Implementing physiologically-based approaches to improve Brain-Computer Interfaces usability in post-stroke motor rehabilitation

Stroke is one of the leading causes of long-term motor disability and, as such, directly impacts on daily living activities. Identifying new strategies to recover motor function is a central goal of clinical research. In the last years the approach to the post-stroke function restore has moved from the physical rehabilitation to the evidence-based neurological rehabilitation. Brain-Computer Interface (BCI) technology offers the possibility to detect, monitor and eventually modulate brain activity. The potential of guiding altered brain activity back to a physiological condition through BCI and the assumption that this recovery of brain activity leads to the restoration of behaviour is the key element for the use of BCI systems for therapeutic purposes. To bridge the gap between research-oriented methodology in BCI design and the usability of a system in the clinical realm requires efforts towards BCI signal processing procedures that would optimize the balance between system accuracy and usability. The thesis focused on this issue and aimed to propose new algorithms and signal processing procedures that, by combining physiological and engineering approaches, would provide the basis for designing more usable BCI systems to support post-stroke motor recovery. Results showed that introduce new physiologically-driven approaches to the pre-processing of BCI data, methods to support professional end-users in the BCI control parameter selection according to evidence-based rehabilitation principles and algorithms for the parameter adaptation in time make the BCI technology more affordable, more efficient, and more usable and, therefore, transferable to the clinical realm

Spatial filters selection towards a rehabilitation BCI

Introducing BCI technology in supporting motor imagery (MI) training has revealed the rehabilitative potential of MI, contributing to significantly better motor functional outcomes in stroke patients. To provide the most accurate and personalized feedback during the treatment, several stages of the electroencephalographic signal processing have to be optimized, including spatial filtering. This study focuses on data-independent approaches to optimize spatial filtering step. Specific aims were: i) assessment of spatial filters' performance in relation to the hand and foot scalp areas; ii) evaluation of simultaneous use of multiple spatial filters; iii) minimization of the number of electrodes needed for training. Our findings indicate that different spatial filters showed different performance related to the scalp areas considered. The simultaneous use of EEG signals conditioned with different spatial filters could either improve classification performance or, at same level of performance could lead to a reduction of the number of electrodes needed for successive training, thus improving usability of BCIs in clinical rehabilitation context

The Promotoer: a successful story of translational research in BCI for motor rehabilitation

Several groups have recently demonstrated in the context of randomized controlled trials (RCTs) how sensorimotor Brain-Computer Interface (BCI) systems can be beneficial for post-stroke motor recovery. Following a successful RCT, at Fondazione Santa Lucia (FSL) a further translational effort was made with the implementation of the Promotœr, an all in-one BCIsupported MI training station. Up to now, 25 patients underwent training with the Promotɶr during their admission for rehabilitation purposes (in add-on to standard therapy). Two illustrative cases are presented. Though currently limited to FSL, the Promotɶr represents a successful story of translational research in BCI for stroke rehabilitation. Results are promising both in terms of feasibility of a BCI training in the context of a real rehabilitation program and in terms of clinical and neurophysiological benefits observed in the patients

GUIDER: a GUI for semiautomatic, physiologically driven EEG feature selection for a rehabilitation BCI

GUIDER is a graphical user interface developed in MATLAB software environment to identify electroencephalography (EEG)-based brain computer interface (BCI) control features for a rehabilitation application (i.e. post-stroke motor imagery training). In this context, GUIDER aims to combine physiological and machine learning approaches. Indeed, GUIDER allows therapists to set parameters and constraints according to the rehabilitation principles (e.g. affected hemisphere, sensorimotor relevant frequencies) and foresees an automatic method to select the features among the defined subset. As a proof of concept, we compared offline performances between manual, just based on operator’s expertise and experience, and GUIDER semiautomatic features selection on BCI data collected from stroke patients during BCI-supported motor imagery training. Preliminary results suggest that this semiautomatic approach could be successfully applied to support the human selection reducing operator dependent variability in view of future multi-centric clinical trials

Neurophysiological constraints of control parameters for a brain computer interface system to support post-stroke motor rehabilitation

The Promotɶr is an all-in-one Brain Computer Interface (BCI)-system developed at Fondazione Santa Lucia (Rome, Italy) to support hand motor imagery practice after stroke. In this paper we focus on the optimization of control parameters for the BCI training. We compared two procedures for the feature selection: in the first, features were selected by means of a manual procedure (requiring “skilled users”), in the second a semiautomatic method, developed by us combining physiological and machine learning approaches, guided the feature selection. EEG-based BCI data set collected from 13 stroke patients were analyzed to the aim. No differences were found between the two procedures (paired-samples t-test, p=0.13). Results suggest that the semiautomatic procedure could be applied to support the manual feature selection, allowing no-skilled users to approach BCI technology for motor rehabilitation of stroke patients

Cortico-muscular coupling to control a hybrid brain-computer interface for upper limb motor rehabilitation: A pseudo-online study on stroke patients

Brain-Computer Interface (BCI) systems for motor rehabilitation after stroke have proven their efficacy to enhance upper limb motor recovery by reinforcing motor related brain activity. Hybrid BCIs (h-BCIs) exploit both central and peripheral activation and are frequently used in assistive BCIs to improve classification performances. However, in a rehabilitative context, brain and muscular features should be extracted to promote a favorable motor outcome, reinforcing not only the volitional control in the central motor system, but also the effective projection of motor commands to target muscles, i.e., central-to-peripheral communication. For this reason, we considered cortico-muscular coupling (CMC) as a feature for a h-BCI devoted to post-stroke upper limb motor rehabilitation. In this study, we performed a pseudo-online analysis on 13 healthy participants (CTRL) and 12 stroke patients (EXP) during executed (CTRL, EXP unaffected arm) and attempted (EXP affected arm) hand grasping and extension to optimize the translation of CMC computation and CMC-based movement detection from offline to online. Results showed that updating the CMC computation every 125 ms (shift of the sliding window) and accumulating two predictions before a final classification decision were the best trade-off between accuracy and speed in movement classification, independently from the movement type. The pseudo-online analysis on stroke participants revealed that both attempted and executed grasping/extension can be classified through a CMC-based movement detection with high performances in terms of classification speed (mean delay between movement detection and EMG onset around 580 ms) and accuracy (hit rate around 85%). The results obtained by means of this analysis will ground the design of a novel non-invasive h-BCI in which the control feature is derived from a combined EEG and EMG connectivity pattern estimated during upper limb movement attempts

The Promotoer, a brain-computer interface-assisted intervention to promote upper limb functional motor recovery after stroke: a statistical analysis plan for a randomized controlled trial

Background: Electroencephalography (EEG)-based brain-computer interfaces (BCIs) allow to modulate the sensorimotor rhythms and are emerging technologies for promoting post-stroke motor function recovery. The Promotoer study aims to assess the short and long-term efficacy of the Promotoer system, an EEG-based BCI assisting motor imagery (MI) practice, in enhancing post-stroke functional hand motor recovery. This paper details the statistical analysis plan of the Promotoer study. Methods: The Promotoer study is a randomized, controlled, assessor-blinded, single-centre, superiority trial, with two parallel groups and a 1:1 allocation ratio. Subacute stroke patients are randomized to EEG-based BCI-assisted MI training or to MI training alone (i.e. no BCI). An internal pilot study for sample size re-assessment is planned. The primary outcome is the effectiveness of the Upper Extremity Fugl-Meyer Assessment (UE-FMA) score. Secondary outcomes include clinical, functional, and user experience scores assessed at the end of intervention and at follow-up. Neurophysiological assessments are also planned. Effectiveness formulas have been specified, and intention-to-treat and per-protocol populations have been defined. Statistical methods for comparisons of groups and for development of a predictive score of significant improvement are described. Explorative subgroup analyses and methodology to handle missing data are considered. Discussion: The Promotoer study will provide robust evidence for the short/long-term efficacy of the Promotoer system in subacute stroke patients undergoing a rehabilitation program. Moreover, the development of a predictive score of response will allow transferring of the Promotoer system to optimal clinical practice. By carefully describing the statistical principles and procedures, the statistical analysis plan provides transparency in the analysis of data. Trial registration: ClinicalTrials.gov NCT04353297 . Registered on April 15, 2020

A user-centred approach to unlock the potential of non-invasive BCIs: an unprecedented international translational effort

Non-invasive Mental Task-based Brain-Computer Interfaces (MT-BCIs) enable their users to interact with the environment through their brain activity alone (measured using electroencephalography for example), by performing mental tasks such as mental calculation or motor imagery. Current developments in technology hint at a wide range of possible applications, both in the clinical and non-clinical domains. MT-BCIs can be used to control (neuro)prostheses or interact with video games, among many other applications. They can also be used to restore cognitive and motor abilities for stroke rehabilitation, or even improve athletic performance.Nonetheless, the expected transfer of MT-BCIs from the lab to the marketplace will be greatly impeded if all resources are allocated to technological aspects alone. We cannot neglect the Human End-User that sits in the centre of the loop. Indeed, self-regulating one’s brain activity through mental tasks to interact is an acquired skill that requires appropriate training. Yet several studies have shown that current training procedures do not enable MT-BCI users to reach adequate levels of performance. Therefore, one significant challenge for the community is that of improving end-user training.To do so, another fundamental challenge must be taken into account: we need to understand the processes that underlie MT-BCI performance and user learning. It is currently estimated that 10 to 30% of people cannot control an MT-BCI. These people are often referred to as “BCI inefficient”. But the concept of “BCI inefficiency” is debated. Does it really exist? Or, are low performances due to insufficient training, training procedures that are unsuited to these users or is the BCI data processing not sensitive enough? The currently available literature does not allow for a definitive answer to these questions as most published studies either include a limited number of participants (i.e., 10 to 20 participants) and/or training sessions (i.e., 1 or 2). We still have very little insight into what the MT-BCI learning curve looks like, and into which factors (including both user-related and machine-related factors) influence this learning curve. Finding answers will require a large number of experiments, involving a large number of participants taking part in multiple training sessions. It is not feasible for one research lab or even a small consortium to undertake such experiments alone. Therefore, an unprecedented coordinated effort from the research community is necessary.We are convinced that combining forces will allow us to characterise in detail MT-BCI user learning, and thereby provide a mandatory step toward transferring BCIs “out of the lab”. This is why we gathered an international, interdisciplinary consortium of BCI researchers from more than 20 different labs across Europe and Japan, including pioneers in the field. This collaboration will enable us to collect considerable amounts of data (at least 100 participants for 20 training sessions each) and establish a large open database. Based on this precious resource, we could then lead sound analyses to answer the previously mentioned questions. Using this data, our consortium could offer solutions on how to improve MT-BCI training procedures using innovative approaches (e.g., personalisation using intelligent tutoring systems) and technologies (e.g., virtual reality). The CHIST-ERA programme represents a unique opportunity to conduct this ambitious project, which will foster innovation in our field and strengthen our community

Brain-Computer Interface

The Brain-Computer Interfaces (BCIs) allow a person to act on the environment in absence of neuromuscular activity. The rehabilitative BCIs will be the focus of this chapter, with a special reference to the design and validation of non-invasive BCI technology in the field of neurological rehabilitation after stroke. We shall also give an overview of the most recent advancements in BCI application to restore motor function in individuals with spinal cord injury (SCI). To close the chapter, we shall remark the future developments to foster the clinical viability of BCI technology

Bipolar filters improve usability of Brain-Computer Interface technology in post-stroke motor rehabilitation

The development of usable and accurate brain-computer interface (BCI) systems enables the transfer of this technology to clinical routine. When working with electroencephalographic signals (EEG), an important factor to optimize the signal to noise ratio of the signal is to choose the appropriate spatial filters. Specific aims of this study were (a) to compare classification performances of two commonly used filters, two bipolar filters (longitudinal and transversal) and the combination of both bipolar filters obtained by pooling EEG features together, (b) to compare the number of physical electrodes needed as consequence of the spatial filter choice. Bipolar filters showed classification performances comparable to those provided by the most commonly used filters, despite requiring a significantly lower number of electrodes. Longitudinal bipolar filters showed the best accuracy to number of electrodes ratio; thus, its usage is suggested for applications such as upper limb motor rehabilitation in post-stroke patient