The challenge of controlling an auditory BCI in the case of severe motor disability

Abstract Background The locked-in syndrome (LIS), due to a lesion in the pons, impedes communication. This situation can also be met after some severe brain injury or in advanced Amyotrophic Lateral Sclerosis (ALS). In the most severe condition, the persons cannot communicate at all because of a com...

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Main Authors: Perrine Séguin, Emmanuel Maby, Mélodie Fouillen, Anatole Otman, Jacques Luauté, Pascal Giraux, Dominique Morlet, Jérémie Mattout
Format: Article
Language:English
Published: BMC 2024-01-01
Series:Journal of NeuroEngineering and Rehabilitation
Subjects:
Online Access:https://doi.org/10.1186/s12984-023-01289-3
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author Perrine Séguin
Emmanuel Maby
Mélodie Fouillen
Anatole Otman
Jacques Luauté
Pascal Giraux
Dominique Morlet
Jérémie Mattout
author_facet Perrine Séguin
Emmanuel Maby
Mélodie Fouillen
Anatole Otman
Jacques Luauté
Pascal Giraux
Dominique Morlet
Jérémie Mattout
author_sort Perrine Séguin
collection DOAJ
description Abstract Background The locked-in syndrome (LIS), due to a lesion in the pons, impedes communication. This situation can also be met after some severe brain injury or in advanced Amyotrophic Lateral Sclerosis (ALS). In the most severe condition, the persons cannot communicate at all because of a complete oculomotor paralysis (Complete LIS or CLIS). This even prevents the detection of consciousness. Some studies suggest that auditory brain–computer interface (BCI) could restore a communication through a « yes–no» code. Methods We developed an auditory EEG-based interface which makes use of voluntary modulations of attention, to restore a yes–no communication code in non-responding persons. This binary BCI uses repeated speech sounds (alternating “yes” on the right ear and “no” on the left ear) corresponding to either frequent (short) or rare (long) stimuli. Users are instructed to pay attention to the relevant stimuli only. We tested this BCI with 18 healthy subjects, and 7 people with severe motor disability (3 “classical” persons with locked-in syndrome and 4 persons with ALS). Results We report online BCI performance and offline event-related potential analysis. On average in healthy subjects, online BCI accuracy reached 86% based on 50 questions. Only one out of 18 subjects could not perform above chance level. Ten subjects had an accuracy above 90%. However, most patients could not produce online performance above chance level, except for two people with ALS who obtained 100% accuracy. We report individual event-related potentials and their modulation by attention. In addition to the classical P3b, we observed a signature of sustained attention on responses to frequent sounds, but in healthy subjects and patients with good BCI control only. Conclusions Auditory BCI can be very well controlled by healthy subjects, but it is not a guarantee that it can be readily used by the target population of persons in LIS or CLIS. A conclusion that is supported by a few previous findings in BCI and should now trigger research to assess the reasons of such a gap in order to propose new and efficient solutions. Clinical trial registrations: No. NCT02567201 (2015) and NCT03233282 (2013).
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spelling doaj.art-7c627b45077242399a1e1ce0c3e506792024-01-21T12:13:07ZengBMCJournal of NeuroEngineering and Rehabilitation1743-00032024-01-0121111510.1186/s12984-023-01289-3The challenge of controlling an auditory BCI in the case of severe motor disabilityPerrine Séguin0Emmanuel Maby1Mélodie Fouillen2Anatole Otman3Jacques Luauté4Pascal Giraux5Dominique Morlet6Jérémie Mattout7Lyon Neuroscience Research Center, INSERM UMRS 1028, CNRS UMR 5292, Université Claude Bernard Lyon 1, Université de LyonLyon Neuroscience Research Center, INSERM UMRS 1028, CNRS UMR 5292, Université Claude Bernard Lyon 1, Université de LyonLyon Neuroscience Research Center, INSERM UMRS 1028, CNRS UMR 5292, Université Claude Bernard Lyon 1, Université de LyonLyon Neuroscience Research Center, INSERM UMRS 1028, CNRS UMR 5292, Université Claude Bernard Lyon 1, Université de LyonLyon Neuroscience Research Center, INSERM UMRS 1028, CNRS UMR 5292, Université Claude Bernard Lyon 1, Université de LyonLyon Neuroscience Research Center, INSERM UMRS 1028, CNRS UMR 5292, Université Claude Bernard Lyon 1, Université de LyonLyon Neuroscience Research Center, INSERM UMRS 1028, CNRS UMR 5292, Université Claude Bernard Lyon 1, Université de LyonLyon Neuroscience Research Center, INSERM UMRS 1028, CNRS UMR 5292, Université Claude Bernard Lyon 1, Université de LyonAbstract Background The locked-in syndrome (LIS), due to a lesion in the pons, impedes communication. This situation can also be met after some severe brain injury or in advanced Amyotrophic Lateral Sclerosis (ALS). In the most severe condition, the persons cannot communicate at all because of a complete oculomotor paralysis (Complete LIS or CLIS). This even prevents the detection of consciousness. Some studies suggest that auditory brain–computer interface (BCI) could restore a communication through a « yes–no» code. Methods We developed an auditory EEG-based interface which makes use of voluntary modulations of attention, to restore a yes–no communication code in non-responding persons. This binary BCI uses repeated speech sounds (alternating “yes” on the right ear and “no” on the left ear) corresponding to either frequent (short) or rare (long) stimuli. Users are instructed to pay attention to the relevant stimuli only. We tested this BCI with 18 healthy subjects, and 7 people with severe motor disability (3 “classical” persons with locked-in syndrome and 4 persons with ALS). Results We report online BCI performance and offline event-related potential analysis. On average in healthy subjects, online BCI accuracy reached 86% based on 50 questions. Only one out of 18 subjects could not perform above chance level. Ten subjects had an accuracy above 90%. However, most patients could not produce online performance above chance level, except for two people with ALS who obtained 100% accuracy. We report individual event-related potentials and their modulation by attention. In addition to the classical P3b, we observed a signature of sustained attention on responses to frequent sounds, but in healthy subjects and patients with good BCI control only. Conclusions Auditory BCI can be very well controlled by healthy subjects, but it is not a guarantee that it can be readily used by the target population of persons in LIS or CLIS. A conclusion that is supported by a few previous findings in BCI and should now trigger research to assess the reasons of such a gap in order to propose new and efficient solutions. Clinical trial registrations: No. NCT02567201 (2015) and NCT03233282 (2013).https://doi.org/10.1186/s12984-023-01289-3Auditory brain–computer interfaceLocked-in syndromeAmyotrophic lateral sclerosisEvent related potentials
spellingShingle Perrine Séguin
Emmanuel Maby
Mélodie Fouillen
Anatole Otman
Jacques Luauté
Pascal Giraux
Dominique Morlet
Jérémie Mattout
The challenge of controlling an auditory BCI in the case of severe motor disability
Journal of NeuroEngineering and Rehabilitation
Auditory brain–computer interface
Locked-in syndrome
Amyotrophic lateral sclerosis
Event related potentials
title The challenge of controlling an auditory BCI in the case of severe motor disability
title_full The challenge of controlling an auditory BCI in the case of severe motor disability
title_fullStr The challenge of controlling an auditory BCI in the case of severe motor disability
title_full_unstemmed The challenge of controlling an auditory BCI in the case of severe motor disability
title_short The challenge of controlling an auditory BCI in the case of severe motor disability
title_sort challenge of controlling an auditory bci in the case of severe motor disability
topic Auditory brain–computer interface
Locked-in syndrome
Amyotrophic lateral sclerosis
Event related potentials
url https://doi.org/10.1186/s12984-023-01289-3
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