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Research ArticleResearch Article: New Research, Sensory and Motor Systems

Attention Cueing in Rivalry: Insights from Pupillometry

Miriam Acquafredda, Paola Binda and Claudia Lunghi
eNeuro 6 June 2022, 9 (3) ENEURO.0497-21.2022; https://doi.org/10.1523/ENEURO.0497-21.2022
Miriam Acquafredda
1Department of Neuroscience, Psychology, Pharmacology and Child Health, University of Florence, Florence 50135, Italy
2Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa 56126, Italy
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Paola Binda
2Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa 56126, Italy
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Claudia Lunghi
3Laboratoire des Systèmes Perceptifs, Département d’Études Cognitives, École Normale Supérieure, Paris Sciences et Lettres University, Centre National de la Recherche Scientifique, Paris 75005, France
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Article Figures & Data

Figures

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  • Extended Data
  • Figure 1.
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    Figure 1.

    Dichoptic stimulation and rivalry dynamics. A, Schematics of the stimuli (white or black patches overlayed with orthogonal thin lines), presented dichoptically through a four-mirror stereoscope. B, Schematic representation of the possible stimulus configurations (thin lines omitted) and perceptual outcomes for binocular rivalry (BINriv) and interocular grouping rivalry (IOGriv). C, Example traces from a segment of the experiment, where participants used keypresses to report the dominant percept (square wave) and we recorded pupil size modulations (blue wave). D, Probability density function of the normalized phase durations for exclusive dominance of white or black disk percepts in binocular rivalry and interocular grouping rivalry.

  • Figure 2.
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    Figure 2.

    Pupil modulations track perceptual alternations. Baseline subtracted pupil size traces aligned to perceptual switches toward exclusive dominance of a white disk or a black disk percept and averaged across phases, separately for binocular rivalry (A) and interocular grouping rivalry (B). In all panels, shadings report mean ± 1 SE across participants and the blue marks on the x-axis highlight time points where pairwise comparisons between traces are significant (one tailed t test, p < 0.05 FDR corrected). Observations regarding the latency of the pupillary response and its relative magnitude are reported in Extended Data Figure 2-1, where nonbaseline subtracted traces are shown.

  • Figure 3.
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    Figure 3.

    Attention cueing affect perceptual alternations but not pupil modulations. A, B, Perceptual dominance for exclusive white or black disk percepts, without attentional cueing (dashed lines) or when the white or the black disk percept were cued (continuous lines, cueing condition indicated on the abscissa). Error bars report ±1 SE across participants. C, D, Baseline corrected average pupil size computed in a fixed temporal window (between –0.5 and 1 s from the perceptual transition) during phases of exclusive dominance of the black (black line) and the white disk (red line). Results from the no-cueing condition are reported by dashed lines. Continuous lines report the results from the trials where the white or the black percepts were cued (separated on the abscissa). Error bars report ±1 SE across participants. E, F, Individual participants’ attentional modulation indices for perceptual dominance (x-axis) and pupil size (y-axis), computed with Equations 3, 4. Dash-dot blue lines mark the x = 0 and y = 0 lines, indicating no effect of attention cueing. Each circle reports results from one participant; red dots highlight participants with a significant attentional modulation index for perceptual dominance. Red lines show the best fitting line and its 95% confidence intervals. In all panels, the left column reports results for binocular rivalry and the right for interocular grouping rivalry.

  • Figure 4.
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    Figure 4.

    Pupil time courses are comparable across cueing conditions. A, B, Pupil size traces aligned to perceptual switches toward exclusive dominance of a white disk or a black disk percept computed across phases in individual participants and then averaged for each cueing condition, separately for binocular rivalry and interocular grouping rivalry. C, D, Time course of the difference between baseline corrected pupil size during black and white percepts, computed in individual participants and then averaged for each cueing condition. The resulting traces show no effect of cueing. The same conclusions can be drawn skipping the baseline correction step or defining pupil baseline over a wider temporal interval around perceptual switch, as shown in Extended Data Figure 4-1. In all panels, shadings report mean ±1 SE across participants.

  • Figure 5.
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    Figure 5.

    Effects of attention cueing versus enhancing contrast. A, B, Perceptual dominance for exclusive white or black disk percepts, in the no cue condition (dashed lines) or when the physical contrast of the white disk was enhanced/cued (continuous lines, contrast, or cueing condition indicated on the abscissa). Error bars report ±1 SE across participants. C, Time course of the difference between baseline corrected pupil size during black and white percepts, computed in individual participants and then averaged for each condition. The blue marks on the x-axis highlight time points where pairwise comparisons between the +100% and the no cue condition traces are significant (p < 0.05 FDR corrected). Shadings report mean ±1 SE across participants.

  • Figure 6.
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    Figure 6.

    A,B, Proportion of mixed percepts in no cueing or cueing conditions (collapsed across white and black cued) for binocular rivalry (BINriv) and interocular grouping rivalry (IOGriv). Error bars report ±1 s.e. across participants. ns: not significant. C,D, Pupil traces during mixed percepts in the three cueing conditions for binocular rivalry (BINriv) and interocular grouping rivalry (IOGriv). Shaded areas show ±1 s.e. across participants and blue marks on the x-axis highlight timepoints where pairwise comparisons between the white and black cueing conditions are significant (p < 0.05 FDR corrected).

Tables

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    Table 1

    The effects of cueing on proportions and pupil size

    ProportionsPupil size
    Dominant perceptF(1,37) = 146.46*
    p < 0.001
    logBF = 30.54
    ηp2 = 0.80
    F(1,37) = 46.09*
    p < 0.001
    logBF = 22.52
    ηp2 = 0.55
    Rivalry typeF(1,37) = 82.62*
    p < 0.001
    logBF = 25.49
    ηp2 = 0.69
    F(1,37) = 0.12
    p = 0.73
    logBF = −0.90
    ηp2 = 0.003
    Cued perceptF(1,37) = 5.37*
    p = 0.03
    logBF = −0.82
    ηp2 = 0.13
    F(1,37) = 1.91
    p = 0.17
    logBF = −0.78
    ηp2 = 0.05
    Dominant percept × rivalry typeF(1,37) = 0.99
    p = 0.33
    logBF = −0.62
    ηp2 = 0.03
    F(1,37) = 0.17
    p = 0.68
    logBF = −0.72
    ηp2 = 0.005
    Dominant percept × cued perceptF(1,37) = 32.96*
    p < 0.001
    logBF = 11.33
    ηp2 = 0.47
    F(1,37) = 1.78
    p = 0.19
    logBF = −0.53
    ηp2 = 0.05
    Rivalry type × cued perceptF(1,37) = 0.08
    p = 0.77
    logBF = −0.78
    ηp2 = 0.002
    F(1,37) = 1.92
    p = 0.17
    logBF = −0.54
    ηp2 = 0.05
    Dominant percept × rivalry type × cued perceptF(1,37) = 5.45*
    p = 0.02
    logBF = −0.11
    ηp2 = 0.13
    F(1,37) = 0.03
    p = 0.85
    logBF = −0.41
    ηp2 < 0.001
    • Three-way ANOVA for attention cueing results, with factors: dominant percept (white/black disk), cueing (white/black cued), rivalry type (binocular/interocular grouping rivalry). These results were not affected by shifting the baseline or skipping this step (Extended Data Table 1-1). * for p < 0.05 or lower.

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    Table 2

    Contrast enhancement effects

    ProportionsPupil size
    Dominant perceptF(1,9) = 4.47
    p = 0.06
    logBF = 0.19
    F(1,9) = 18.40*
    p = 0.002
    logBF = 13.99
    Contrast incrementF(4,9) = 4.23*
    p = 0.007
    logBF = −0.44
    F(4,9) = 1.16
    p = 0.34
    logBF = −1.30
    Dominant percept × contrast incrementF(4,9) = 39.75*
    p < 0.001
    logBF = 12.36
    F(4,9) = 14.11*
    p < 0.001
    logBF = 3.38
    • Two-way ANOVA for contrast enhancement results, with factors: dominant percept (white/black disk) and contrast increment (0%, 25%, 50%, 100%, 150%). Greenhouse–Geisser corrected values. * for p < 0.05 or lower.

    • View popup
    Table 3

    The effects of cueing on proportions and pupil size in the control experiment

    ProportionsPupil size
    Modulation index: no cue vs. cueingt(9) = 5.66*
    p < 0.001
    logBF = 2.04
    t(9) = 0.66
    p = 0.52
    logBF = −0.43
    25% contrast increment
    vs cueing
    t(9) = 5.46*
    p < 0.001
    logBF = 1.95
    t(9) = 0.41
    p = 0.69
    logBF = −0.48
    50% contrast increment
     vs cueing
    t(9) = 2.43*
    p = 0.04
    logBF = 0.33
    t(9) = 0.52
    p = 0.61
    logBF = −0.45
    100% contrast increment
     vs cueing
    t(9) = 0.77
    p = 0.46
    logBF = −0.40
    t(9) = 3.29*
    p = 0.01
    logBF = 0.81
    150% contrast increment
     vs cueing
    t(9) = 3.83*
    p = 0.004
    logBF = 1.11
    t(9) = 4.73*
    p = 0.001
    logBF = 1.58
    • Modulation indices from the control experiment: comparison of attention cueing versus no cue (first row) and attention cueing versus contrast enhancement by 25%, 50%, 100%, and 150%. * for p < 0.05 or lower.

Extended Data

  • Figures
  • Tables
  • Extended Data Figure 2-1

    Pupil size modulations in rivalry and simulation conditions. Time course of the difference between pupil size during black and white percepts, computed in individual participants, and then averaged for binocular rivalry (dark blue curve), interocular grouping rivalry (light blue curve) and simulation (green curve). In all panels, shadings report mean ±1 SE across participants and the blue marks on the x-axis highlight time points where each trace is significantly different from 0 (one tailed t test, p < 0.05 FDR corrected). Pupil modulations during binocular and interocular grouping rivalry averaged, respectively, 39.14 ± 8.15% (mean ± 1 SE across participants) and 43.80 ± 10.26% of the pupil size modulations observed during simulated rivalry, as previously reported by Binda and colleagues (Binda et al.,2013) in a different spatial-attention task. Moreover, they consistently started before the perceptual switch, and this was more pronounced in the rivalry conditions than in the simulated rivalry (significant pupil difference started 160 ms before the switch in binocular and 320 ms in interocular grouping rivalry, compared with almost no latency for simulated rivalry). This finding, in line with Fahle et al. (2011) and Naber et al. (2011), may reflect the graded nature of rivalry transitions, which may delay change detection in rivalry compared with the sharp transitions used in the simulated rivalry condition. Download Figure 2-1, TIF file.

  • Extended Data Figure 4-1

    Pupil modulations track perceptual alternations comparably across cueing conditions irrespectively of whether and how pupil traces are baseline corrected. Pupil size traces aligned to perceptual switches towards exclusive dominance of a white disk or a black disk percept and averaged across phases, separately for binocular rivalry (A) and interocular grouping rivalry (B) and separately for the two cueing conditions: cueing the white percept (dashed lines) or the black percept (continuous lines). Shading report ±1 SE across participants. These traces are computed without subtracting any baseline correction (A, B) and after subtracting a baseline computed as average pupil size in the [–5:5] s interval around perceptual switch (C, D). Note how the resulting traces are virtually indistinguishable: in both cases pupil size still allows to discriminate white and black percepts (red and black curves are clearly separated) but shows no effect of cueing (dashed and continuous lines are virtually superimposed, together with the blue traces). Coherently, we found that cueing did not affect preswitch pupil baseline used for the main figures, which was computed in the [–1:–0.5] s interval from the perceptual switch (main effect of cued percept: F(1,37) = 1.51, p = 0.23, logBF = –0.60; dominant percept × cued percept interaction: F(1,37) = 0.14, p = 0.71, logBF = –0.74). Download Figure 4-1, TIF file.

  • Extended Data Table 1-1

    Three-way ANOVA for attention cueing results. Three-way ANOVA for attention cueing results, with factors: dominant percept (white/black disk), cueing (white/black cued), rivalry type (binocular/interocular grouping rivalry). We confirmed our results on cueing with a three-way ANOVA entered with the average pupil size in the interval [–0.5:1] s (the same interval used for Table 1 in the main text) but now skipping the baseline correction step (first column) or subtracting a baseline computed as the average pupil size in the [–5:5] s interval around perceptual switch (second column). In both cases, we confirm the main effect of dominant percept type and the absence of any reliable effect of attention cueing, suggesting that our results are not limited to the specific window we used to compute the baseline pupil size.

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Attention Cueing in Rivalry: Insights from Pupillometry
Miriam Acquafredda, Paola Binda, Claudia Lunghi
eNeuro 6 June 2022, 9 (3) ENEURO.0497-21.2022; DOI: 10.1523/ENEURO.0497-21.2022

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Attention Cueing in Rivalry: Insights from Pupillometry
Miriam Acquafredda, Paola Binda, Claudia Lunghi
eNeuro 6 June 2022, 9 (3) ENEURO.0497-21.2022; DOI: 10.1523/ENEURO.0497-21.2022
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Keywords

  • attention
  • binocular rivalry
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  • pupillary light response
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