A hybrid brain-muscle-machine interface for stroke rehabilitation: Usability and functionality validation in a 2-week intensive intervention.

Introduction: The primary constraint of non-invasive brain-machine interfaces (BMIs) in stroke rehabilitation lies in the poor spatial resolution of motor intention related neural activity capture. To address this limitation, hybrid brain-muscle-machine interfaces (hBMIs) have been suggested as superior alternatives. These hybrid interfaces incorporate supplementary input data from muscle signals to enhance the accuracy, smoothness and dexterity of rehabilitation device control. Nevertheless, determining the distribution of control between the brain and muscles is a complex task, particularly when applied to exoskeletons with multiple degrees of freedom (DoFs). Here we present a feasibility, usability and functionality study of a bio-inspired hybrid brain-muscle machine interface to continuously control an upper limb exoskeleton with 7 DoFs. Methods: The system implements a hierarchical control strategy that follows the biologically natural motor command pathway from the brain to the muscles. Additionally, it employs an innovative mirror myoelectric decoder, offering patients a reference model to assist them in relearning healthy muscle activation patterns during training. Furthermore, the multi-DoF exoskeleton enables the practice of coordinated arm and hand movements, which may facilitate the early use of the affected arm in daily life activities. In this pilot trial six chronic and severely paralyzed patients controlled the multi-DoF exoskeleton using their brain and muscle activity. The intervention consisted of 2 weeks of hBMI training of functional tasks with the system followed by physiotherapy. Patients' feedback was collected during and after the trial by means of several feedback questionnaires. Assessment sessions comprised clinical scales and neurophysiological measurements, conducted prior to, immediately following the intervention, and at a 2-week follow-up. Results: Patients' feedback indicates a great adoption of the technology and their confidence in its rehabilitation potential. Half of the patients showed improvements in their arm function and 83% improved their hand function. Furthermore, we found improved patterns of muscle activation as well as increased motor evoked potentials after the intervention. Discussion: This underscores the significant potential of bio-inspired interfaces that engage the entire nervous system, spanning from the brain to the muscles, for the rehabilitation of stroke patients, even those who are severely paralyzed and in the chronic phase.

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.

Real-Time Control of a Multi-Degree-of-Freedom Mirror Myoelectric Interface During Functional Task Training.

Motor learning mediated by motor training has in the past been explored for rehabilitation. Myoelectric interfaces together with exoskeletons allow patients to receive real-time feedback about their muscle activity. However, the number of degrees of freedom that can be simultaneously controlled is limited, which hinders the training of functional tasks and the effectiveness of the rehabilitation therapy. The objective of this study was to develop a myoelectric interface that would allow multi-degree-of-freedom control of an exoskeleton involving arm, wrist and hand joints, with an eye toward rehabilitation. We tested the effectiveness of a myoelectric decoder trained with data from one upper limb and mirrored to control a multi-degree-of-freedom exoskeleton with the opposite upper limb (i.e., mirror myoelectric interface) in 10 healthy participants. We demonstrated successful simultaneous control of multiple upper-limb joints by all participants. We showed evidence that subjects learned the mirror myoelectric model within the span of a five-session experiment, as reflected by a significant decrease in the time to execute trials and in the number of failed trials. These results are the necessary precursor to evaluating if a decoder trained with EMG from the healthy limb could foster learning of natural EMG patterns and lead to motor rehabilitation in stroke patients.

Functional synergy recruitment index as a reliable biomarker of motor function and recovery in chronic stroke patients.

Objective. Stroke affects the expression of muscle synergies underlying motor control, most notably in patients with poorer motor function. The majority of studies on muscle synergies have conventionally approached this analysis by assuming alterations in the inner structures of synergies after stroke. Although different synergy-based features based on this assumption have to some extent described pathological mechanisms in post-stroke neuromuscular control, a biomarker that reliably reflects motor function and recovery is still missing.Approach. Based on the theory of muscle synergies, we alternatively hypothesize that functional synergy structures are physically preserved and measure the temporal correlation between the recruitment profiles of healthy modules by paretic and healthy muscles, a feature hereafter reported as the FSRI. We measured clinical scores and extracted the muscle synergies of both ULs of 18 chronic stroke survivors from the electromyographic activity of 8 muscles during bilateral movements before and after 4 weeks of non-invasive BMI controlled robot therapy and physiotherapy. We computed the FSRI as well as features quantifying inter-limb structural differences and evaluated the correlation of these synergy-based measures with clinical scores.Main results. Correlation analysis revealed weak relationships between conventional features describing inter-limb synergy structural differences and motor function. In contrast, FSRI values during specific or combined movement data significantly correlated with UL motor function and recovery scores. Additionally, we observed that BMI-based training with contingent positive proprioceptive feedback led to improved FSRI values during the specific trained finger extension movement.Significance. We demonstrated that FSRI can be used as a reliable physiological biomarker of motor function and recovery in stroke, which can be targeted via BMI-based proprioceptive therapies and adjuvant physiotherapy to boost effective rehabilitation.

Design and effectiveness evaluation of mirror myoelectric interfaces: a novel method to restore movement in hemiplegic patients.

The motor impairment occurring after a stroke is characterized by pathological muscle activation patterns or synergies. However, while robot-aided myoelectric interfaces have been proposed for stroke rehabilitation, they do not address this issue, which might result in inefficient interventions. Here, we present a novel paradigm that relies on the correction of the pathological muscle activity as a way to elicit rehabilitation, even in patients with complete paralysis. Previous studies demonstrated that there are no substantial inter-limb differences in the muscle synergy organization of healthy individuals. We propose building a subject-specific model of muscle activity from the healthy limb and mirroring it to use it as a learning tool for the patient to reproduce the same healthy myoelectric patterns on the paretic limb during functional task training. Here, we aim at understanding how this myoelectric model, which translates muscle activity into continuous movements of a 7-degree of freedom upper limb exoskeleton, could transfer between sessions, arms and tasks. The experiments with 8 healthy individuals and 2 chronic stroke patients proved the feasibility and effectiveness of such myoelectric interface. We anticipate the proposed method to become an efficient strategy for the correction of maladaptive muscle activity and the rehabilitation of stroke patients.

Design of continuous EMG classification approaches towards the control of a robotic exoskeleton in reaching movements.

Myoelectric control of rehabilitation devices engages active recruitment of muscles for motor task accomplishment, which has been proven to be essential in motor rehabilitation. Unfortunately, most electromyographic (EMG) activity-based controls are limited to one single degree-of-freedom (DoF), not permitting multi-joint functional tasks. On the other hand, discrete EMG-triggered approaches fail to provide continuous feedback about muscle recruitment during movement. For such purposes, myoelectric interfaces for continuous recognition of functional movements are necessary. Here we recorded EMG activity using 5 bipolar electrodes placed on the upper-arm in 8 healthy participants while they performed reaching movements in 8 different directions. A pseudo on-line system was developed to continuously predict movement intention and attempted arm direction. We evaluated two hierarchical classification approaches. Movement intention detection triggered different movement direction classifiers (4 or 8 classes) that were trained and tested over a 5-fold cross validation. We also investigated the effect of 3 different window lengths to extract EMG features on classification. We obtained classification accuracies above 70% for both hierarchical approaches. These results highlight the viability of classifying online 8 upper-arm different directions using surface EMG activity of 5 muscles and represent a first step towards an online EMG-based control for rehabilitation devices.

A hybrid brain-machine interface based on EEG and EMG activity for the motor rehabilitation of stroke patients.

Including supplementary information from the brain or other body parts in the control of brain-machine interfaces (BMIs) has been recently proposed and investigated. Such enriched interfaces are referred to as hybrid BMIs (hBMIs) and have been proven to be more robust and accurate than regular BMIs for assistive and rehabilitative applications. Electromyographic (EMG) activity is one of the most widely utilized biosignals in hBMIs, as it provides a quite direct measurement of the motion intention of the user. Whereas most of the existing non-invasive EEG-EMG-hBMIs have only been subjected to offline testings or are limited to one degree of freedom (DoF), we present an EEG-EMG-hBMI that allows the simultaneous control of 7-DoFs of the upper limb with a robotic exoskeleton. Moreover, it establishes a biologically-inspired hierarchical control flow, requiring the active participation of central and peripheral structures of the nervous system. Contingent visual and proprioceptive feedback about the user's EEG and EMG activity is provided in the form of velocity modulation during functional task training. We believe that training with this closed-loop system may facilitate functional neuroplastic processes and eventually elicit a joint brain and muscle motor rehabilitation. Its usability is validated during a real-time operation session in a healthy participant and a chronic stroke patient, showing encouraging results for its application to a clinical rehabilitation scenario.

Classification of different reaching movements from the same limb using EEG.

OBJECTIVE: Brain-computer-interfaces (BCIs) have been proposed not only as assistive technologies but also as rehabilitation tools for lost functions. However, due to the stochastic nature, poor spatial resolution and signal to noise ratio from electroencephalography (EEG), multidimensional decoding has been the main obstacle to implement non-invasive BCIs in real-live rehabilitation scenarios. This study explores the classification of several functional reaching movements from the same limb using EEG oscillations in order to create a more versatile BCI for rehabilitation. APPROACH: Nine healthy participants performed four 3D center-out reaching tasks in four different sessions while wearing a passive robotic exoskeleton at their right upper limb. Kinematics data were acquired from the robotic exoskeleton. Multiclass extensions of Filter Bank Common Spatial Patterns (FBCSP) and a linear discriminant analysis (LDA) classifier were used to classify the EEG activity into four forward reaching movements (from a starting position towards four target positions), a backward movement (from any of the targets to the starting position and rest). Recalibrating the classifier using data from previous or the same session was also investigated and compared. MAIN RESULTS: Average EEG decoding accuracy were significantly above chance with 67%, 62.75%, and 50.3% when decoding three, four and six tasks from the same limb, respectively. Furthermore, classification accuracy could be increased when using data from the beginning of each session as training data to recalibrate the classifier. SIGNIFICANCE: Our results demonstrate that classification from several functional movements performed by the same limb is possible with acceptable accuracy using EEG oscillations, especially if data from the same session are used to recalibrate the classifier. Therefore, an ecologically valid decoding could be used to control assistive or rehabilitation mutli-degrees of freedom (DoF) robotic devices using EEG data. These results have important implications towards assistive and rehabilitative neuroprostheses control in paralyzed patients.

Comparing metrics to evaluate performance of regression methods for decoding of neural signals.

The use of regression methods for decoding of neural signals has become popular, with its main applications in the field of Brain-Machine Interfaces (BMIs) for control of prosthetic devices or in the area of Brain-Computer Interfaces (BCIs) for cursor control. When new methods for decoding are being developed or the parameters for existing methods should be optimized to increase performance, a metric is needed that gives an accurate estimate of the prediction error. In this paper, we evaluate different performance metrics regarding their robustness for assessing prediction errors. Using simulated data, we show that different kinds of prediction error (noise, scaling error, bias) have different effects on the different metrics and evaluate which methods are best to assess the overall prediction error, as well as the individual types of error. Based on the obtained results we can conclude that the most commonly used metrics correlation coefficient (CC) and normalized root-mean-squared error (NRMSE) are well suited for evaluation of cross-validated results, but should not be used as sole criterion for cross-subject or cross-session evaluations.

Towards decoding of functional movements from the same limb using EEG.

In recent years, there has been an increasing interest in using electroencephalographic (EEG) activity to close the loop between brain oscillations and movement to induce functional motor rehabilitation. Rehabilitation robots or exoskeletons have been controlled using EEG activity. However, all studies have used a 2-class or one-dimensional decoding scheme. In this study we investigated EEG decoding of 5 functional movements of the same limb towards an online scenario. Six healthy participants performed a three-dimensional center-out reaching task based on direction movements (four directions and rest) wearing a 32-channel EEG cap. A BCI design based on multiclass extensions of Spectrally Weighted Common Spatial Patterns (Spec-CSP) and a linear discriminant analysis (LDA) classifier was developed and tested offline. The decoding accuracy was 5-fold cross-validated. A decoding accuracy of 39.5% on average for all the six subjects was obtained (chance level being 20%). The results of the current study demonstrate multiple functional movements decoding (significantly higher than chance level) from the same limb using EEG data. This study represents first steps towards a same limb multi degree of freedom (DOF) online EEG based BCI for motor restoration.