Correction: Predicting Mental Imagery-Based BCI Performance from Personality, Cognitive Profile and Neurophysiological Patterns.

[This corrects the article DOI: 10.1371/journal.pone.0143962.].

Influence of the visuo-proprioceptive illusion of movement and motor imagery of the wrist on EEG cortical excitability among healthy participants.

INTRODUCTION: Motor Imagery (MI) is a powerful tool to stimulate sensorimotor brain areas and is currently used in motor rehabilitation after a stroke. The aim of our study was to evaluate whether an illusion of movement induced by visuo-proprioceptive immersion (VPI) including tendon vibration (TV) and Virtual moving hand (VR) combined with MI tasks could be more efficient than VPI alone or MI alone on cortical excitability assessed using Electroencephalography (EEG). METHODS: We recorded EEG signals in 20 healthy participants in 3 different conditions: MI tasks involving their non-dominant wrist (MI condition); VPI condition; and VPI with MI tasks (combined condition). Each condition lasted 3 minutes, and was repeated 3 times in randomized order. Our main judgment criterion was the Event-Related De-synchronization (ERD) threshold in sensori-motor areas in each condition in the brain motor area. RESULTS: The combined condition induced a greater change in the ERD percentage than the MI condition alone, but no significant difference was found between the combined and the VPI condition (p = 0.07) and between the VPI and MI condition (p = 0.20). CONCLUSION: This study demonstrated the interest of using a visuo-proprioceptive immersion with MI rather than MI alone in order to increase excitability in motor areas of the brain. Further studies could test this hypothesis among patients with stroke to provide new perspectives for motor rehabilitation in this population.

Long-Term BCI Training of a Tetraplegic User: Adaptive Riemannian Classifiers and User Training.

While often presented as promising assistive technologies for motor-impaired users, electroencephalography (EEG)-based Brain-Computer Interfaces (BCIs) remain barely used outside laboratories due to low reliability in real-life conditions. There is thus a need to design long-term reliable BCIs that can be used outside-of-the-lab by end-users, e.g., severely motor-impaired ones. Therefore, we propose and evaluate the design of a multi-class Mental Task (MT)-based BCI for longitudinal training (20 sessions over 3 months) of a tetraplegic user for the CYBATHLON BCI series 2019. In this BCI championship, tetraplegic pilots are mentally driving a virtual car in a racing video game. We aimed at combining a progressive user MT-BCI training with a newly designed machine learning pipeline based on adaptive Riemannian classifiers shown to be promising for real-life applications. We followed a two step training process: the first 11 sessions served to train the user to control a 2-class MT-BCI by performing either two cognitive tasks (REST and MENTAL SUBTRACTION) or two motor-imagery tasks (LEFT-HAND and RIGHT-HAND). The second training step (9 remaining sessions) applied an adaptive, session-independent Riemannian classifier that combined all 4 MT classes used before. Moreover, as our Riemannian classifier was incrementally updated in an unsupervised way it would capture both within and between-session non-stationarity. Experimental evidences confirm the effectiveness of this approach. Namely, the classification accuracy improved by about 30% at the end of the training compared to initial sessions. We also studied the neural correlates of this performance improvement. Using a newly proposed BCI user learning metric, we could show our user learned to improve his BCI control by producing EEG signals matching increasingly more the BCI classifier training data distribution, rather than by improving his EEG class discrimination. However, the resulting improvement was effective only on synchronous (cue-based) BCI and it did not translate into improved CYBATHLON BCI game performances. For the sake of overcoming this in the future, we unveil possible reasons for these limited gaming performances and identify a number of promising future research directions. Importantly, we also report on the evolution of the user's neurophysiological patterns and user experience throughout the BCI training and competition.

Why we should systematically assess, control and report somatosensory impairments in BCI-based motor rehabilitation after stroke studies.

The neuronal loss resulting from stroke forces 80% of the patients to undergo motor rehabilitation, for which Brain-Computer Interfaces (BCIs) and NeuroFeedback (NF) can be used. During the rehabilitation, when patients attempt or imagine performing a movement, BCIs/NF provide them with a synchronized sensory (e.g., tactile) feedback based on their sensorimotor-related brain activity that aims at fostering brain plasticity and motor recovery. The co-activation of ascending (i.e., somatosensory) and descending (i.e., motor) networks indeed enables significant functional motor improvement, together with significant sensorimotor-related neurophysiological changes. Somatosensory abilities are essential for patients to perceive the feedback provided by the BCI system. Thus, somatosensory impairments may significantly alter the efficiency of BCI-based motor rehabilitation. In order to precisely understand and assess the impact of somatosensory impairments, we first review the literature on post-stroke BCI-based motor rehabilitation (14 randomized clinical trials). We show that despite the central role that somatosensory abilities play on BCI-based motor rehabilitation post-stroke, the latter are rarely reported and used as inclusion/exclusion criteria in the literature on the matter. We then argue that somatosensory abilities have repeatedly been shown to influence the motor rehabilitation outcome, in general. This stresses the importance of also considering them and reporting them in the literature in BCI-based rehabilitation after stroke, especially since half of post-stroke patients suffer from somatosensory impairments. We argue that somatosensory abilities should systematically be assessed, controlled and reported if we want to precisely assess the influence they have on BCI efficiency. Not doing so could result in the misinterpretation of reported results, while doing so could improve (1) our understanding of the mechanisms underlying motor recovery (2) our ability to adapt the therapy to the patients' impairments and (3) our comprehension of the between-subject and between-study variability of therapeutic outcomes mentioned in the literature.

Consensus on the reporting and experimental design of clinical and cognitive-behavioural neurofeedback studies (CRED-nf checklist).

Neurofeedback has begun to attract the attention and scrutiny of the scientific and medical mainstream. Here, neurofeedback researchers present a consensus-derived checklist that aims to improve the reporting and experimental design standards in the field.

Using EEG-based brain computer interface and neurofeedback targeting sensorimotor rhythms to improve motor skills: Theoretical background, applications and prospects.

Many Brain Computer Interface (BCI) and neurofeedback studies have investigated the impact of sensorimotor rhythm (SMR) self-regulation training procedures on motor skills enhancement in healthy subjects and patients with motor disabilities. This critical review aims first to introduce the different definitions of SMR EEG target in BCI/Neurofeedback studies and to summarize the background from neurophysiological and neuroplasticity studies that led to SMR being considered as reliable and valid EEG targets to improve motor skills through BCI/neurofeedback procedures. The second objective of this review is to introduce the main findings regarding SMR BCI/neurofeedback in healthy subjects. Third, the main findings regarding BCI/neurofeedback efficiency in patients with hypokinetic activities (in particular, motor deficit following stroke) as well as in patients with hyperkinetic activities (in particular, Attention Deficit Hyperactivity Disorder, ADHD) will be introduced. Due to a range of limitations, a clear association between SMR BCI/neurofeedback training and enhanced motor skills has yet to be established. However, SMR BCI/neurofeedback appears promising, and highlights many important challenges for clinical neurophysiology with regards to therapeutic approaches using BCI/neurofeedback.

Defining and quantifying users' mental imagery-based BCI skills: a first step.

OBJECTIVE: While promising for many applications, electroencephalography (EEG)-based brain-computer interfaces (BCIs) are still scarcely used outside laboratories, due to a poor reliability. It is thus necessary to study and fix this reliability issue. Doing so requires the use of appropriate reliability metrics to quantify both the classification algorithm and the BCI user's performances. So far, classification accuracy (CA) is the typical metric used for both aspects. However, we argue in this paper that CA is a poor metric to study BCI users' skills. Here, we propose a definition and new metrics to quantify such BCI skills for mental imagery (MI) BCIs, independently of any classification algorithm. APPROACH: We first show in this paper that CA is notably unspecific, discrete, training data and classifier dependent, and as such may not always reflect successful self-modulation of EEG patterns by the user. We then propose a definition of MI-BCI skills that reflects how well the user can self-modulate EEG patterns, and thus how well he could control an MI-BCI. Finally, we propose new performance metrics, classDis, restDist and classStab that specifically measure how distinct and stable the EEG patterns produced by the user are, independently of any classifier. MAIN RESULTS: By re-analyzing EEG data sets with such new metrics, we indeed confirmed that CA may hide some increase in MI-BCI skills or hide the user inability to self-modulate a given EEG pattern. On the other hand, our new metrics could reveal such skill improvements as well as identify when a mental task performed by a user was no different than rest EEG. SIGNIFICANCE: Our results showed that when studying MI-BCI users' skills, CA should be used with care, and complemented with metrics such as the new ones proposed. Our results also stressed the need to redefine BCI user training by considering the different BCI subskills and their measures. To promote the complementary use of our new metrics, we provide the Matlab code to compute them for free and open-source.

Using Recent BCI Literature to Deepen our Understanding of Clinical Neurofeedback: A Short Review.

In their recent paper, Alkoby et al. (2017) provide the readership with an extensive and very insightful review of the factors influencing NeuroFeedback (NF) performance. These factors are drawn from both the NF literature and the Brain-Computer Interface (BCI) literature. Our short review aims to complement Alkoby et al.'s review by reporting recent additions to the BCI literature. The object of this paper is to highlight this literature and discuss its potential relevance and usefulness to better understand the processes underlying NF and further improve the design of clinical trials assessing NF efficacy. Indeed, we are convinced that while NF and BCI are fundamentally different in many ways, both the BCI and NF communities could reach compelling achievements by building upon one another. By reviewing the recent BCI literature, we identified three types of factors that influence BCI performance: task-specific, cognitive/motivational and technology-acceptance-related factors. Since BCIs and NF share a common goal (i.e., learning to modulate specific neurophysiological patterns), similar cognitive and neurophysiological processes are likely to be involved during the training process. Thus, the literature on BCI training may help (1) to deepen our understanding of neurofeedback training processes and (2) to understand the variables that influence the clinical efficacy of NF. This may help to properly assess and/or control the influence of these variables during randomized controlled trials.

Why standard brain-computer interface (BCI) training protocols should be changed: an experimental study.

OBJECTIVE: While promising, electroencephaloraphy based brain-computer interfaces (BCIs) are 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 the efficiency of a standard BCI training protocol for the acquisition of non-BCI related skills in a BCI-free context, which enabled us 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 was aimed at measuring the correlations between motor tasks and MI-BCI performance. The ten best and ten worst performers of the first study were recruited for an MI-BCI experiment during which they had to learn to perform two MI tasks. We also assessed users' spatial ability and pre-training µ 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. This suggests that standard training protocols are suboptimal for skill teaching. No correlation was found between motor tasks and MI-BCI performance. However, spatial ability played an important role in MI-BCI performance. In addition, 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 ability is confirmed as impacting on MI-BCI performance, and (3) when faced with difficult pre-training, subjects seemed to explore more strategies and therefore learn better.

Predicting Mental Imagery-Based BCI Performance from Personality, Cognitive Profile and Neurophysiological Patterns.

Mental-Imagery based Brain-Computer Interfaces (MI-BCIs) allow their users to send commands to a computer using their brain-activity alone (typically measured by ElectroEncephaloGraphy-EEG), which is processed while they perform specific mental tasks. While very promising, MI-BCIs remain barely used outside laboratories because of the difficulty encountered by users to control them. Indeed, although some users obtain good control performances after training, a substantial proportion remains unable to reliably control an MI-BCI. This huge variability in user-performance led the community to look for predictors of MI-BCI control ability. However, these predictors were only explored for motor-imagery based BCIs, and mostly for a single training session per subject. In this study, 18 participants were instructed to learn to control an EEG-based MI-BCI by performing 3 MI-tasks, 2 of which were non-motor tasks, across 6 training sessions, on 6 different days. Relationships between the participants' BCI control performances and their personality, cognitive profile and neurophysiological markers were explored. While no relevant relationships with neurophysiological markers were found, strong correlations between MI-BCI performances and mental-rotation scores (reflecting spatial abilities) were revealed. Also, a predictive model of MI-BCI performance based on psychometric questionnaire scores was proposed. A leave-one-subject-out cross validation process revealed the stability and reliability of this model: it enabled to predict participants' performance with a mean error of less than 3 points. This study determined how users' profiles impact their MI-BCI control ability and thus clears the way for designing novel MI-BCI training protocols, adapted to the profile of each user.