on intuitive SMR control. Feasibility of such shared vision-guided B/NMI control was assumed when executions were initialized within 3 s (fluent control) and a minimum of 75 % of subtasks were executed within that time (reliable control). We showed feasibility in healthy subjects as well as stroke survivors without report of any side effects documenting safe use. Similarly, feasibility and safety of bilateral B/NMI control after cervical SCI was evaluated. To enable bilateral B/NMI control, established EEG-based grasping and EOG-based releasing or stop commands were complemented with a novel EOG command allowing to switch laterality by performing prolonged horizontal eye movements (>1 s) to the left or to the right. Study results with healthy subjects and tetraplegics document fluent initialization of grasping motions below 3 s as well as safe use as unintended grasping could be stopped before a full motion was conducted. Superiority of novel bilateral control was documented by a higher accuracy of up to 22 % in tetraplegics compared to a bilateral control without prolonged EOG command. Lastly, as reliable B/NMI control is cognitively demanding, e.g., by imagining or attempting the desired movements, we investigated whether heart rate variability (HRV) can be used as biomarker to predict declining control performance, which is often reported in stroke survivors due to their cognitive impairments. Referring to the close brain-heart connection, we showed in healthy subjects that a decline in HRV is specific as well as predictive to a decline in B/NMI control performance within a single training session. The predictive link was revealed by a Granger-causality analysis. In conclusion, we could demonstrate important enhancements in B/NMI control paradigms including complex whole-arm exoskeleton control as well as individual performance monitoring within a training session based on HRV. Both achievements contribute to broaden the use as a standard therapy in stroke neurorehabilitation. Especially the predictive characteristic of HRV paves the way for adaptive B/NMI control paradigms to account for individual differences among impaired stroke survivors. Moreover, we also showed feasibility and safety of a novel implementation for bilateral B/NMI control, which is necessary for reliable operation of two hand-exoskeletons for bimanual ADLs after SCI

An EEG-EMG Correlation-based Brain-Computer Interface for Hand Orthosis Supported Neuro-Rehabilitation

Background Corticomuscular coupling has been investigated for long, to find out the underlying mechanisms behind cortical drives to produce different motor tasks. Although important in rehabilitation perspective, the use of corticomuscular coupling for driving brain-computer interface (BCI)-based neurorehabilitation is much ignored. This is primarily due to the fact that the EEG-EMG coherence popularly used to compute corticomuscular coupling, fails to produce sufficient accuracy in single-trial based prediction of motor tasks in a BCI system. New Method In this study, we have introduced a new corticomuscular feature extraction method based on the correlation between band-limited power time-courses (CBPT) associated with EEG and EMG. 16 healthy individuals and 8 hemiplegic patients participated in a BCI-based hand orthosis triggering task, to test the performance of the CBPT method. The healthy population was equally divided into two groups; one experimental group for CBPT-based BCI experiment and another control group for EEG-EMG coherence based BCI experiment. Results The classification accuracy of the CBPT-based BCI system was found to be 92.81±2.09% for the healthy experimental group and 84.53±4.58% for the patients’ group. Comparison with existing method The CBPT method significantly (p−value < 0.05) outperformed the conventional EEG-EMG coherence method in terms of classification accuracy. Conclusions The experimental results clearly indicate that the EEG-EMG CBPT is a better alternative as a corticomuscular feature to drive a BCI system. Additionally, it is also feasible to use the proposed method to design BCI-based robotic neurorehabilitation paradigms