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Clinical Trial
. 2024 Jan 18;21(1):9.
doi: 10.1186/s12984-023-01289-3.

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

Perrine Séguin #  1   2   3 , Emmanuel Maby #  1 , Mélodie Fouillen  1 , Anatole Otman  1 , Jacques Luauté  1   4 , Pascal Giraux  1   2   3 , Dominique Morlet  1 , Jérémie Mattout  5
Affiliations
Clinical Trial

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

Perrine Séguin et al. J Neuroeng Rehabil. .

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).

Keywords: Amyotrophic lateral sclerosis; Auditory brain–computer interface; Event related potentials; Locked-in syndrome.

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Conflict of interest statement

The authors declare no competing interests as defined by BMC, or other interests that might be perceived to influence the results and/or discussion reported in this paper.

Figures

Fig. 1
Fig. 1
Auditory brain-computer interface protocol for healthy subjects (SOA = 250 ms). One block comprised 30 standards sounds and 6 deviants of each category (“Yes” or “No”), i.e. 72 stimuli. The deviant sounds happen randomly. It took 18 s to obtain an answer
Fig. 2
Fig. 2
EEG electrode lay-out
Fig. 3
Fig. 3
Offline classification results of ATTENDED versus IGNORED stimuli with and without ICA correction. Offline BCI simulations with 15 channels, for healthy subjects (a) and patients (b). Boxplots filled with light gray stand for accuracy results with no pre-processing of the data, except filtering. Boxplots filled with dark gray stand for the condition where the signal was preprocessed with ICA, removing blinks, saccades and a DC component. Stimulations: Total: Pool of responses to all stimuli, STD: Pool of all responses do standards, DEV: Pool of all responses to deviants, YES: Pool of all responses to « yes», NO: Pool of all responses to « no»
Fig. 4
Fig. 4
Offline classification results of ATTENDED versus IGNORED stimuli with different duration of blocks. Offline BCI simulations with 15 channels, for healthy subjects. Stimulations: Total: Pool of responses to all stimuli, STD: Pool of all responses do standards, DEV: Pool of all responses to deviants, YES: Pool of all responses to « yes», NO: Pool of all responses to « no»
Fig. 5
Fig. 5
Backward selection of relevant electrodes. A Horizontal axis, from left to right: at each step of the backward selection, an additional electrode is removed (the one that minimizes the loss in accuracy). Vertical axis: Accuracy. B Spatial locations of the most relevant 15 electrodes in green rectangle. Spatial location of the most relevant 7 electrodes in red rectangle
Fig. 6
Fig. 6
Effect of attention on event related potentials (ERPs): group average for healthy subjects. Mean ERPs for attended and unattended sounds, standards (a) and deviants (b). The SOA is at 250 ms, with an alternance of ATTENDED (Att) and IGNORED (Ign) sounds, hence a switch in the attentional modulation every 250 ms. Each stimulus onset is represented by a vertical dashed line. The solid curve depicts the response when the first stimulus is attended, while the dashed curve depicts the responses when the first stimulus is ignored. The shaded area corresponds to the period when this difference is significant. This analysis was performed on the preprocessed signals using ICA. TFCE: Threshold-free cluster enhancement test for the difference between attended and ignored sounds. Each line represents one electrode. When significant, the clusters for one electrode appear in white (negative) or in gray (positive). There is no significant cluster for the standards
Fig. 7
Fig. 7
Effect of attention on averaged evoked related potentials (ERPs) to sounds “yes” in patient ALS3 and ALS4. Mean ERPs for attended and unattended sounds, standards (a) and deviants (b). The SOA is at 400 ms, with an alternance of ATTENDED (Att) and IGNORED (Ign) sounds, hence a switch in the attentional modulation every 400 ms. Each stimulus onset is represented by a vertical dashed line. The solid curve depicts the response when the first stimulus is attended, while the dashed curve depicts the responses when the first stimulus is ignored. The shaded area corresponds to the period when this difference is significant. This analysis was performed on the preprocessed signals using ICA. TFCE: Threshold-free cluster enhancement test for the difference between attended and ignored sounds. Each line represents one electrode. When significant, the clusters for one electrode appear in white (negative) or in gray (positive)
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