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.

BioPyC, an Open-Source Python Toolbox for Offline Electroencephalographic and Physiological Signals Classification.

Research on brain-computer interfaces (BCIs) has become more democratic in recent decades, and experiments using electroencephalography (EEG)-based BCIs has dramatically increased. The variety of protocol designs and the growing interest in physiological computing require parallel improvements in processing and classification of both EEG signals and bio signals, such as electrodermal activity (EDA), heart rate (HR) or breathing. If some EEG-based analysis tools are already available for online BCIs with a number of online BCI platforms (e.g., BCI2000 or OpenViBE), it remains crucial to perform offline analyses in order to design, select, tune, validate and test algorithms before using them online. Moreover, studying and comparing those algorithms usually requires expertise in programming, signal processing and machine learning, whereas numerous BCI researchers come from other backgrounds with limited or no training in such skills. Finally, existing BCI toolboxes are focused on EEG and other brain signals but usually do not include processing tools for other bio signals. Therefore, in this paper, we describe BioPyC, a free, open-source and easy-to-use Python platform for offline EEG and biosignal processing and classification. Based on an intuitive and well-guided graphical interface, four main modules allow the user to follow the standard steps of the BCI process without any programming skills: (1) reading different neurophysiological signal data formats, (2) filtering and representing EEG and bio signals, (3) classifying them, and (4) visualizing and performing statistical tests on the results. We illustrate BioPyC use on four studies, namely classifying mental tasks, the cognitive workload, emotions and attention states from EEG signals.

Monitoring Pilot's Mental Workload Using ERPs and Spectral Power with a Six-Dry-Electrode EEG System in Real Flight Conditions.

Recent technological progress has allowed the development of low-cost and highly portable brain sensors such as pre-amplified dry-electrodes to measure cognitive activity out of the laboratory. This technology opens promising perspectives to monitor the "brain at work" in complex real-life situations such as while operating aircraft. However, there is a need to benchmark these sensors in real operational conditions. We therefore designed a scenario in which twenty-two pilots equipped with a six-dry-electrode EEG system had to perform one low load and one high load traffic pattern along with a passive auditory oddball. In the low load condition, the participants were monitoring the flight handled by a flight instructor, whereas they were flying the aircraft in the high load condition. At the group level, statistical analyses disclosed higher P300 amplitude for the auditory target (Pz, P4 and Oz electrodes) along with higher alpha band power (Pz electrode), and higher theta band power (Oz electrode) in the low load condition as compared to the high load one. Single trial classification accuracy using both event-related potentials and event-related frequency features at the same time did not exceed chance level to discriminate the two load conditions. However, when considering only the frequency features computed over the continuous signal, classification accuracy reached around 70% on average. This study demonstrates the potential of dry-EEG to monitor cognition in a highly ecological and noisy environment, but also reveals that hardware improvement is still needed before it can be used for everyday flight operations.

Ecological decoding of visual aesthetic preference with oscillatory electroencephalogram features-A mini-review.

In today's digital information age, human exposure to visual artifacts has reached an unprecedented quasi-omnipresence. Some of these cultural artifacts are elevated to the status of artworks which indicates a special appreciation of these objects. For many persons, the perception of such artworks coincides with aesthetic experiences (AE) that can positively affect health and wellbeing. AEs are composed of complex cognitive and affective mental and physiological states. More profound scientific understanding of the neural dynamics behind AEs would allow the development of passive Brain-Computer-Interfaces (BCI) that offer personalized art presentation to improve AE without the necessity of explicit user feedback. However, previous empirical research in visual neuroaesthetics predominantly investigated functional Magnetic Resonance Imaging and Event-Related-Potentials correlates of AE in unnaturalistic laboratory conditions which might not be the best features for practical neuroaesthetic BCIs. Furthermore, AE has, until recently, largely been framed as the experience of beauty or pleasantness. Yet, these concepts do not encompass all types of AE. Thus, the scope of these concepts is too narrow to allow personalized and optimal art experience across individuals and cultures. This narrative mini-review summarizes the state-of-the-art in oscillatory Electroencephalography (EEG) based visual neuroaesthetics and paints a road map toward the development of ecologically valid neuroaesthetic passive BCI systems that could optimize AEs, as well as their beneficial consequences. We detail reported oscillatory EEG correlates of AEs, as well as machine learning approaches to classify AE. We also highlight current limitations in neuroaesthetics and suggest future directions to improve EEG decoding of AE.

Modeling Complex EEG Data Distribution on the Riemannian Manifold Toward Outlier Detection and Multimodal Classification.

OBJECTIVE: The usage of Riemannian geometry for Brain-computer interfaces (BCIs) has gained momentum in recent years. Most of the machine learning techniques proposed for Riemannian BCIs consider the data distribution on a manifold to be unimodal. However, the distribution is likely to be multimodal rather than unimodal since high-data variability is a crucial limitation of electroencephalography (EEG). In this paper, we propose a novel data modeling method for considering complex data distributions on a Riemannian manifold of EEG covariance matrices, aiming to improve BCI reliability. METHODS: Our method, Riemannian spectral clustering (RiSC), represents EEG covariance matrix distribution on a manifold using a graph with proposed similarity measurement based on geodesic distances, then clusters the graph nodes through spectral clustering. This allows flexibility to model both a unimodal and a multimodal distribution on a manifold. RiSC can be used as a basis to design an outlier detector named outlier detection Riemannian spectral clustering (odenRiSC) and a multimodal classifier named multimodal classifier Riemannian spectral clustering (mcRiSC). All required parameters of odenRiSC/mcRiSC are selected in data-driven manner. Moreover, there is no need to pre-set a threshold for outlier detection and the number of modes for multimodal classification. RESULTS: The experimental evaluation revealed odenRiSC can detect EEG outliers more accurately than existing methods and mcRiSC outperformed the standard unimodal classifier, especially on high-variability datasets. CONCLUSION: odenRiSC/mcRiSC are anticipated to contribute to making real-life BCIs outside labs and neuroergonomics applications more robust. SIGNIFICANCE: RiSC can work as a robust EEG outlier detector and multimodal classifier.

Impact of the baseline temporal selection on the ERD/ERS analysis for Motor Imagery-based BCI.

Motor Imagery-based Brain-Computer Interfaces (MI-BCIs) are neurotechnologies that exploit the modulation of sensorimotor rhythms over the motor cortices, respectively known as Event-Related Desynchronization (ERD) and Synchronization (ERS). The interpretation of ERD/ERS is directly related to the selection of the baseline used to estimate them, and might result in a misleading ERD/ERS visualization. In fact, in BCI paradigms, if two trials are separated by a few seconds, taking a baseline close to the end of the previous trial could result in an over-estimation of the ERD, while taking a baseline too close to the upcoming trial could result in an under-estimation of the ERD. This phenomenon may cause a functional misinterpretation of the ERD/ERS phenomena in MI-BCI studies. This may also impair BCI performances for MI vs Rest classification, since such baselines are often used as resting states. In this paper, we propose to investigate the effect of several baseline time window selections on ERD/ERS modulations and BCI performances. Our results show that considering the selected temporal baseline effect is essential to analyze the modulations of ERD/ERS during MI-BCI use.

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

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

A large EEG database with users' profile information for motor imagery brain-computer interface research.

We present and share a large database containing electroencephalographic signals from 87 human participants, collected during a single day of brain-computer interface (BCI) experiments, organized into 3 datasets (A, B, and C) that were all recorded using the same protocol: right and left hand motor imagery (MI). Each session contains 240 trials (120 per class), which represents more than 20,800 trials, or approximately 70 hours of recording time. It includes the performance of the associated BCI users, detailed information about the demographics, personality profile as well as some cognitive traits and the experimental instructions and codes (executed in the open-source platform OpenViBE). Such database could prove useful for various studies, including but not limited to: (1) studying the relationships between BCI users' profiles and their BCI performances, (2) studying how EEG signals properties varies for different users' profiles and MI tasks, (3) using the large number of participants to design cross-user BCI machine learning algorithms or (4) incorporating users' profile information into the design of EEG signal classification algorithms.

Riemannian Channel Selection for BCI With Between-Session Non-Stationarity Reduction Capabilities.

OBJECTIVE: Between-session non-stationarity is a major challenge of current Brain-Computer Interfaces (BCIs) that affects system performance. In this paper, we investigate the use of channel selection for reducing between-session non-stationarity with Riemannian BCI classifiers. We use the Riemannian geometry framework of covariance matrices due to its robustness and promising performances. Current Riemannian channel selection methods do not consider between-session non-stationarity and are usually tested on a single session. Here, we propose a new channel selection approach that specifically considers non-stationarity effects and is assessed on multi-session BCI data sets. METHODS: We remove the least significant channels using a sequential floating backward selection search strategy. Our contributions include: 1) quantifying the non-stationarity effects on brain activity in multi-class problems by different criteria in a Riemannian framework and 2) a method to predict whether BCI performance can improve using channel selection. RESULTS: We evaluate the proposed approaches on three multi-session and multi-class mental tasks (MT)-based BCI datasets. They could lead to significant improvements in performance as compared to using all channels for datasets affected by between-session non-stationarity and to significant superiority to the state-of-the-art Riemannian channel selection methods over all datasets, notably when selecting small channel set sizes. CONCLUSION: Reducing non-stationarity by channel selection could significantly improve Riemannian BCI classification accuracy. SIGNIFICANCE: Our proposed channel selection approach contributes to make Riemannian BCI classifiers more robust to between-session non-stationarities.

ERD modulations during motor imageries relate to users' traits and BCI performances.

Improving user performances is one of the major issues for Motor Imagery (MI) - based BCI control. MI-BCIs exploit the modulation of sensorimotor rhythms (SMR) over the motor and sensorimotor cortices to discriminate several mental states and enable user interaction. Such modulations are known as Event-Related Desynchronization (ERD) and Synchronization (ERS), coming from the mu (7-13 Hz) and beta (15-30 Hz) frequency bands. This kind of BCI opens up promising fields, particularly to control assistive technologies, for sport training or even for post-stroke motor rehabilitation. However, MI - BCIs remain barely used outside laboratories, notably due to their lack of robustness and usability (15 to 30% of users seem unable to gain control of an MI-BCI). One way to increase user performance would be to better understand the relationships between user traits and ERD/ERS modulations underlying BCI performance. Therefore, in this article we analyzed how cerebral motor patterns underlying MI tasks (i.e., ERDs and ERSs) are modulated depending (i) on nature of the task (i.e., right-hand MI and left-hand MI), (ii) the session during which the task was performed (i.e., calibration or user training) and (iii) on the characteristics of the user (e.g., age, gender, manual activity, personality traits) on a large MI-BCI data base of N=75 participants. One of the originality of this study is to combine the investigation of human factors related to the user's traits and the neurophysiological ERD modulations during the MI task. Our study revealed for the first time an association between ERD and self-control from the 16PF5 questionnaire.

Class-distinctiveness-based frequency band selection on the Riemannian manifold for oscillatory activity-based BCIs: preliminary results.

Considering user-specific settings is known to enhance Brain-Computer Interface (BCI) performances. In particular, the optimal frequency band for oscillatory activity classification is highly user-dependent and many frequency band selection methods have been developed in the past two decades. However, it is not well studied whether those conventional methods can be efficiently applied to the Riemannian BCIs, a recent family of BCI systems that utilize the non-Euclidean nature of the data unlike conventional BCI pipelines. In this paper, we proposed a novel frequency band selection method working on the Riemannian manifold. The frequency band is selected considering the class distinctiveness as quantified based on the inter-class distance and the intra-class variance on the manifold. An advantage of this method is that the frequency bandwidth can be adjusted for each individual without intensive optimization steps. In a comparative experiment using a public dataset of motor imagery-based BCI, our method showed a substantial improvement in average accuracy over both a fixed broad frequency band and a popular conventional frequency band selection method. In particular, our method substantially improved performances for subjects with initially low accuracies. This preliminary result suggests the importance of developing new user-specific setting algorithms considering the manifold properties, rather than directly applying methods developed prior to the rise of the Riemannian BCIs.

Towards Identifying Optimal Biased Feedback for Various User States and Traits in Motor Imagery BCI.

OBJECTIVE: Neural self-regulation is necessary for achieving control over brain-computer interfaces (BCIs). This can be an arduous learning process especially for motor imagery BCI. Various training methods were proposed to assist users in accomplishing BCI control and increase performance. Notably the use of biased feedback, i.e. non-realistic representation of performance. Benefits of biased feedback on performance and learning vary between users (e.g. depending on their initial level of BCI control) and remain speculative. To disentangle the speculations, we investigate what personality type, initial state and calibration performance (CP) could benefit from a biased feedback. METHODS: We conduct an experiment (n = 30 for 2 sessions). The feedback provided to each group (n = 10) is either positively, negatively or not biased. RESULTS: Statistical analyses suggest that interactions between bias and: 1) workload, 2) anxiety, and 3) self-control significantly affect online performance. For instance, low initial workload paired with negative bias is associated to higher peak performances (86%) than without any bias (69%). High anxiety relates negatively to performance no matter the bias (60%), while low anxiety matches best with negative bias (76%). For low CP, learning rate (LR) increases with negative bias only short term (LR = 2%) as during the second session it severely drops (LR = -1%). CONCLUSION: We unveil many interactions between said human factors and bias. Additionally, we use prediction models to confirm and reveal even more interactions. SIGNIFICANCE: This paper is a first step towards identifying optimal biased feedback for a personality type, state, and CP in order to maximize BCI performance and learning.

Retrospective on the First Passive Brain-Computer Interface Competition on Cross-Session Workload Estimation.

As is the case in several research domains, data sharing is still scarce in the field of Brain-Computer Interfaces (BCI), and particularly in that of passive BCIs-i.e., systems that enable implicit interaction or task adaptation based on a user's mental state(s) estimated from brain measures. Moreover, research in this field is currently hindered by a major challenge, which is tackling brain signal variability such as cross-session variability. Hence, with a view to develop good research practices in this field and to enable the whole community to join forces in working on cross-session estimation, we created the first passive brain-computer interface competition on cross-session workload estimation. This competition was part of the 3rd International Neuroergonomics conference. The data were electroencephalographic recordings acquired from 15 volunteers (6 females; average 25 y.o.) who performed 3 sessions-separated by 7 days-of the Multi-Attribute Task Battery-II (MATB-II) with 3 levels of difficulty per session (pseudo-randomized order). The data -training and testing sets-were made publicly available on Zenodo along with Matlab and Python toy code (https://doi.org/10.5281/zenodo.5055046). To this day, the database was downloaded more than 900 times (unique downloads of all version on the 10th of December 2021: 911). Eleven teams from 3 continents (31 participants) submitted their work. The best achieving processing pipelines included a Riemannian geometry-based method. Although better than the adjusted chance level (38% with an α at 0.05 for a 3-class classification problem), the results still remained under 60% of accuracy. These results clearly underline the real challenge that is cross-session estimation. Moreover, they confirmed once more the robustness and effectiveness of Riemannian methods for BCI. On the contrary, chance level results were obtained by one third of the methods-4 teams- based on Deep Learning. These methods have not demonstrated superior results in this contest compared to traditional methods, which may be due to severe overfitting. Yet this competition is the first step toward a joint effort to tackle BCI variability and to promote good research practices including reproducibility.

A review of user training methods in brain computer interfaces based on mental tasks.

Mental-tasks based brain-computer interfaces (MT-BCIs) allow their users to interact with an external device solely by using brain signals produced through mental tasks. While MT-BCIs are promising for many applications, they are still barely used outside laboratories due to their lack of reliability. MT-BCIs require their users to develop the ability to self-regulate specific brain signals. However, the human learning process to control a BCI is still relatively poorly understood and how to optimally train this ability is currently under investigation. Despite their promises and achievements, traditional training programs have been shown to be sub-optimal and could be further improved. In order to optimize user training and improve BCI performance, human factors should be taken into account. An interdisciplinary approach should be adopted to provide learners with appropriate and/or adaptive training. In this article, we provide an overview of existing methods for MT-BCI user training-notably in terms of environment, instructions, feedback and exercises. We present a categorization and taxonomy of these training approaches, provide guidelines on how to choose the best methods and identify open challenges and perspectives to further improve MT-BCI user training.

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.

Detecting EEG outliers for BCI on the Riemannian manifold using spectral clustering.

Automatically detecting and removing Electroencephalogram (EEG) outliers is essential to design robust brain-computer interfaces (BCIs). In this paper, we propose a novel outlier detection method that works on the Riemannian manifold of sample covariance matrices (SCMs). Existing outlier detection methods run the risk of erroneously rejecting some samples as outliers, even if there is no outlier, due to the detection being based on a reference matrix and a threshold. To address this limitation, our method, Riemannian Spectral Clustering (RiSC), detects outliers by clustering SCMs into non-outliers and outliers, based on a proposed similarity measure. This considers the Riemannian geometry of the space and magnifies the similarity within the non-outlier cluster and weakens it between non-outlier and outlier clusters, instead of setting a threshold. To assess RiSC performance, we generated artificial EEG datasets contaminated by different outlier strengths and numbers. Comparing Hit-False (HF) difference between RiSC and existing outlier detection methods confirmed that RiSC could detect outliers significantly better (p < 0.001). In particular, RiSC improved HF difference the most for datasets with the most severe outlier contamination.

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.

Speed of Rapid Serial Visual Presentation of Pictures, Numbers and Words Affects Event-Related Potential-Based Detection Accuracy.

Rapid serial visual presentation (RSVP) based brain-computer interfaces (BCIs) can detect target images among a continuous stream of rapidly presented images, by classifying a viewer's event related potentials (ERPs) associated with the target and non-targets images. Whilst the majority of RSVP-BCI studies to date have concentrated on the identification of a single type of image, namely pictures, here we study the capability of RSVP-BCI to detect three different target image types: pictures, numbers and words. The impact of presentation duration (speed) i.e., 100-200ms (5-10Hz), 200-300ms (3.3-5Hz) or 300-400ms (2.5-3.3Hz), is also investigated. 2-way repeated measure ANOVA on accuracies of detecting targets from non-target stimuli (ratio 1:9) measured via area under the receiver operator characteristics curve (AUC) for N=15 subjects revealed a significant effect of factor Stimulus-Type (pictures, numbers, words) (F (2,28) = 7.243, p = 0.003 ) and for Stimulus-Duration (F (2,28) = 5.591, p = 0.011). Furthermore, there is an interaction between stimulus type and duration: F (4,56) = 4.419, p = 0.004 ). The results indicate that when designing RSVP-BCI paradigms, the content of the images and the rate at which images are presented impact on the accuracy of detection and hence these parameters are key experimental variables in protocol design and applications, which apply RSVP for multimodal image datasets.

Active inference as a unifying, generic and adaptive framework for a P300-based BCI.

OBJECTIVE: Going adaptive is a major challenge for the field of brain-computer interface (BCI). This entails a machine that optimally articulates inference about the user's intentions and its own actions. Adaptation can operate over several dimensions which calls for a generic and flexible framework. APPROACH: We appeal to one of the most comprehensive computational approach to brain (adaptive) functions: the active inference (AI) framework. It entails an explicit (probabilistic) model of the user that the machine interacts with, here involved in a P300-spelling task. This takes the form of a discrete input-output state-space model establishing the link between the machine's (i) observations-a P300 or error potential for instance, (ii) representations-of the user intentions to spell or pause, and (iii) actions-to flash, spell or switch-off the application. MAIN RESULTS: Using simulations with real EEG data from 18 subjects, results demonstrate the ability of AI to yield a significant increase in bit rate (17%) over state-of-the-art approaches, such as dynamic stopping. SIGNIFICANCE: Thanks to its flexibility, this one model enables to implement optimal (dynamic) stopping but also optimal flashing (i.e. active sampling), automated error correction, and switching off when the user does not look at the screen anymore. Importantly, this approach enables the machine to flexibly arbitrate between all these possible actions. We demonstrate AI as a unifying and generic framework to implement a flexible interaction behaviour in a given BCI context.