Hybrid brain-computer interface and functional electrical stimulation for sensorimotor training in participants with tetraplegia: a proof-of-concept study

Background and Purpose: Impaired hand function decreases quality of life in persons with tetraplegia. We tested functional electrical stimulation (FES) controlled by a hybrid brain-computer interface (BCI) for improving hand function in participants with tetraplegia. Methods: Two participants with subacute tetraplegia (participant 1: C5 Brown-Sequard syndrome, participant 2: complete C5 lesion) took part in this proof-of-concept study. The goal was to determine whether the BCI system could drive the FES device by accurately classifying participants' intent (open or close the hand). Participants 1 and 2 received 10 sessions and 4 sessions of BCI-FES, respectively. A novel time-switch BCI strategy based on motor imagery was used to activate the FES. In one session, we tested a hybrid BCI-FES based on 2 spontaneously generated brain rhythms: a sensory-motor rhythm during motor imagery to activate a stimulator and occipital alpha rhythms to deactivate the stimulator. Participants received BCI-FES therapy 2 to 3 times a week in addition to conventional therapy. Imagery ability and muscle strength were measured before and after treatment. Results: Visual feedback was associated with a 4-fold increase of brain response during motor imagery in both participants. For participant 1, classification accuracy (open/closed) for motor imagery-based BCI was 83.5% (left hand) and 83.8% (right hand); participant 2 had a classification accuracy of 83.8% for the right hand. Participant 1 had moderate improvement in muscle strength, while there was no change for participant 2. Discussion and Conclusion: We demonstrated feasibility of BCI-FES, using 2 naturally generated brain rhythms. Studies on a larger number of participants are needed to separate the effects of BCI training from effects of conventional therapy

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

Exploiting Multiple Sensory Modalities in Brain-Machine Interfaces

Recent improvements in cortically-controlled brain-machine interfaces (BMIs) have raised hopes that such technologies may improve the quality of life of severely motor-disabled patients. However, current generation BMIs do not perform up to their potential due to the neglect of the full range of sensory feedback in their strategies for training and control. Here we confirm that neurons in the primary motor cortex (MI) encode sensory information and demonstrate a significant heterogeneity in their responses with respect to the type of sensory modality available to the subject about a reaching task. We further show using mutual information and directional tuning analyses that the presence of multi-sensory feedback (i.e. vision and proprioception) during replay of movements evokes neural responses in MI that are almost indistinguishable from those responses measured during overt movement. Finally, we suggest how these playback-evoked responses may be used to improve BMI performance

Time to reconcile research findings and clinical practice on upper limb neurorehabilitation

The problemIn the field of upper limb neurorehabilitation, the translation from research findings to clinical practice remains troublesome. Patients are not receiving treatments based on the best available evidence. There are certainly multiple reasons to account for this issue, including the power of habit over innovation, subjective beliefs over objective results. We need to take a step forward, by looking at most important results from randomized controlled trials, and then identify key active ingredients that determined the success of interventions. On the other hand, we need to recognize those specific categories of patients having the greatest benefit from each intervention, and why. The aim is to reach the ability to design a neurorehabilitation program based on motor learning principles with established clinical efficacy and tailored for specific patient's needs. Proposed solutionsThe objective of the present manuscript is to facilitate the translation of research findings to clinical practice. Starting from a literature review of selected neurorehabilitation approaches, for each intervention the following elements were highlighted: definition of active ingredients; identification of underlying motor learning principles and neural mechanisms of recovery; inferences from research findings; and recommendations for clinical practice. Furthermore, we included a dedicated chapter on the importance of a comprehensive assessment (objective impairments and patient's perspective) to design personalized and effective neurorehabilitation interventions. ConclusionsIt's time to reconcile research findings with clinical practice. Evidence from literature is consistently showing that neurological patients improve upper limb function, when core strategies based on motor learning principles are applied. To this end, practical take-home messages in the concluding section are provided, focusing on the importance of graded task practice, high number of repetitions, interventions tailored to patient's goals and expectations, solutions to increase and distribute therapy beyond the formal patient-therapist session, and how to integrate different interventions to maximize upper limb motor outcomes. We hope that this manuscript will serve as starting point to fill the gap between theory and practice in upper limb neurorehabilitation, and as a practical tool to leverage the positive impact of clinicians on patients' recovery

Time to reconcile research findings and clinical practice on upper limb neurorehabilitation

In the field of upper limb neurorehabilitation, the translation from research findings to clinical practice remains troublesome. Patients are not receiving treatments based on the best available evidence. There are certainly multiple reasons to account for this issue, including the power of habit over innovation, subjective beliefs over objective results. We need to take a step forward, by looking at most important results from randomized controlled trials, and then identify key active ingredients that determined the success of interventions. On the other hand, we need to recognize those specific categories of patients having the greatest benefit from each intervention, and why. The aim is to reach the ability to design a neurorehabilitation program based on motor learning principles with established clinical efficacy and tailored for specific patient's needs. The objective of the present manuscript is to facilitate the translation of research findings to clinical practice. Starting from a literature review of selected neurorehabilitation approaches, for each intervention the following elements were highlighted: definition of active ingredients; identification of underlying motor learning principles and neural mechanisms of recovery; inferences from research findings; and recommendations for clinical practice. Furthermore, we included a dedicated chapter on the importance of a comprehensive assessment (objective impairments and patient's perspective) to design personalized and effective neurorehabilitation interventions. It's time to reconcile research findings with clinical practice. Evidence from literature is consistently showing that neurological patients improve upper limb function, when core strategies based on motor learning principles are applied. To this end, practical take-home messages in the concluding section are provided, focusing on the importance of graded task practice, high number of repetitions, interventions tailored to patient's goals and expectations, solutions to increase and distribute therapy beyond the formal patient-therapist session, and how to integrate different interventions to maximize upper limb motor outcomes. We hope that this manuscript will serve as starting point to fill the gap between theory and practice in upper limb neurorehabilitation, and as a practical tool to leverage the positive impact of clinicians on patients' recovery

Classification of Tactile and Motor Velocity-Evoked Hemodynamic Response in Primary Somatosensory and Motor Cortices as Measured by Functional Near-Infrared Spectroscopy

Functional near-infrared spectroscopy (fNIRS) is an emerging technique in studying cerebral hemodynamics; however, consensus on the analysis methods and the clinical applications has yet to be established. In this study, we demonstrate the results of a pilot fNIRS study of cerebral hemodynamic response (HR) evoked by pneumotactile and sensorimotor stimuli on the dominant hand. Our goal is to find the optimal stimulus parameters to maximally evoke HR in the primary somatosensory and motor cortices. We use a pulsatile pneumatic array of 14 tactile cells that were attached to the glabrous surface of the dominant hand, with a patterned stimulus that resembles saltation at three distinct traverse velocities [10, 25, and 45 cm/s]. NIRS optodes (16 sources; 20 detectors) are bilaterally and symmetrically placed over the pre-and post-central gyri (M1 and S1). Our objective is to identify the extent to which cerebral HR can encode the velocity of the somatosensory and/or motor stimuli. We use common spatial pattern for feature extraction and regularized-discriminant analysis for classifying the fNIRS time series into velocity classes. The classification results demonstrate discriminatory features of the fNIRS signal from each distinct stimulus velocity. The results are inconclusive regarding the velocity which evokes the highest intensity of hemodynamic response

CLOSED-LOOP AFFERENT NERVE ELECTRICAL STIMULATION FOR REHABILITATION OF HAND FUNCTION IN SUBJECTS WITH INCOMPLETE SPINAL CORD INJURY

Peripheral nerve stimulation (PNS) is commonly used to promote use-dependent cortical plasticity for rehabilitation of motor function in spinal cord injury. Pairing transcranial magnetic stimulation (TMS) with PNS has been shown to increase motor evoked potentials most when the two stimuli are timed to arrive in the cortex simultaneously. This suggests that a mechanism of timing-dependent plasticity (TDP) may be a more effective method of promoting motor rehabilitation. The following thesis is the result of applying a brain-computer interface to apply PNS in closed-loop simultaneously to movement intention onset as measured by EEG of the sensorimotor cortex to test whether TDP can be induced in incomplete spinal cord injured individuals with upper limb motor impairment. 4 motor incomplete SCI subjects have completed 12 sessions of closed-loop PNS delivered over 4-6 weeks. Benefit was observed for every subject although not consistently across metrics. 3 out of 4 subjects exhibited increased maximum voluntary contraction force (MVCF) between first and last interventions for one or both hands. TMS-measured motor map volume increased for both hemispheres in one subject, and TMS center of gravity shifted in 3 subjects consistent with studies in which motor function improved or was restored. These observations suggest that rehabilitation using similar designs for responsive stimulation could improve motor impairment in SCI

Enhancing Nervous System Recovery through Neurobiologics, Neural Interface Training, and Neurorehabilitation.

After an initial period of recovery, human neurological injury has long been thought to be static. In order to improve quality of life for those suffering from stroke, spinal cord injury, or traumatic brain injury, researchers have been working to restore the nervous system and reduce neurological deficits through a number of mechanisms. For example, neurobiologists have been identifying and manipulating components of the intra- and extracellular milieu to alter the regenerative potential of neurons, neuro-engineers have been producing brain-machine and neural interfaces that circumvent lesions to restore functionality, and neurorehabilitation experts have been developing new ways to revitalize the nervous system even in chronic disease. While each of these areas holds promise, their individual paths to clinical relevance remain difficult. Nonetheless, these methods are now able to synergistically enhance recovery of native motor function to levels which were previously believed to be impossible. Furthermore, such recovery can even persist after training, and for the first time there is evidence of functional axonal regrowth and rewiring in the central nervous system of animal models. To attain this type of regeneration, rehabilitation paradigms that pair cortically-based intent with activation of affected circuits and positive neurofeedback appear to be required-a phenomenon which raises new and far reaching questions about the underlying relationship between conscious action and neural repair. For this reason, we argue that multi-modal therapy will be necessary to facilitate a truly robust recovery, and that the success of investigational microscopic techniques may depend on their integration into macroscopic frameworks that include task-based neurorehabilitation. We further identify critical components of future neural repair strategies and explore the most updated knowledge, progress, and challenges in the fields of cellular neuronal repair, neural interfacing, and neurorehabilitation, all with the goal of better understanding neurological injury and how to improve recovery

Sensory threshold neuromuscular electrical stimulation fosters motor imagery performance

Motor imagery (MI) has been largely studied as a way to enhance motor learning and to restore motor functions. Although it is agreed that users should emphasize kinesthetic imagery during MI, recordings of MI brain patterns are not sufficiently reliable for many subjects. It has been suggested that the usage of somatosensory feedback would be more suitable than standardly used visual feedback to enhance MI brain patterns. However, somatosensory feedback should not interfere with the recorded MI brain pattern. In this study we propose a novel feedback modality to guide subjects during MI based on sensory threshold neuromuscular electrical stimulation (St-NMES). St-NMES depolarizes sensory and motor axons without eliciting any muscular contraction. We hypothesize that St-NMES does not induce detectable ERD brain patterns and fosters MI performance. Twelve novice subjects were included in a cross-over design study. We recorded their EEG, comparing St-NMES with visual feedback during MI or resting tasks. We found that St-NMES not only induced significantly larger desynchronization over sensorimotor areas (p<0.05) but also significantly enhanced MI brain connectivity patterns. Moreover, classification accuracy and stability were significantly higher with St-NMES. Importantly, St-NMES alone did not induce detectable artifacts, but rather the changes in the detected patterns were due to an increased MI performance. Our findings indicate that St-NMES is a promising feedback in order to foster MI performance and cold be used for BMI online applications