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Showing papers in "Journal of Neural Engineering in 2016"


Journal ArticleDOI
TL;DR: These results show that the method provides a solid framework for the decomposition of multi-channel invasive and non-invasive EMG signals that allows the study of the behavior of a large number of concurrently active motor units.
Abstract: Objective. The study of motor unit behavior has been classically performed by selective recording systems of muscle electrical activity (EMG signals) and decomposition algorithms able to discriminate between individual motor unit action potentials from multi-unit signals. In this study, we provide a general framework for the decomposition of multi-channel intramuscular and surface EMG signals and we extensively validate this approach with experimental recordings. Approach. First, we describe the conditions under which the assumptions of the convolutive blind separation model are satisfied. Second, we propose an approach of convolutive sphering of the observations followed by an iterative extraction of the sources. This approach is then validated using intramuscular signals recorded by novel multi-channel thin-film electrodes on the Abductor Digiti Minimi of the hand and Tibilias Anterior muscles, as well as on high-density surface EMG signals recorded by electrode grids on the First Dorsal Interosseous muscle. The validation was based on the comparison with the gold standard of manual decomposition (for intramuscular recordings) and on the two-source method (for comparison of intramuscular and surface EMG recordings) for the three human muscles and contraction forces of up to 90% MVC. Main results. The average number of common sources identified for the validation was 14 ± 7 (averaged across all trials and subjects and all comparisons), with a rate of agreement in their discharge timings of 92.8 ± 3.2%. The average Decomposability Index, calculated on the automatic decomposed signals, was 16.0 ± 2.2 (7.3–44.1). For comparison, the same index calculated on the manual decomposed signals was 15.0 ± 3.0 (6.3–76.6). Significance. These results show that the method provides a solid framework for the decomposition of multi-channel invasive and non-invasive EMG signals that allows the study of the behavior of a large number of concurrently active motor units.

378 citations


Journal ArticleDOI
TL;DR: A brief history of neuromorphic engineering is presented, some of the principal current large-scale projects, their main features, how their approaches are complementary and distinct, their advantages and drawbacks, and highlight the sorts of capabilities that each can deliver to neural modellers are highlighted.
Abstract: Neuromorphic computing covers a diverse range of approaches to information processing all of which demonstrate some degree of neurobiological inspiration that differentiates them from mainstream conventional computing systems. The philosophy behind neuromorphic computing has its origins in the seminal work carried out by Carver Mead at Caltech in the late 1980s. This early work influenced others to carry developments forward, and advances in VLSI technology supported steady growth in the scale and capability of neuromorphic devices. Recently, a number of large-scale neuromorphic projects have emerged, taking the approach to unprecedented scales and capabilities. These large-scale projects are associated with major new funding initiatives for brain-related research, creating a sense that the time and circumstances are right for progress in our understanding of information processing in the brain. In this review we present a brief history of neuromorphic engineering then focus on some of the principal current large-scale projects, their main features, how their approaches are complementary and distinct, their advantages and drawbacks, and highlight the sorts of capabilities that each can deliver to neural modellers.

275 citations


Journal ArticleDOI
TL;DR: This study demonstrated that an array of 96 microelectrodes can be implanted into the human peripheral nervous system for up to 1 month durations and could provide intuitive control of a virtual prosthetic hand with broad sensory feedback.
Abstract: OBJECTIVE An important goal of neuroprosthetic research is to establish bidirectional communication between the user and new prosthetic limbs that are capable of controlling >20 different movements. One strategy for achieving this goal is to interface the prosthetic limb directly with efferent and afferent fibres in the peripheral nervous system using an array of intrafascicular microelectrodes. This approach would provide access to a large number of independent neural pathways for controlling high degree-of-freedom prosthetic limbs, as well as evoking multiple-complex sensory percepts. APPROACH Utah Slanted Electrode Arrays (USEAs, 96 recording/stimulating electrodes) were implanted for 30 days into the median (Subject 1-M, 31 years post-amputation) or ulnar (Subject 2-U, 1.5 years post-amputation) nerves of two amputees. Neural activity was recorded during intended movements of the subject's phantom fingers and a linear Kalman filter was used to decode the neural data. Microelectrode stimulation of varying amplitudes and frequencies was delivered via single or multiple electrodes to investigate the number, size and quality of sensory percepts that could be evoked. Device performance over time was assessed by measuring: electrode impedances, signal-to-noise ratios (SNRs), stimulation thresholds, number and stability of evoked percepts. MAIN RESULTS The subjects were able to proportionally, control individual fingers of a virtual robotic hand, with 13 different movements decoded offline (r = 0.48) and two movements decoded online. Electrical stimulation across one USEA evoked >80 sensory percepts. Varying the stimulation parameters modulated percept quality. Devices remained intrafascicularly implanted for the duration of the study with no significant changes in the SNRs or percept thresholds. SIGNIFICANCE This study demonstrated that an array of 96 microelectrodes can be implanted into the human peripheral nervous system for up to 1 month durations. Such an array could provide intuitive control of a virtual prosthetic hand with broad sensory feedback.

272 citations


Journal ArticleDOI
TL;DR: Experimental data show that stimulation at higher charge densities can be achieved without causing tissue damage, suggesting that safety parameters for microelectrodes might be distinct from those defined for macro electrodes, however, these increased charges may need to be justified by bench, non-clinical or clinical testing to provide evidence of device safety.
Abstract: OBJECTIVE Recent initiatives in bioelectronic modulation of the nervous system by the NIH (SPARC), DARPA (ElectRx, SUBNETS) and the GlaxoSmithKline Bioelectronic Medicines effort are ushering in a new era of therapeutic electrical stimulation. These novel therapies are prompting a re-evaluation of established electrical thresholds for stimulation-induced tissue damage. APPROACH In this review, we explore what is known and unknown in published literature regarding tissue damage from electrical stimulation. MAIN RESULTS For macroelectrodes, the potential for tissue damage is often assessed by comparing the intensity of stimulation, characterized by the charge density and charge per phase of a stimulus pulse, with a damage threshold identified through histological evidence from in vivo experiments as described by the Shannon equation. While the Shannon equation has proved useful in assessing the likely occurrence of tissue damage, the analysis is limited by the experimental parameters of the original studies. Tissue damage is influenced by factors not explicitly incorporated into the Shannon equation, including pulse frequency, duty cycle, current density, and electrode size. Microelectrodes in particular do not follow the charge per phase and charge density co-dependence reflected in the Shannon equation. The relevance of these factors to tissue damage is framed in the context of available reports from modeling and in vivo studies. SIGNIFICANCE It is apparent that emerging applications, especially with microelectrodes, will require clinical charge densities that exceed traditional damage thresholds. Experimental data show that stimulation at higher charge densities can be achieved without causing tissue damage, suggesting that safety parameters for microelectrodes might be distinct from those defined for macroelectrodes. However, these increased charge densities may need to be justified by bench, non-clinical or clinical testing to provide evidence of device safety.

245 citations


Journal ArticleDOI
TL;DR: Sensory feedback by peripheral nerve stimulation improved object discrimination and manipulation, embodiment, and confidence in individuals with limb loss with blindfolded performance similar to sighted performance in the wooden block and magnetic block tasks.
Abstract: Objective. Tactile feedback is critical to grip and object manipulation. Its absence results in reliance on visual and auditory cues. Our objective was to assess the effect of sensory feedback on task performance in individuals with limb loss. Approach. Stimulation of the peripheral nerves using implanted cuff electrodes provided two subjects with sensory feedback with intensity proportional to forces on the thumb, index, and middle fingers of their prosthetic hand during object manipulation. Both subjects perceived the sensation on their phantom hand at locations corresponding to the locations of the forces on the prosthetic hand. A bend sensor measured prosthetic hand span. Hand span modulated the intensity of sensory feedback perceived on the thenar eminence for subject 1 and the middle finger for subject 2. We performed three functional tests with the blindfolded subjects. First, the subject tried to determine whether or not a wooden block had been placed in his prosthetic hand. Second, the subject had to locate and remove magnetic blocks from a metal table. Third, the subject performed the Southampton Hand Assessment Procedure (SHAP). We also measured the subject's sense of embodiment with a survey and his self-confidence. Main results. Blindfolded performance with sensory feedback was similar to sighted performance in the wooden block and magnetic block tasks. Performance on the SHAP, a measure of hand mechanical function and control, was similar with and without sensory feedback. An embodiment survey showed an improved sense of integration of the prosthesis in self body image with sensory feedback. Significance. Sensory feedback by peripheral nerve stimulation improved object discrimination and manipulation, embodiment, and confidence. With both forms of feedback, the blindfolded subjects tended toward results obtained with visual feedback.

201 citations


Journal ArticleDOI
TL;DR: In this paper, the authors provide a network approach insensitive to the effects that epoch length has on functional connectivity and network reconstruction, and show that both PLI and AEC depend on epoch length and that this has an impact on the reconstructed network topology, particularly at the scalp-level.
Abstract: OBJECTIVE: Graph theory and network science tools have revealed fundamental mechanisms of functional brain organization in resting-state M/EEG analysis. Nevertheless, it is still not clearly understood how several methodological aspects may bias the topology of the reconstructed functional networks. In this context, the literature shows inconsistency in the chosen length of the selected epochs, impeding a meaningful comparison between results from different studies. APPROACH: The aim of this study was to provide a network approach insensitive to the effects that epoch length has on functional connectivity and network reconstruction. Two different measures, the phase lag index (PLI) and the amplitude envelope correlation (AEC) were applied to EEG resting-state recordings for a group of 18 healthy volunteers using non-overlapping epochs with variable length (1, 2, 4, 6, 8, 10, 12, 14 and 16 s). Weighted clustering coefficient (CCw), weighted characteristic path length (L w) and minimum spanning tree (MST) parameters were computed to evaluate the network topology. The analysis was performed on both scalp and source-space data. MAIN RESULTS: Results from scalp analysis show a decrease in both mean PLI and AEC values with an increase in epoch length, with a tendency to stabilize at a length of 12 s for PLI and 6 s for AEC. Moreover, CCw and L w show very similar behaviour, with metrics based on AEC more reliable in terms of stability. In general, MST parameters stabilize at short epoch lengths, particularly for MSTs based on PLI (1-6 s versus 4-8 s for AEC). At the source-level the results were even more reliable, with stability already at 1 s duration for PLI-based MSTs. SIGNIFICANCE: The present work suggests that both PLI and AEC depend on epoch length and that this has an impact on the reconstructed network topology, particularly at the scalp-level. Source-level MST topology is less sensitive to differences in epoch length, therefore enabling the comparison of brain network topology between different studies.

181 citations


Journal ArticleDOI
TL;DR: This study has validated the use of carbon fiber microelectrode arrays as a chronic neural recording technology and demonstrated the ability to detect single units with high amplitude over 3 months, and show the potential to record for even longer periods.
Abstract: OBJECTIVE Individual carbon fiber microelectrodes can record unit activity in both acute and semi-chronic (∼1 month) implants. Additionally, new methods have been developed to insert a 16 channel array of carbon fiber microelectrodes. Before assessing the in vivo long-term viability of these arrays, accelerated soak tests were carried out to determine the most stable site coating material. Next, a multi-animal, multi-month, chronic implantation study was carried out with carbon fiber microelectrode arrays and silicon electrodes. APPROACH Carbon fibers were first functionalized with one of two different formulations of PEDOT and subjected to accelerated aging in a heated water bath. After determining the best PEDOT formula to use, carbon fiber arrays were chronically implanted in rat motor cortex. Some rodents were also implanted with a single silicon electrode, while others received both. At the end of the study a subset of animals were perfused and the brain tissue sliced. Tissue sections were stained for astrocytes, microglia, and neurons. The local reactive responses were assessed using qualitative and quantitative methods. MAIN RESULTS Electrophysiology recordings showed the carbon fibers detecting unit activity for at least 3 months with average amplitudes of ∼200 μV. Histology analysis showed the carbon fiber arrays with a minimal to non-existent glial scarring response with no adverse effects on neuronal density. Silicon electrodes showed large glial scarring that impacted neuronal counts. SIGNIFICANCE This study has validated the use of carbon fiber microelectrode arrays as a chronic neural recording technology. These electrodes have demonstrated the ability to detect single units with high amplitude over 3 months, and show the potential to record for even longer periods. In addition, the minimal reactive response should hold stable indefinitely, as any response by the immune system may reach a steady state after 12 weeks.

169 citations


Journal ArticleDOI
TL;DR: The results demonstrate the ability of ECoG-based BMIs to leverage the native functional anatomy of sensorimotor cortical populations to immediately control individual finger movements in real time.
Abstract: Objective. We used native sensorimotor representations of fingers in a brain–machine interface (BMI) to achieve immediate online control of individual prosthetic fingers. Approach. Using high gamma responses recorded with a high-density electrocorticography (ECoG) array, we rapidly mapped the functional anatomy of cued finger movements. We used these cortical maps to select ECoG electrodes for a hierarchical linear discriminant analysis classification scheme to predict: (1) if any finger was moving, and, if so, (2) which digit was moving. To account for sensory feedback, we also mapped the spatiotemporal activation elicited by vibrotactile stimulation. Finally, we used this prediction framework to provide immediate online control over individual fingers of the Johns Hopkins University Applied Physics Laboratory modular prosthetic limb. Main results. The balanced classification accuracy for detection of movements during the online control session was 92% (chance: 50%). At the onset of movement, finger classification was 76% (chance: 20%), and 88% (chance: 25%) if the pinky and ring finger movements were coupled. Balanced accuracy of fully flexing the cued finger was 64%, and 77% had we combined pinky and ring commands. Offline decoding yielded a peak finger decoding accuracy of 96.5% (chance: 20%) when using an optimized selection of electrodes. Offline analysis demonstrated significant finger-specific activations throughout sensorimotor cortex. Activations either prior to movement onset or during sensory feedback led to discriminable finger control. Significance. Our results demonstrate the ability of ECoG-based BMIs to leverage the native functional anatomy of sensorimotor cortical populations to immediately control individual finger movements in real time.

167 citations


Journal ArticleDOI
TL;DR: Standard MI-BCI training protocols are suggested to be suboptimal for skill teaching, spatial ability is confirmed as impacting on MI- BCI performance, and when faced with difficult pre-training, subjects seemed to explore more strategies and therefore learn better.
Abstract: Objective While promising, ElectroEncephaloGraphy based Brain-Computer Interfaces (BCIs) remain barely used due to their lack of reliability: 15% to 30% of users are unable to control a BCI. Standard training protocols may be partly responsible as they do not satisfy recommendations from psychology. Our main objective was to determine in practice to what extent standard training protocols impact users' Motor-Imagery based BCI (MI-BCI) control performance. Approach We performed two experiments. The first consisted in evaluating a standard BCI training protocol efficiency for the acquisition of non-BCI related skills in a BCI-free context, which enabled to rule out the possible impact of BCIs on the training outcome. Thus, participants (N=54) were asked to perform simple motor-tasks. The second experiment aimed at measuring the correlations between motor-task and MI-BCI performances. The 10 best and 10 worst performers of the first study were recruited for an MI-BCI experiment during which they had to learn to perform 2 MI-tasks. We also assessed users' spatial abilities and pre-training mu rhythm amplitude, as both have been related to MI-BCI performance in the literature. Main Results Around 17% of the participants were unable to learn to perform the motor-tasks, which is close to the BCI-illiteracy rate. It suggests that standard training protocols are suboptimal for skill-teaching. No correlation was found between motor-task and MI-BCI performance. However, spatial abilities played an important role in MI-BCI performance. Besides, once the " spatial ability" covariable had been controlled for, using an ANCOVA, it appeared that participants who faced difficulty during the first experiment improved during the second while the others did not. Significance These studies suggest that 1) standard MI-BCI training protocols are suboptimal for skill-teaching, 2) spatial abilities are confirmed to impact MI-BCI performances and 3) when faced with difficult pre-training, subjects seem to explore more strategies and therefore learn better.

139 citations


Journal ArticleDOI
TL;DR: A systematic review of the literature shows that a majority of current studies focus on thoracic level injury as well as there is an emphasis on ambulatory-related primary outcome measures.
Abstract: OBJECTIVE: Powered exoskeletons promise to increase the quality of life of people with lower-body paralysis or weakened legs by assisting or restoring legged mobility while providing health benefits across multiple physiological systems. Here, a systematic review of the literature on powered exoskeletons addressed critical questions: What is the current evidence of clinical efficacy for lower-limb powered exoskeletons? What are the benefits and risks for individuals with spinal cord injury (SCI)? What are the levels of injury considered in such studies? What are their outcome measures? What are the opportunities for the next generation exoskeletons? APPROACH: A systematic search of online databases was performed to identify clinical trials and safety or efficacy studies with lower-limb powered exoskeletons for individuals with SCI. Twenty-two studies with eight powered exoskeletons thus selected, were analyzed based on the protocol design, subject demographics, study duration, and primary/secondary outcome measures for assessing exoskeleton's performance in SCI subjects. MAIN RESULTS: Findings show that the level of injury varies across studies, with T10 injuries being represented in 45.4% of the studies. A categorical breakdown of outcome measures revealed 63% of these measures were gait and ambulation related, followed by energy expenditure (16%), physiological improvements (13%), and usability and comfort (8%). Moreover, outcome measures varied across studies, and none had measures spanning every category, making comparisons difficult. SIGNIFICANCE: This review of the literature shows that a majority of current studies focus on thoracic level injury as well as there is an emphasis on ambulatory-related primary outcome measures. Future research should: 1) develop criteria for optimal selection and training of patients most likely to benefit from this technology, 2) design multimodal gait intention detection systems that engage and empower the user, 3) develop real-time monitoring and diagnostic capabilities, and 4) adopt comprehensive metrics for assessing safety, benefits, and usability. Language: en

131 citations


Journal ArticleDOI
TL;DR: These results provide evidence that signal loss in MEAs is truly multifactorial, and future MEA designs must address these problems through more durable insulation materials, more inert electrode alloys, and pharmacologic suppression of fibroblasts and leukocytes.
Abstract: Objective. Signal attenuation is a major problem facing intracortical sensors for chronic neuroprosthetic applications. Many studies suggest that failure is due to gliosis around the electrode tips, however, mechanical and material causes of failure are often overlooked. The purpose of this study was to investigate the factors contributing to progressive signal decline by using scanning electron microscopy (SEM) to visualize structural changes in chronically implanted arrays and histology to examine the tissue response at corresponding implant sites. Approach. We examined eight chronically implanted intracortical microelectrode arrays (MEAs) explanted from non-human primates at times ranging from 37 to 1051 days post-implant. We used SEM, in vivo neural recordings, and histology (GFAP, Iba-1, NeuN). Three MEAs that were never implanted were also imaged as controls. Main results. SEM revealed progressive corrosion of the platinum electrode tips and changes to the underlying silicon. The parylene insulation was prone to cracking and delamination, and in some instances the silicone elastomer also delaminated from the edges of the MEA. Substantial tissue encapsulation was observed and was often seen growing into defects in the platinum and parylene. These material defects became more common as the time in vivo increased. Histology at 37 and 1051 days post-implant showed gliosis, disruption of normal cortical architecture with minimal neuronal loss, and high Iba-1 reactivity, especially within the arachnoid and dura. Electrode tracts were either absent or barely visible in the cortex at 1051 days, but were seen in the fibrotic encapsulation material suggesting that the MEAs were lifted out of the brain. Neural recordings showed a progressive drop in impedance, signal amplitude, and viable channels over time. Significance. These results provide evidence that signal loss in MEAs is truly multifactorial. Gliosis occurs in the first few months after implantation but does not prevent useful recordings for several years. Progressive meningeal fibrosis encapsulates and lifts MEAs out of the cortex while ongoing foreign body reactions lead to progressive degradation of the materials. Long-term impedance drops are due to the corrosion of platinum, cracking and delamination of parylene, and delamination of silicone elastomer. Oxygen radicals released by cells of the immune system likely mediate the degradation of these materials. Future MEA designs must address these problems through more durable insulation materials, more inert electrode alloys, and pharmacologic suppression of fibroblasts and leukocytes.

Journal ArticleDOI
TL;DR: The proposed method allows real-time adaptive artifact removal for EEG-based closed-loop BMI applications and mobile EEG studies in general, thereby increasing the range of tasks that can be studied in action and context while reducing the need for discarding data due to artifacts.
Abstract: Objective. Non-invasive measurement of human neural activity based on the scalp electroencephalogram (EEG) allows for the development of biomedical devices that interface with the nervous system for scientific, diagnostic, therapeutic, or restorative purposes. However, EEG recordings are often considered as prone to physiological and non-physiological artifacts of different types and frequency characteristics. Among them, ocular artifacts and signal drifts represent major sources of EEG contamination, particularly in real-time closed-loop brain–machine interface (BMI) applications, which require effective handling of these artifacts across sessions and in natural settings. Approach. We extend the usage of a robust adaptive noise cancelling (ANC) scheme ( filtering) for removal of eye blinks, eye motions, amplitude drifts and recording biases simultaneously. We also characterize the volume conduction, by estimating the signal propagation levels across all EEG scalp recording areas due to ocular artifact generators. We find that the amplitude and spatial distribution of ocular artifacts vary greatly depending on the electrode location. Therefore, fixed filtering parameters for all recording areas would naturally hinder the true overall performance of an ANC scheme for artifact removal. We treat each electrode as a separate sub-system to be filtered, and without the loss of generality, they are assumed to be uncorrelated and uncoupled. Main results. Our results show over 95–99.9% correlation between the raw and processed signals at non-ocular artifact regions, and depending on the contamination profile, 40–70% correlation when ocular artifacts are dominant. We also compare our results with the offline independent component analysis and artifact subspace reconstruction methods, and show that some local quantities are handled better by our sample-adaptive real-time framework. Decoding performance is also compared with multi-day experimental data from 2 subjects, totaling 19 sessions, with and without filtering of the raw data. Significance. The proposed method allows real-time adaptive artifact removal for EEG-based closed-loop BMI applications and mobile EEG studies in general, thereby increasing the range of tasks that can be studied in action and context while reducing the need for discarding data due to artifacts. Significant increase in decoding performances also justify the effectiveness of the method to be used in real-time closed-loop BMI applications.

Journal ArticleDOI
TL;DR: The results suggest that the use of higher frequency visual stimuli is more beneficial for performance improvement and stability as time passes when developing practical SSVEP-based BCI applications.
Abstract: Objective. Most existing brain–computer interface (BCI) designs based on steady-state visual evoked potentials (SSVEPs) primarily use low frequency visual stimuli (e.g., <20 Hz) to elicit relatively high SSVEP amplitudes. While low frequency stimuli could evoke photosensitivity-based epileptic seizures, high frequency stimuli generally show less visual fatigue and no stimulus-related seizures. The fundamental objective of this study was to investigate the effect of stimulation frequency and duty-cycle on the usability of an SSVEP-based BCI system. Approach. We developed an SSVEP-based BCI speller using multiple LEDs flickering with low frequencies (6–14.9 Hz) with a duty-cycle of 50%, or higher frequencies (26–34.7 Hz) with duty-cycles of 50%, 60%, and 70%. The four different experimental conditions were tested with 26 subjects in order to investigate the impact of stimulation frequency and duty-cycle on performance and visual fatigue, and evaluated with a questionnaire survey. Resting state alpha powers were utilized to interpret our results from the neurophysiological point of view. Main results. The stimulation method employing higher frequencies not only showed less visual fatigue, but it also showed higher and more stable classification performance compared to that employing relatively lower frequencies. Different duty-cycles in the higher frequency stimulation conditions did not significantly affect visual fatigue, but a duty-cycle of 50% was a better choice with respect to performance. The performance of the higher frequency stimulation method was also less susceptible to resting state alpha powers, while that of the lower frequency stimulation method was negatively correlated with alpha powers. Significance. These results suggest that the use of higher frequency visual stimuli is more beneficial for performance improvement and stability as time passes when developing practical SSVEP-based BCI applications.

Journal ArticleDOI
TL;DR: In this article, the impact of the reference electrode impact on scalp EEG functional connectivity and graph network properties has been investigated, and it was shown that the distortion of connectivity patterns was larger for the vertex electrode (Cz), the digitally linked mastoids (DLM), the average reference (AVE), and the reference electrodes standardization technique (REST).
Abstract: OBJECTIVE Several scalp EEG functional connectivity studies, mostly clinical, seem to overlook the reference electrode impact. The subsequent interpretation of brain connectivity is thus often biased by the choice of a non-neutral reference. This study aims at systematically investigating these effects. APPROACH As EEG reference, we examined the vertex electrode (Cz), the digitally linked mastoids (DLM), the average reference (AVE), and the reference electrode standardization technique (REST). As a connectivity metric, we used the imaginary part of the coherency. We tested simulated and real data (eyes-open resting state) by evaluating the influence of electrode density, the effect of head model accuracy in the REST transformation, and the impact on the characterization of the topology of functional networks from graph analysis. MAIN RESULTS Simulations demonstrated that REST significantly reduced the distortion of connectivity patterns when compared to AVE, Cz, and DLM references. Moreover, the availability of high-density EEG systems and an accurate knowledge of the head model are crucial elements to improve REST performance, with the individual realistic head model being preferable to the standard realistic head model. For real data, a systematic change of the spatial pattern of functional connectivity depending on the chosen reference was also observed. The distortion of connectivity patterns was larger for the Cz reference, and progressively decreased when using the DLM, the AVE, and the REST. Strikingly, we also showed that network attributes derived from graph analysis, i.e. node degree and local efficiency, are significantly influenced by the EEG reference choice. SIGNIFICANCE Overall, this study highlights that significant differences arise in scalp EEG functional connectivity and graph network properties, in dependence on the chosen reference. We hope that our study will convey the message that caution should be used when interpreting and comparing results obtained from different laboratories using different reference schemes.

Journal ArticleDOI
TL;DR: It is concluded that concealed behind-the-ear EEG recordings can be an alternative to classical cap EEG acquisition for auditory attention monitoring and further evidence for the feasibility of around the- ear EEG recordings is found and well described ERPs can be measured.
Abstract: Objective. This study presents a direct comparison of a classical EEG cap setup with a new around-the-ear electrode array (cEEGrid) to gain a better understanding of the potential of ear-centered EEG. Approach. Concurrent EEG was recorded from a classical scalp EEG cap and two cEEGrids that were placed around the left and the right ear. Twenty participants performed a spatial auditory attention task in which three sound streams were presented simultaneously. The sound streams were three seconds long and differed in the direction of origin (front, left, right) and the number of beats (3, 4, 5 respectively), as well as the timbre and pitch. The participants had to attend to either the left or the right sound stream. Main results. We found clear attention modulated ERP effects reflecting the attended sound stream for both electrode setups, which agreed in morphology and effect size. A single-trial template matching classification showed that the direction of attention could be decoded significantly above chance (50%) for at least 16 out of 20 participants for both systems. The comparably high classification results of the single trial analysis underline the quality of the signal recorded with the cEEGrids. Significance. These findings are further evidence for the feasibility of around the-ear EEG recordings and demonstrate that well described ERPs can be measured. We conclude that concealed behind-the-ear EEG recordings can be an alternative to classical cap EEG acquisition for auditory attention monitoring.

Journal ArticleDOI
TL;DR: The results suggest that the phantom head and motion platform can be used to assess motion artifact removal algorithms and compare different EEG systems for motion artifact sensitivity.
Abstract: Objective. Electroencephalography (EEG) can assess brain activity during whole-body motion in humans but head motion can induce artifacts that obfuscate electrocortical signals. Definitive solutions for removing motion artifact from EEG have yet to be found, so creating methods to assess signal processing routines for removing motion artifact are needed. We present a novel method for investigating the influence of head motion on EEG recordings as well as for assessing the efficacy of signal processing approaches intended to remove motion artifact. Approach. We used a phantom head device to mimic electrical properties of the human head with three controlled dipolar sources of electrical activity embedded in the phantom. We induced sinusoidal vertical motions on the phantom head using a custom-built platform and recorded EEG signals with three different acquisition systems while the head was both stationary and in varied motion conditions. Main results. Recordings showed up to 80% reductions in signal-to-noise ratio (SNR) and up to 3600% increases in the power spectrum as a function of motion amplitude and frequency. Independent component analysis (ICA) successfully isolated the three dipolar sources across all conditions and systems. There was a high correlation (r > 0.85) and marginal increase in the independent components' (ICs) power spectrum (~15%) when comparing stationary and motion parameters. The SNR of the IC activation was 400%–700% higher in comparison to the channel data SNR, attenuating the effects of motion on SNR. Significance. Our results suggest that the phantom head and motion platform can be used to assess motion artifact removal algorithms and compare different EEG systems for motion artifact sensitivity. In addition, ICA is effective in isolating target electrocortical events and marginally improving SNR in relation to stationary recordings.

Journal ArticleDOI
TL;DR: The use of two of these devices, Utah electrode arrays and Utah slanted electrode arrays, are highlighted in two therapeutic interventions: recording volitional skeletal motor commands from the central nervous system and recording motor commands and evoking somatosensory percepts in the peripheral nervous system.
Abstract: This paper briefly describes some of the recent progress in the development of penetrating microelectrode arrays and highlights the use of two of these devices, Utah electrode arrays and Utah slanted electrode arrays, in two therapeutic interventions: recording volitional skeletal motor commands from the central nervous system, and recording motor commands and evoking somatosensory percepts in the peripheral nervous system (PNS). The paper also briefly explores other potential sites for microelectrode array interventions that could be profitably pursued and that could have important consequences in enhancing the quality of life of patients that has been compromised by disorders of the central and PNSs.

Journal ArticleDOI
TL;DR: The findings suggest that auditory oddball results measured in natural real-life scenarios are influenced mainly by increased cognitive load due to being in an unconstrained environment.
Abstract: Objective. In the past few years there has been a growing interest in studying brain functioning in natural, real-life situations. Mobile EEG allows to study the brain in real unconstrained environments but it faces the intrinsic challenge that it is impossible to disentangle observed changes in brain activity due to increase in cognitive demands by the complex natural environment or due to the physical involvement. In this work we aim to disentangle the influence of cognitive demands and distractions that arise from such outdoor unconstrained recordings. Approach. We evaluate the ERP and single trial characteristics of a three-class auditory oddball paradigm recorded in outdoor scenario's while peddling on a fixed bike or biking freely around. In addition we also carefully evaluate the trial specific motion artifacts through independent gyro measurements and control for muscle artifacts. Main results. A decrease in P300 amplitude was observed in the free biking condition as compared to the fixed bike conditions. Above chance P300 single-trial classification in highly dynamic real life environments while biking outdoors was achieved. Certain significant artifact patterns were identified in the free biking condition, but neither these nor the increase in movement (as derived from continuous gyrometer measurements) can explain the differences in classification accuracy and P300 waveform differences with full clarity. The increased cognitive load in real-life scenarios is shown to play a major role in the observed differences. Significance. Our findings suggest that auditory oddball results measured in natural real-life scenarios are influenced mainly by increased cognitive load due to being in an unconstrained environment.

Journal ArticleDOI
TL;DR: This study believes that this study represents the first demonstration that truly three-dimensional movements can be predicted from ECoG recordings in human patients, and underscores the potential to develop BCI systems with multiple degrees of freedom inhuman patients using E CoG.
Abstract: OBJECTIVE Electrocorticography (ECoG) signals have emerged as a potential control signal for brain-computer interface (BCI) applications due to balancing signal quality and implant invasiveness. While there have been numerous demonstrations in which ECoG signals were used to decode motor movements and to develop BCI systems, the extent of information that can be decoded has been uncertain. Therefore, we sought to determine if ECoG signals could be used to decode kinematics (speed, velocity, and position) of arm movements in 3D space. APPROACH To investigate this, we designed a 3D center-out reaching task that was performed by five epileptic patients undergoing temporary placement of ECoG arrays. We used the ECoG signals within a hierarchical partial-least squares (PLS) regression model to perform offline prediction of hand speed, velocity, and position. MAIN RESULTS The hierarchical PLS regression model enabled us to predict hand speed, velocity, and position during 3D reaching movements from held-out test sets with accuracies above chance in each patient with mean correlation coefficients between 0.31 and 0.80 for speed, 0.27 and 0.54 for velocity, and 0.22 and 0.57 for position. While beta band power changes were the most significant features within the model used to classify movement and rest, the local motor potential and high gamma band power changes, were the most important features in the prediction of kinematic parameters. SIGNIFICANCE We believe that this study represents the first demonstration that truly three-dimensional movements can be predicted from ECoG recordings in human patients. Furthermore, this prediction underscores the potential to develop BCI systems with multiple degrees of freedom in human patients using ECoG.

Journal ArticleDOI
TL;DR: The results demonstrate the feasibility of using a closed-loop BCI to learn to control a walking avatar under normal and altered visuomotor perturbations, which involved cortical adaptations.
Abstract: Objective The control of human bipedal locomotion is of great interest to the field of lower-body brain-computer interfaces (BCIs) for gait rehabilitation. While the feasibility of closed-loop BCI systems for the control of a lower body exoskeleton has been recently shown, multi-day closed-loop neural decoding of human gait in a BCI virtual reality (BCI-VR) environment has yet to be demonstrated. BCI-VR systems provide valuable alternatives for movement rehabilitation when wearable robots are not desirable due to medical conditions, cost, accessibility, usability, or patient preferences. Approach In this study, we propose a real-time closed-loop BCI that decodes lower limb joint angles from scalp electroencephalography (EEG) during treadmill walking to control a walking avatar in a virtual environment. Fluctuations in the amplitude of slow cortical potentials of EEG in the delta band (0.1-3 Hz) were used for prediction; thus, the EEG features correspond to time-domain amplitude modulated potentials in the delta band. Virtual kinematic perturbations resulting in asymmetric walking gait patterns of the avatar were also introduced to investigate gait adaptation using the closed-loop BCI-VR system over a period of eight days. Main results Our results demonstrate the feasibility of using a closed-loop BCI to learn to control a walking avatar under normal and altered visuomotor perturbations, which involved cortical adaptations. The average decoding accuracies (Pearson's r values) in real-time BCI across all subjects increased from (Hip: 0.18 ± 0.31; Knee: 0.23 ± 0.33; Ankle: 0.14 ± 0.22) on Day 1 to (Hip: 0.40 ± 0.24; Knee: 0.55 ± 0.20; Ankle: 0.29 ± 0.22) on Day 8. Significance These findings have implications for the development of a real-time closed-loop EEG-based BCI-VR system for gait rehabilitation after stroke and for understanding cortical plasticity induced by a closed-loop BCI-VR system.

Journal ArticleDOI
TL;DR: It is reported that VNS may benefit from improved stimulation delivery using very advanced technologies, however, most of the results from fundamental animal studies still need to be demonstrated in humans.
Abstract: Objective. Neural signals along the vagus nerve (VN) drive many somatic and autonomic functions. The clinical interest of VN stimulation (VNS) is thus potentially huge and has already been demonstrated in epilepsy. However, side effects are often elicited, in addition to the targeted neuromodulation. Approach. This review examines the state of the art of VNS applied to two emerging modulations of autonomic function: heart failure and obesity, especially morbid obesity. Main results. We report that VNS may benefit from improved stimulation delivery using very advanced technologies. However, most of the results from fundamental animal studies still need to be demonstrated in humans.

Journal ArticleDOI
TL;DR: This study demonstrates that an efficient and stable in time workload estimation can be achieved using task-independent spatially filtered ERPs elicited in a minimally intrusive manner.
Abstract: OBJECTIVE: Mental workload is frequently estimated by EEG-based mental state monitoring systems. Usually, these systems use spectral markers and event-related potentials (ERPs). To our knowledge, no study has directly compared their performance for mental workload assessment, nor evaluated the stability in time of these markers and of the performance of the associated mental workload estimators. This study proposes a comparison of two processing chains, one based on the power in five frequency bands, and one based on ERPs, both including a spatial filtering step (respectively CSP and CCA), an FLDA classification and a 10-fold cross-validation. APPROACH: To get closer to a real life implementation, spectral markers were extracted from a short window (i.e. towards reactive systems) that did not include any motor activity and the analyzed ERPs were elicited by a task-independent probe that required a reflex-like answer (i.e. close to the ones required by dead man's vigilance devices). The data were acquired from 20 participants who performed a Sternberg memory task for 90 min (i.e. 2/6 digits to memorize) inside which a simple detection task was inserted. The results were compared both when the testing was performed at the beginning and end of the session. MAIN RESULTS: Both chains performed significantly better than random; however the one based on the spectral markers had a low performance (60%) and was not stable in time. Conversely, the ERP-based chain gave very high results (91%) and was stable in time. SIGNIFICANCE: This study demonstrates that an efficient and stable in time workload estimation can be achieved using task-independent spatially filtered ERPs elicited in a minimally intrusive manner.

Journal ArticleDOI
TL;DR: The online emgFB was superior to the classic forceFB in realistic conditions that included electrotactile stimulation, limited feedback resolution (8 levels), cognitive processing delay, and time constraints (fast grasping).
Abstract: Objective. A drawback of active prostheses is that they detach the subject from the produced forces, thereby preventing direct mechanical feedback. This can be compensated by providing somatosensory feedback to the user through mechanical or electrical stimulation, which in turn may improve the utility, sense of embodiment, and thereby increase the acceptance rate. Approach. In this study, we compared a novel approach to closing the loop, namely EMG feedback (emgFB), to classic force feedback (forceFB), using electrotactile interface in a realistic task setup. Eleven intact-bodied subjects and one transradial amputee performed a routine grasping task while receiving emgFB or forceFB. The two feedback types were delivered through the same electrotactile interface, using a mixed spatial/frequency coding to transmit 8 discrete levels of the feedback variable. In emgFB, the stimulation transmitted the amplitude of the processed myoelectric signal generated by the subject (prosthesis input), and in forceFB the generated grasping force (prosthesis output). The task comprised 150 trials of routine grasping at six forces, randomly presented in blocks of five trials (same force). Interquartile range and changes in the absolute error (AE) distribution (magnitude and dispersion) with respect to the target level were used to assess precision and overall performance, respectively. Main results. Relative to forceFB, emgFB significantly improved the precision of myoelectric commands (min/max of the significant levels) for 23%/36% as well as the precision of force control for 12%/32%, in intact-bodied subjects. Also, the magnitude and dispersion of the AE distribution were reduced. The results were similar in the amputee, showing considerable improvements. Significance. Using emgFB, the subjects therefore decreased the uncertainty of the forward pathway. Since there is a correspondence between the EMG and force, where the former anticipates the latter, the emgFB allowed for predictive control, as the subjects used the feedback to adjust the desired force even before the prosthesis contacted the object. In conclusion, the online emgFB was superior to the classic forceFB in realistic conditions that included electrotactile stimulation, limited feedback resolution (8 levels), cognitive processing delay, and time constraints (fast grasping).

Journal ArticleDOI
TL;DR: The proposed flexible electrotactile stimulation system is convenient for practical applications and can be used to implement sensory perception training and/or closed-loop control of myoelectric prostheses, providing grasping force and proprioceptive feedback.
Abstract: Objective. The aim of the present work was to develop and test a flexible electrotactile stimulation system to provide real-time feedback to the prosthesis user. The system requirements were to accommodate the capabilities of advanced multi-DOF myoelectric hand prostheses and transmit the feedback variables (proprioception and force) using intuitive coding, with high resolution and after minimal training. Approach. We developed a fully-programmable and integrated electrotactile interface supporting time and space distributed stimulation over custom designed flexible array electrodes. The system implements low-level access to individual stimulation channels as well as a set of high-level mapping functions translating the state of a multi-DoF prosthesis (aperture, grasping force, wrist rotation) into a set of predefined dynamic stimulation profiles. The system was evaluated using discrimination tests employing spatial and frequency coding (10 able-bodied subjects) and dynamic patterns (10 able-bodied and 6 amputee subjects). The outcome measure was the success rate (SR) in discrimination. Main results. The more practical electrode with the common anode configuration performed similarly to the more usual concentric arrangement. The subjects could discriminate six spatial and four frequency levels with SR >90% after a few minutes of training, whereas the performance significantly deteriorated for more levels. The dynamic patterns were intuitive for the subjects, although amputees showed lower SR than able-bodied individuals (86% ± 10% versus 99% ± 3%). Significance. The tests demonstrated that the system was easy to setup and apply. The design and resolution of the multipad electrode was evaluated. Importantly, the novel dynamic patterns, which were successfully tested, can be superimposed to transmit multiple feedback variables intuitively and simultaneously. This is especially relevant for closing the loop in modern multifunction prostheses. Therefore, the proposed system is convenient for practical applications and can be used to implement sensory perception training and/or closed-loop control of myoelectric prostheses, providing grasping force and proprioceptive feedback.

Journal ArticleDOI
TL;DR: The results indicate that automatic HFO detection with unsupervised clustering methods exploring the time-frequency content of raw iEEG can be efficiently used to identify the epileptogenic zone with an accurate and efficient manner.
Abstract: Objective. High frequency oscillations (HFOs) in intracranial electroencephalography (iEEG) recordings are considered as promising clinical biomarkers of epileptogenic regions in the brain. The aim of this study is to improve and automatize the detection of HFOs by exploring the time–frequency content of iEEG and to investigate the seizure onset zone (SOZ) detection accuracy during the sleep, awake and pre-ictal states in patients with epilepsy, for the purpose of assisting the localization of SOZ in clinical practice. Approach. Ten-minute iEEG segments were defined during different states in eight patients with refractory epilepsy. A three-stage algorithm was implemented to detect HFOs in these segments. First, an amplitude based initial detection threshold was used to generate a large pool of HFO candidates. Then distinguishing features were extracted from the time and time–frequency domain of the raw iEEG and used with a Gaussian mixture model clustering to isolate HFO events from other activities. The spatial distribution of HFO clusters was correlated with the seizure onset channels identified by neurologists in seven patient with good surgical outcome. Main results. The overlapping rates of localized channels and seizure onset locations were high in all states. The best result was obtained using the iEEG data during sleep, achieving a sensitivity of 81%, and a specificity of 96%. The channels with maximum number of HFOs identified epileptogenic areas where the seizures occurred more frequently. Significance. The current study was conducted using iEEG data collected in realistic clinical conditions without channel pre-exclusion. HFOs were investigated with novel features extracted from the entire frequency band, and were correlated with SOZ in different states. The results indicate that automatic HFO detection with unsupervised clustering methods exploring the time–frequency content of raw iEEG can be efficiently used to identify the epileptogenic zone with an accurate and efficient manner.

Journal ArticleDOI
TL;DR: The results suggest that ECoG may provide a means by which stable chronic cortical recordings can be obtained with comparatively little tissue damage, facilitating the development of clinically viable BMI systems.
Abstract: Objective Electrocorticography (ECoG), used as a neural recording modality for brain-machine interfaces (BMIs), potentially allows for field potentials to be recorded from the surface of the cerebral cortex for long durations without suffering the host-tissue reaction to the extent that it is common with intracortical microelectrodes. Though the stability of signals obtained from chronically implanted ECoG electrodes has begun receiving attention, to date little work has characterized the effects of long-term implantation of ECoG electrodes on underlying cortical tissue. Approach We implanted and recorded from a high-density ECoG electrode grid subdurally over cortical motor areas of a Rhesus macaque for 666 d. Main results Histological analysis revealed minimal damage to the cortex underneath the implant, though the grid itself was encapsulated in collagenous tissue. We observed macrophages and foreign body giant cells at the tissue-array interface, indicative of a stereotypical foreign body response. Despite this encapsulation, cortical modulation during reaching movements was observed more than 18 months post-implantation. Significance These results suggest that ECoG may provide a means by which stable chronic cortical recordings can be obtained with comparatively little tissue damage, facilitating the development of clinically viable BMI systems.

Journal ArticleDOI
TL;DR: The initial efforts toward the design of a neural speech recognition system that performs continuous phoneme recognition on English stimuli with arbitrary vocabulary sizes using the high gamma band power of local field potentials in the STG and neighboring cortical areas obtained via electrocorticography are described.
Abstract: Objective The superior temporal gyrus (STG) and neighboring brain regions play a key role in human language processing. Previous studies have attempted to reconstruct speech information from brain activity in the STG, but few of them incorporate the probabilistic framework and engineering methodology used in modern speech recognition systems. In this work, we describe the initial efforts toward the design of a neural speech recognition (NSR) system that performs continuous phoneme recognition on English stimuli with arbitrary vocabulary sizes using the high gamma band power of local field potentials in the STG and neighboring cortical areas obtained via electrocorticography. Approach The system implements a Viterbi decoder that incorporates phoneme likelihood estimates from a linear discriminant analysis model and transition probabilities from an n-gram phonemic language model. Grid searches were used in an attempt to determine optimal parameterizations of the feature vectors and Viterbi decoder. Main results The performance of the system was significantly improved by using spatiotemporal representations of the neural activity (as opposed to purely spatial representations) and by including language modeling and Viterbi decoding in the NSR system. Significance These results emphasize the importance of modeling the temporal dynamics of neural responses when analyzing their variations with respect to varying stimuli and demonstrate that speech recognition techniques can be successfully leveraged when decoding speech from neural signals. Guided by the results detailed in this work, further development of the NSR system could have applications in the fields of automatic speech recognition and neural prosthetics.

Journal ArticleDOI
TL;DR: This work shows the importance of using realistic binaural listening conditions and training on a balanced set of experimental conditions to obtain results that are more representative for the true AAD performance in practical applications.
Abstract: Objective. We consider the problem of Auditory Attention Detection (AAD), where the goal is to detect which speaker a person is attending to, in a multi-speaker environment, based on neural activity. This work aims to analyze the influence of head-related filtering and ear-specific decoding on the performance of an AAD algorithm. Approach. We recorded high-density EEG of 16 normal-hearing subjects as they listened to two speech streams while tasked to attend to the speaker in either their left or right ear. The attended ear was switched between trials. The speech stimuli were administered either dichotically, or after filtering using Head-Related Transfer Functions (HRTFs). A spatio-temporal decoder was trained and used to reconstruct the attended stimulus envelope, and the correlations between the reconstructed and the original stimulus envelopes were used to perform AAD, and arrive at a percentage correct score over all trials. Main results. We found that the HRTF condition resulted in significantly higher AAD performance than the dichotic condition. However, speech intelligibility, measured under the same set of conditions, was lower for the HRTF filtered stimuli. We also found that decoders trained and tested for a specific attended ear performed better, compared to decoders trained and tested for both left and right attended ear simultaneously. In the context of the decoders supporting hearing prostheses, the former approach is less realistic, and studies in which each subject always had to attend to the same ear may find over-optimistic results. Significance. This work shows the importance of using realistic binaural listening conditions and training on a balanced set of experimental conditions to obtain results that are more representative for the true AAD performance in practical applications.

Journal ArticleDOI
TL;DR: S/N was more stable over post-implant time than was AP amplitude, but its increased correlation with neuronal density after many months indicates ongoing loss of neurons around the microelectrodes, which appears to pose the greatest threats to the microElectrodes' long-term functionality.
Abstract: Objective To quantify relations between the neuronal activity recorded with chronically-implanted intracortical microelectrodes and the histology of the surrounding tissue, using radial distance from the tip sites and time after array implantation as parameters. Approach 'Utah'-type intracortical microelectrode arrays were implanted into cats' sensorimotor cortex for 275-364 days. The brain tissue around the implants was immuno-stained for the neuronal marker NeuN and for the astrocyte marker GFAP. Pearson's product-moment correlations were used to quantify the relations between these markers and the amplitudes of the recorded neuronal action potentials (APs) and their signal-to-noise ratios (S/N). Main results S/N was more stable over post-implant time than was AP amplitude, but its increased correlation with neuronal density after many months indicates ongoing loss of neurons around the microelectrodes. S/N was correlated with neuron density out to at least 140 μm from the microelectrodes, while AP amplitude was correlated with neuron density and GFAP density within ∼80 μm. Correlations between AP amplitude and histology markers (GFAP and NeuN density) were strongest immediately after implantation, while correlation between the neuron density and S/N was strongest near the time the animals were sacrificed. Unlike AP amplitude, there was no significant correlation between S/N and density of GFAP around the tip sites. Significance Our findings indicate an evolving interaction between changes in the tissue surrounding the microelectrodes and the microelectrode's electrical properties. Ongoing loss of neurons around recording microelectrodes, and the interactions between their delayed electrical deterioration and early tissue scarring around the tips appear to pose the greatest threats to the microelectrodes' long-term functionality.

Journal ArticleDOI
TL;DR: Combined BCI-FES therapy results in better neurological recovery and better improvement of muscle strength than FES alone, and should be considered as a therapeutic tool rather than solely a long-term assistive device for the restoration of a lost function.
Abstract: Objective. To compare neurological and functional outcomes between two groups of hospitalised patients with subacute tetraplegia. Approach. Seven patients received 20 sessions of brain computer interface (BCI) controlled functional electrical stimulation (FES) while five patients received the same number of sessions of passive FES for both hands. The neurological assessment measures were event related desynchronization (ERD) during movement attempt, Somatosensory evoked potential (SSEP) of the ulnar and median nerve; assessment of hand function involved the range of motion (ROM) of wrist and manual muscle test. Main results. Patients in both groups initially had intense ERD during movement attempt that was not restricted to the sensory-motor cortex. Following the treatment, ERD cortical activity restored towards the activity in able-bodied people in BCI-FES group only, remaining wide-spread in FES group. Likewise, SSEP returned in 3 patients in BCI-FES group, having no changes in FES group. The ROM of the wrist improved in both groups. Muscle strength significantly improved for both hands in BCI-FES group. For FES group, a significant improvement was noticed for right hand flexor muscles only. Significance. Combined BCI-FES therapy results in better neurological recovery and better improvement of muscle strength than FES alone. For spinal cord injured patients, BCI-FES should be considered as a therapeutic tool rather than solely a long-term assistive device for the restoration of a lost function.