Effect of lower limb exoskeleton on the modulation of neural activity and gait classification

: Neurorehabilitation with robotic devices requires a paradigm shift to enhance human-robot interaction. The coupling of robot assisted gait training (RAGT) with a brain-machine interface (BMI) represents an important step in this direction but requires better elucidation of the effect of RAGT on the user's neural modulation. Here, we investigated how different exoskeleton walking modes modify brain and muscular activity during exoskeleton assisted gait. We recorded electroencephalographic (EEG) and electromyographic (EMG) activity from ten able-bodied volunteers walking with an exoskeleton with three modes of user assistance (i.e., transparent, adaptive and full assistance) and during free overground gait. Results identified that exoskeleton walking (irrespective of the exoskeleton mode) induces a stronger modulation of central mid-line mu (8-13 Hz) and low-beta (14-20 Hz) rhythms compared to free overground walking. These modifications are accompanied by a significant re-organization of the EMG patterns in exoskeleton walking. On the other hand, we observed no significant differences in neural activity during exoskeleton walking with the different assistance levels. We subsequently implemented four gait classifiers based on deep neural networks trained on the EEG data during the different walking conditions. Our hypothesis was that exoskeleton modes could impact the creation of a BMI-driven RAGT. We demonstrated that all classifiers achieved an average accuracy of 84.13 ± 3.49% in classifying swing and stance phases on their respective datasets. In addition, we demonstrated that the classifier trained on the transparent mode exoskeleton data can classify gait phases during adaptive and full modes with an accuracy of 78.3 ± 4.8%, while the classifier trained on free overground walking data fails to classify the gait during exoskeleton walking (accuracy of 59.4 ± 11.8%). These findings provide important insights into the effect of robotic training on neural activity and contribute to the advancement of BMI technology for improving robotic gait rehabilitation therapy

How brain-computer interface technology may improve the diagnosis of the disorders of consciousness: A comparative study

ObjectiveClinical assessment of consciousness relies on behavioural assessments, which have several limitations. Hence, disorder of consciousness (DOC) patients are often misdiagnosed. In this work, we aimed to compare the repetitive assessment of consciousness performed with a clinical behavioural and a Brain-Computer Interface (BCI) approach. Materials and methodsFor 7 weeks, sixteen DOC patients participated in weekly evaluations using both the Coma Recovery Scale-Revised (CRS-R) and a vibrotactile P300 BCI paradigm. To use the BCI, patients had to perform an active mental task that required detecting specific stimuli while ignoring other stimuli. We analysed the reliability and the efficacy in the detection of command following resulting from the two methodologies. ResultsOver repetitive administrations, the BCI paradigm detected command following before the CRS-R in seven patients. Four clinically unresponsive patients consistently showed command following during the BCI assessments. ConclusionBrain-Computer Interface active paradigms might contribute to the evaluation of the level of consciousness, increasing the diagnostic precision of the clinical bedside approach. SignificanceThe integration of different diagnostic methods leads to a better knowledge and care for the DOC

EEG Biomarkers Related With the Functional State of Stroke Patients

Recent studies explored promising new quantitative methods to analyze electroencephalography (EEG) signals. This paper analyzes the correlation of two EEG parameters, Brain Symmetry Index (BSI) and Laterality Coefficient (LC), with established functional scales for the stroke assessment. Thirty-two healthy subjects and thirty-six stroke patients with upper extremity hemiparesis were recruited for this study. The stroke patients where subdivided in three groups according to the stroke location: Cortical, Subcortical, and Cortical + Subcortical. The participants performed assessment visits to record the EEG in the resting state and perform functional tests using rehabilitation scales. Then, stroke patients performed 25 sessions using a motor-imagery based Brain Computer Interface system (BCI). BSI was calculated with the EEG data in resting state and LC was calculated with the Event-Related Synchronization maps. The results of this study demonstrated significant differences in the BSI between the healthy group and Subcortical group (P = 0.001), and also between the healthy and Cortical+Subcortical group (P = 0.019). No significant differences were found between the healthy group and the Cortical group (P = 0.505). Furthermore, the BSI analysis in the healthy group based on gender showed statistical differences (P = 0.027). In the stroke group, the correlation between the BSI and the functional state of the upper extremity assessed by Fugl-Meyer Assessment (FMA) was also significant, ρ = −0.430 and P = 0.046. The correlation between the BSI and the FMA-Lower extremity was not significant (ρ = −0.063, P = 0.852). Similarly, the LC calculated in the alpha band has significative correlation with FMA of upper extremity (ρ = −0.623 and P < 0.001) and FMA of lower extremity (ρ = −0.509 and P = 0.026). Other important significant correlations between LC and functional scales were observed. In addition, the patients showed an improvement in the FMA-upper extremity after the BCI therapy (ΔFMA = 1 median [IQR: 0-8], P = 0.002). The quantitative EEG tools used here may help support our understanding of stroke and how the brain changes during rehabilitation therapy. These tools can help identify changes in EEG biomarkers and parameters during therapy that might lead to improved therapy methods and functional prognoses

Real-time estimation of EEG-based engagement in different tasks

: Objective.Recent trends in brain-computer interface (BCI) research concern the passive monitoring of brain activity, which aim to monitor a wide variety of cognitive states. Engagement is such a cognitive state, which is of interest in contexts such as learning, entertainment or rehabilitation. This study proposes a novel approach for real-time estimation of engagement during different tasks using electroencephalography (EEG).Approach.Twenty-three healthy subjects participated in the BCI experiment. A modified version of the d2 test was used to elicit engagement. Within-subject classification models which discriminate between engaging and resting states were trained based on EEG recorded during a d2 test based paradigm. The EEG was recorded using eight electrodes and the classification model was based on filter-bank common spatial patterns and a linear discriminant analysis. The classification models were evaluated in cross-task applications, namely when playing Tetris at different speeds (i.e. slow, medium, fast) and when watching two videos (i.e. advertisement and landscape video). Additionally, subjects' perceived engagement was quantified using a questionnaire.Main results.The models achieved a classification accuracy of 90% on average when tested on an independent d2 test paradigm recording. Subjects' perceived and estimated engagement were found to be greater during the advertisement compared to the landscape video (p= 0.025 andp<0.001, respectively); greater during medium and fast compared to slow Tetris speed (p<0.001, respectively); not different between medium and fast Tetris speeds. Additionally, a common linear relationship was observed for perceived and estimated engagement (rrm= 0.44,p<0.001). Finally, theta and alpha band powers were investigated, which respectively increased and decreased during more engaging states.Significance.This study proposes a task-specific EEG engagement estimation model with cross-task capabilities, offering a framework for real-world applications

High Classification Accuracy of a Motor Imagery Based Brain-Computer Interface for Stroke Rehabilitation Training

Motor imagery (MI) based brain-computer interfaces (BCI) extract commands in real-time and can be used to control a cursor, a robot or functional electrical stimulation (FES) devices. The control of FES devices is especially interesting for stroke rehabilitation, when a patient can use motor imagery to stimulate specific muscles in real-time. However, damage to motor areas resulting from stroke or other causes might impair control of a motor imagery BCI for rehabilitation. The current work presents a comparative evaluation of the MI-based BCI control accuracy between stroke patients and healthy subjects. Five patients who had a stroke that affected the motor system participated in the current study, and were trained across 10–24 sessions lasting about 1 h each with the recoveriX system. The participants' EEG data were classified while they imagined left or right hand movements, and real-time feedback was provided on a monitor. If the correct imagination was detected, the FES was also activated to move the left or right hand. The grand average mean accuracy was 87.4% for all patients and sessions. All patients were able to achieve at least one session with a maximum accuracy above 96%. Both the mean accuracy and the maximum accuracy were surprisingly high and above results seen with healthy controls in prior studies. Importantly, the study showed that stroke patients can control a MI BCI system with high accuracy relative to healthy persons. This may occur because these patients are highly motivated to participate in a study to improve their motor functions. Participants often reported early in the training of motor improvements and this caused additional motivation. However, it also reflects the efficacy of combining motor imagination, seeing continuous bar feedback, and real hand movement that also activates the tactile and proprioceptive systems. Results also suggested that motor function could improve even if classification accuracy did not, and suggest other new questions to explore in future work. Future studies will also be done with a first-person view 3D avatar to provide improved feedback and thereby increase each patients' sense of engagement

Corrigendum: Performance Differences Using a Vibro-Tactile P300 BCI in LIS-Patients Diagnosed With Stroke and ALS.

[This corrects the article DOI: 10.3389/fnins.2018.00514.].H2020-MSCA-IF-2016-ADOC-75268

Fiberless, Multi-Channel fNIRS-EEG System Based on Silicon Photomultipliers: Towards Sensitive and Ecological Mapping of Brain Activity and Neurovascular Coupling

Portable neuroimaging technologies can be employed for long-term monitoring of neurophysiological and neuropathological states. Functional Near-Infrared Spectroscopy (fNIRS) and Electroencephalography (EEG) are highly suited for such a purpose. Their multimodal integration allows the evaluation of hemodynamic and electrical brain activity together with neurovascular coupling. An innovative fNIRS-EEG system is here presented. The system integrated a novel continuous-wave fNIRS component and a modified commercial EEG device. fNIRS probing relied on fiberless technology based on light emitting diodes and silicon photomultipliers (SiPMs). SiPMs are sensitive semiconductor detectors, whose large detection area maximizes photon harvesting from the scalp and overcomes limitations of fiberless technology. To optimize the signal-to-noise ratio and avoid fNIRS-EEG interference, a digital lock-in was implemented for fNIRS signal acquisition. A benchtop characterization of the fNIRS component showed its high performances with a noise equivalent power below 1 pW. Moreover, the fNIRS-EEG device was tested in vivo during tasks stimulating visual, motor and pre-frontal cortices. Finally, the capabilities to perform ecological recordings were assessed in clinical settings on one Alzheimer’s Disease patient during long-lasting cognitive tests. The system can pave the way to portable technologies for accurate evaluation of multimodal brain activity, allowing their extensive employment in ecological environments and clinical practice

Effects of a Vibro-Tactile P300 Based Brain-Computer Interface on the Coma Recovery Scale-Revised in Patients With Disorders of Consciousness

peer reviewedPersons diagnosed with disorders of consciousness (DOC) typically suffer from motor and cognitive disabilities. Recent research has shown that non-invasive brain-computer interface (BCI) technology could help assess these patients’ cognitive functions and command following abilities. 20 DOC patients participated in the study and performed 10 vibro-tactile P300 BCI sessions over 10 days with 8–12 runs each day. Vibrotactile tactors were placed on the each patient’s left and right wrists and one foot. Patients were instructed, via earbuds, to concentrate and silently count vibrotactile pulses on either their left or right wrist that presented a target stimulus and to ignore the others. Changes of the BCI classification accuracy were investigated over the 10 days. In addition, the Coma Recovery Scale-Revised (CRS-R) score was measured before and after the 10 vibro-tactile P300 sessions. In the first run, 10 patients had a classification accuracy above chance level (>12.5%). In the best run, every patient reached an accuracy ≥60%. The grand average accuracy in the first session for all patients was 40%. In the best session, the grand average accuracy was 88% and the median accuracy across all sessions was 21%. The CRS-R scores compared before and after 10 VT3 sessions for all 20 patients, are showing significant improvement (p = 0.024). Twelve of the twenty patients showed an improvement of 1 to 7 points in the CRS-R score after the VT3 BCI sessions (mean: 2.6). Six patients did not show a change of the CRS-R and two patients showed a decline in the score by 1 point. Every patient achieved at least 60% accuracy at least once, which indicates successful command following. This shows the importance of repeated measures when DOC patients are assessed. The improvement of the CRS-R score after the 10 VT3 sessions is an important issue for future experiments to test the possible therapeutic applications of vibro-tactile and related BCIs with a larger patient group. © Copyright © 2020 Murovec, Heilinger, Xu, Ortner, Spataro, La Bella, Miao, Jin, Chatelle, Laureys, Allison and Guger.247919 - DECODER; H2020-MSCA-IF-2016-ADOC-75268

Performance Differences Using a Vibro-Tactile P300 BCI in LIS-Patients Diagnosed With Stroke and ALS

Patients with locked-in syndrome (LIS) are typically unable to move or communicate and can be misdiagnosed as patients with disorders of consciousness (DOC). Behavioral assessment scales are limited in their ability to detect signs of consciousness in this population. Recent research has shown that brain-computer interface (BCI) technology could supplement behavioral scales and allows to establish communication with these severely disabled patients. In this study, we compared the vibro-tactile P300 based BCI performance in two groups of patients with LIS of different etiologies: stroke (n = 6) and amyotrophic lateral sclerosis (ALS) (n = 9). Two vibro-tactile paradigms were administered to the patients to assess conscious function and command following. The first paradigm is called vibrotactile evoked potentials (EPs) with two tactors (VT2), where two stimulators were placed on the patient’s left and right wrist, respectively. The patients were asked to count the rare stimuli presented to one wrist to elicit a P300 complex to target stimuli only. In the second paradigm, namely vibrotactile EPs with three tactors (VT3), two stimulators were placed on the wrists as done in VT2, and one additional stimulator was placed on his/her back. The task was to count the rare stimuli presented to one wrist, to elicit the event-related potentials (ERPs). The VT3 paradigm could also be used for communication. For this purpose, the patient had to count the stimuli presented to the left hand to answer “yes” and to count the stimuli presented to the right hand to answer “no.” All patients except one performed above chance level in at least one run in the VT2 paradigm. In the VT3 paradigm, all 6 stroke patients and 8/9 ALS patients showed at least one run above chance. Overall, patients achieved higher accuracies in VT2 than VT3. LIS patients due to ALS exhibited higher accuracies that LIS patients due to stroke, in both the VT2 and VT3 paradigms. These initial data suggest that controlling this type of BCI requires specific cognitive abilities that may be impaired in certain sub-groups of severely motor-impaired patients. Future studies on a larger cohort of patients are needed to better identify and understand the underlying cortical mechanisms of these differences

Assessing Command-Following and Communication With Vibro-Tactile P300 Brain-Computer Interface Tools in Patients With Unresponsive Wakefulness Syndrome

Persons diagnosed with disorders of consciousness (DOC) typically suffer from motor disablities, and thus assessing their spared cognitive abilities can be difficult. Recent research from several groups has shown that non-invasive brain-computer interface (BCI) technology can provide assessments of these patients' cognitive function that can supplement information provided through conventional behavioral assessment methods. In rare cases, BCIs may provide a binary communication mechanism. Here, we present results from a vibrotactile BCI assessment aiming at detecting command-following and communication in 12 unresponsive wakefulness syndrome (UWS) patients. Two different paradigms were administered at least once for every patient: (i) VT2 with two vibro-tactile stimulators fixed on the patient's left and right wrists and (ii) VT3 with three vibro-tactile stimulators fixed on both wrists and on the back. The patients were instructed to mentally count either the stimuli on the left or right wrist, which may elicit a robust P300 for the target wrist only. The EEG data from −100 to +600 ms around each stimulus were extracted and sub-divided into 8 data segments. This data was classified with linear discriminant analysis (using a 10 × 10 cross validation) and used to calibrate a BCI to assess command following and YES/NO communication abilities. The grand average VT2 accuracy across all patients was 38.3%, and the VT3 accuracy was 26.3%. Two patients achieved VT3 accuracy ≥80% and went through communication testing. One of these patients answered 4 out of 5 questions correctly in session 1, whereas the other patient answered 6/10 and 7/10 questions correctly in sessions 2 and 4. In 6 other patients, the VT2 or VT3 accuracy was above the significance threshold of 23% for at least one run, while in 4 patients, the accuracy was always below this threshold. The study highlights the importance of repeating EEG assessments to increase the chance of detecting command-following in patients with severe brain injury. Furthermore, the study shows that BCI technology can test command following in chronic UWS patients and can allow some of these patients to answer YES/NO questions