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Research ArticleResearch Article: Negative Results, Cognition and Behavior

Long-Range α-Synchronization as Control Signal for BCI: A Feasibility Study

Martín Esparza-Iaizzo, Irene Vigué-Guix, Manuela Ruzzoli, Mireia Torralba-Cuello and Salvador Soto-Faraco
eNeuro 7 February 2023, 10 (3) ENEURO.0203-22.2023; DOI: https://doi.org/10.1523/ENEURO.0203-22.2023
Martín Esparza-Iaizzo
1Center for Brain and Cognition, Universitat Pompeu Fabra, Barcelona, Spain 08005
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Irene Vigué-Guix
1Center for Brain and Cognition, Universitat Pompeu Fabra, Barcelona, Spain 08005
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Manuela Ruzzoli
2Basque Center on Cognition Brain and Language (BCBL), Donostia–San Sebastián, Spain 20009
3Ikerbasque, Basque Foundation for Science, Bilbao, Spain 20009
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Mireia Torralba-Cuello
1Center for Brain and Cognition, Universitat Pompeu Fabra, Barcelona, Spain 08005
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Salvador Soto-Faraco
1Center for Brain and Cognition, Universitat Pompeu Fabra, Barcelona, Spain 08005
4Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain 20009
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Article Figures & Data

Figures

  • Extended Data
  • Figure 1.
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    Figure 1.

    Experimental design and response rates. A, Schematic trial representation. A black fixation cross in the middle of the screen and two squares (to-be-attended locations) at the bottom left, and bottom right positions were displayed continuously. At the beginning of each trial, participants were instructed to gaze at the fixation cross. After 200 ms (fixation period), an auditory cue appeared for 100 ms (cue period) indicating which hemifields participants must attend (75% validity). After a jittered interstimulus interval of 2000 ± 500 ms, a target appeared at the targeted location during 50 ms (target period). Participants had to report first if they had seen the target (detection task), and after 1000 ms, the location of the target (left/right discrimination task) during 1500 ms. An intertrial interval (ITI) of 1000 ms followed, and a new trial began (adapted from Torralba et al., 2016). B, Response rates for detected and discriminated trials (HITS) related to attended and unattended trials. Black lines over violin plots represent the mean value. Both overall performance (top) and right/left hemifields (bottom) are shown. White dots indicate individual values (adapted from Torralba et al., 2016).

  • Figure 2.
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    Figure 2.

    Target-locked results. A, Target-locked results of the phase-coupling for attended left (light blue) and attended right (dark blue) in fronto-medial to parietal left (FM-PL) and fronto-medial to parietal right (FM-PR) networks. The lower panels depict the cross-trial average time course (± shaded standard error of the mean; SEM) of phase-locking value (PLV) in both conditions (attended left and attended right). Upper panels present the binned violin plots (mean and median) of the pretarget window (−200–0 ms) and the post-target window (200–400 ms); *p < 0.05. B, Target-locked results collapsed as either ipsilateral (FM-PL network and attended left; FM-PR and attended right) or contralateral (FM-PR network and attended left; FM-PL and attended right). The lower panel shows the cross-trial average time course (± shaded SEM) of PLV in ipsilateral (light gray) and contralateral (dark gray) conditions. The upper panel exhibits the distribution of individual PLV with a violin plot, superimposed by the mean and the contralateral to ipsilateral differences between individual PLV; *p < 0.05. Individual results with PLV are found in Extended Data Figure 2-1, and those with phase linearity measurement (PLM) are found in Extended Data Figure 2-2.

  • Figure 3.
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    Figure 3.

    Cue-locked results. A, Group-level results of upper-α phase locking value (PLV). Upper panel shows phase coupling for ipsilateral (light gray) and contralateral (dark gray) sides in time-windows of 200 ms from the cue-locked interval (500–1500 ms after cue presentation). Lower panel shows mean and standard error of the mean of the PLV values. Individual results are shown in Extended Data Figure 3-1. B, Exploratory analysis of PLV differences. Group-level temporal evolution of the z-scored difference between contralateral and ipsilateral PLV for each frequency band (2.4–42 Hz with 16 logarithmic steps). Z-score values range from −0.03 to 0.03. Individual results are shown in Extended Data Figure 3-2.

  • Figure 4.
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    Figure 4.

    Classification outcomes. A, Cross-time phase locking value (PLV) reality check. Replication of results from Figure 2 calculating PLV across time points rather than across trials. Individual results are shown in Extended Data Figure 4-1. B, Optimization results of γ and margin parameters of the Gaussian kernel support vector machine. Ten-fold validation accuracies with varying margin values (x-axis) and γ values (y-axis). Inset shows a detailed view of the z-axis. C, Confusion matrix of the classification outcomes for one participant. y-axis represents ground truth labels (attended right or attended left) and x-axis represents the classifier’s outcomes. Percentages represent the fraction of correctly classified trials of each condition (i.e., each row sums to 100%). Under the percentage is the gross number of classified trials. Results with additional classifiers such as shrinkage linear discriminant analysis (sLDA) and Riemannian minimum distance to the mean (RDMD) are shown in Extended Data Figure 4-2.

  • Figure 5.
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    Figure 5.

    Lateralization index reality check. A, Averaged lateralization index for attended left (light blue) and attended right (dark blue; *p < 0.05, **p < 0.01). White dots denote individual scores, and horizontal line indicates the group mean. B, Lateralization index (mean ± standard error of the mean; SEM) over time. Solid lines and shaded areas represent mean and SEM interval, respectively. Dots on in the x-axis denote the significant difference over time between attended left (light blue) and attended right (dark blue) via cluster-based permutation test. Individual results are shown in Extended Data Figure 5-1. C, D, Lateralization indexes and the difference of contralateral to ipsilateral phase locking value (PLV) for attended left (light blue) and attended right (dark blue) at the pretarget window (C) and the post-target window (D). At the pretarget the correlations for attended right (r = −0.33, p > 0.05) and attended left (r = −0.19, p > 0.05) did not reach significance and neither did the correlations for attended right (r = −0.38, p > 0.05) and attended left (r = −0.46, p > 0.05) at the post-target window. Crosses denote participants with a significant effect in PLV contra-ipsi differences at the pretarget window (−200–0 ms; participant P05) and the post-target window (200–400 ms; P02 and P07). Dots represent the rest of the participants.

Extended Data

  • Figures
  • Extended Data Figure 2-1

    Individual results of target-locked PLV index. Violin plots represent the phase locking values (PLVs) averaged over the pretarget (−200–0 ms, t = 0 as target appearance) and post-target time window (200–400 ms). Ipsilateral (FM-PL network and attended left; FM-PR and attended right) or contralateral (FM-PR network and attended left; FM-PL and attended right) scenarios are exhibited as either light grey or dark grey, respectively. *p < 0.05, **p < 0.01, ***p < 0.001. Download Figure 2-1, EPS file.

  • Extended Data Figure 2-2

    Individual results of target-locked PLM index. Violin plots represent the phase linearity measurement (PLM) over the pretarget (−200–0 ms, t = 0 as target appearance) and post-target time window (200–400 ms). Ipsilateral (FM-PL network and attended left; FM-PR and attended right) or contralateral (FM-PR network and attended left; FM-PL and attended right) scenarios are exhibited as either light grey or dark grey, respectively. *p < 0.05, **p < 0.01, ***p < 0.001. Download Figure 2-2, EPS file.

  • Extended Data Figure 3-1

    Individual results of upper-α cue-locked PLV analysis. Violin plots represent the phase locking values (PLV) averaged over the five time windows (500–700, 700–900, 1100–1300, and 1300–1500 ms; t = 0 as cue appearance). Ipsilateral or contralateral scenarios are exhibited as either light grey or dark grey, respectively. *p < 0.05, **p < 0.01. Download Figure 3-1, EPS file.

  • Extended Data Figure 3-2

    Individual results of cue-locked exploratory PLV analysis. Differences of contralateral to ipsilateral PLV are represented over frequencies (2.4–42 Hz in 16 logarithmic steps) as a percentage of change regarding the cross-frequency mean of each individual. Download Figure 3-2, EPS file.

  • Extended Data Figure 4-1

    Individual results of target-locked cross-time PLV. Violin plots represent the phase locking values (PLV) obtained by calculating PLV as consistency throughout the pretarget (−200–0 ms) and post-target (200–400 ms) time windows. Ipsilateral or contralateral scenarios are exhibited as either light grey or dark grey, respectively. Download Figure 4-1, EPS file.

  • Extended Data Figure 4-2

    Additional classifier analysis. A, Shrinkage linear discriminant analysis. The leftmost panel reveals how classification error is not modulated by gamma parameter of number of predictors. The rightmost panel presents the confusion matrix. B, Riemannian minimum distance to the mean classification results. Download Figure 4-2, EPS file.

  • Extended Data Figure 5-1

    Individual results of lateralization index. Violin plots represent the averaged lateralized index for attended left (light blue) and attended right trials (dark blue) over the cue-locked time window. Shaded plots represent lateralization over time (mean ± SEM). Dots on in the x-axis denote the significant differences over time between attended left and attended right via cluster-based permutation test. *p < 0.05, **p < 0.01, ***p < 0.001. Download Figure 5-1, EPS file.

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Long-Range α-Synchronization as Control Signal for BCI: A Feasibility Study
Martín Esparza-Iaizzo, Irene Vigué-Guix, Manuela Ruzzoli, Mireia Torralba-Cuello, Salvador Soto-Faraco
eNeuro 7 February 2023, 10 (3) ENEURO.0203-22.2023; DOI: 10.1523/ENEURO.0203-22.2023

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Long-Range α-Synchronization as Control Signal for BCI: A Feasibility Study
Martín Esparza-Iaizzo, Irene Vigué-Guix, Manuela Ruzzoli, Mireia Torralba-Cuello, Salvador Soto-Faraco
eNeuro 7 February 2023, 10 (3) ENEURO.0203-22.2023; DOI: 10.1523/ENEURO.0203-22.2023
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Keywords

  • Alpha
  • brain-computer interface
  • EEG
  • oscillations
  • phase coupling
  • visuospatial attention

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