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Featured ArticleResearch Articles, Behavioral/Cognitive

Respiration, Heartbeat, and Conscious Tactile Perception

Martin Grund, Esra Al, Marc Pabst, Alice Dabbagh, Tilman Stephani, Till Nierhaus, Michael Gaebler and Arno Villringer
Journal of Neuroscience 26 January 2022, 42 (4) 643-656; DOI: https://doi.org/10.1523/JNEUROSCI.0592-21.2021
Martin Grund
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig 04103, Germany
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Esra Al
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig 04103, Germany
2MindBrainBody Institute, Berlin School of Mind and Brain, Charité – Universitätsmedizin Berlin and Humboldt-Universität zu Berlin, Berlin 10099, Germany
6DFG Research Training Group 2386 Extrospection, Humboldt-Universität zu Berlin, Berlin 10099, Germany
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Marc Pabst
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig 04103, Germany
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Alice Dabbagh
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig 04103, Germany
3Max Planck Institute for Human Cognitive and Brain Sciences, Pain Perception Group, Leipzig 04103, Germany
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Tilman Stephani
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig 04103, Germany
4International Max Planck Research School NeuroCom, Leipzig 04103, Germany
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Till Nierhaus
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig 04103, Germany
5Neurocomputation and Neuroimaging Unit, Department of Education and Psychology, Freie Universität Berlin, Berlin 14195, Germany
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Michael Gaebler
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig 04103, Germany
2MindBrainBody Institute, Berlin School of Mind and Brain, Charité – Universitätsmedizin Berlin and Humboldt-Universität zu Berlin, Berlin 10099, Germany
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Arno Villringer
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig 04103, Germany
2MindBrainBody Institute, Berlin School of Mind and Brain, Charité – Universitätsmedizin Berlin and Humboldt-Universität zu Berlin, Berlin 10099, Germany
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  • Figure 1.
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    Figure 1.

    Experimental procedure and physiological parameters visualized for one exemplary trial. The tiles represent the participant's visual display and the times given below indicate the presentation duration. The near-threshold electrical finger nerve stimulation was always 0.5 s after the cue onset (salmon-colored fixation cross). Here, only one of four button response mappings is displayed (Y = yes; N = no; U = unconfident; C = confident). In total, 400 near-threshold trials and 200 trials without stimulation (33% catch trials) were presented in randomized order. Exemplary traces of ECG, finger photoplethysmography (PPG), and respiration belt below the trial procedure indicate that stimulus detection was analyzed relative to cardiac and respiratory cycles (0°–360°).

  • Figure 2.
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    Figure 2.

    Distribution of mean angles (stimulus onset relative to cardiac cycle) for (A) correct rejections (green), (B) misses (purple), and (C) hits (red). Each dot indicates the mean angle of one participant. The line around the inner circle shows the density distribution of these mean angles. The direction of the arrow in the center indicates the mean angle across the participants while the arrow length represents the mean resultant length R. The resulting p value of the Rayleigh test of uniformity is noted below.

  • Figure 3.
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    Figure 3.

    Circular distribution within the cardiac cycle of unconfident/confident trials and unconfident/confident misses and hits (A–F), dependent probabilities of unconfident/confident miss/hit at four time intervals after the R-peak (G), and metacognitive efficiency across the cardiac cycle (H). The distributions of mean angles (stimulus onset relative to cardiac cycle) are shown for (A) all unconfident trials (correct rejections, misses, and hits), (B) unconfident misses (red), (C) unconfident hits (red), (D) all confident trials (correct rejections, misses, and hits), (E) confident misses (blue), and (F) confident hits (blue). In A–F, each dot indicates the mean angle of one participant. The line around the inner circle shows the density distribution of these mean angles. The direction of the arrow in the center indicates the mean angle across the participants while the arrow length represents the mean resultant length R. The resulting p value of the Rayleigh test of uniformity is noted below and written in bold if significant. G, Mean dependent probabilities for the four possible outcomes of near-threshold trials given a time interval since the previous R-peak. The numbers for one time interval do not add up exactly to 100% across confident/unconfident misses and hits because of rounding and showing the mean across participants. The asterisks between the bars for confident hits indicate significant t tests. (FDR-corrected p < 0.01).

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    Figure 4.

    Response-specific metacognitive efficiency (M-ratios) across the cardiac cycle. At four cardiac intervals after the R-peak (A, C, E, G), the posterior distributions of group-level M-ratios are shown for no (pink; correct rejection vs miss) and yes-responses (green; hit vs false alarm). On top of these histograms of MCMC samples, boxplots represent the participant-level M-ratios for yes/no-responses. M-ratios of 1 indicate that confidence ratings can perfectly discriminate between correct and incorrect responses. M-ratios below 1 indicate inefficient metacognition. The second column shows the difference between the posterior distributions (in log units) of yes/no-responses as the 95% HDIs at the four cardiac cycle intervals (B, D, F, H). The last row shows the 95% HDIs (in log units) between subsequent cardiac intervals (bini+1 – bini) for yes/no-responses (I, J). These 95% HDIs indicate a credible difference between the corresponding group-level M-ratios if zero (red vertical line) is not included (D, H).

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    Figure 5.

    IBIs before and after the stimulus onset for (A) correct rejections (green), misses (purple), and hits (orange), and for (B) confident (blue) and unconfident (red) decisions. Confidence bands reflect within-participant 95% confidence intervals. The label Stimulus on the y-axis indicates the cardiac cycle when the stimulation or cue only were present. The labels S – 1 and S + 1 indicate the preceding and following intervals, respectively. In A, the two asterisks at S + 1 indicate significant t tests between hits and misses (FDR-corrected p = 0.024), and between hits and correct rejections (FDR-corrected p = 0.017). The one asterisk at S + 2 in A indicates a significant t test between hits and correct rejections (FDR-corrected p = 0.014). In B, the asterisks at S + 1 and S + 2 indicate significant t tests between confident and unconfident decisions (S + 1: FDR-corrected p < 0.005; S + 2: FDR-corrected p = 6 × 10-7). The lines with asterisks on the bottom indicate significant t tests for subsequent IBIs within all conditions (FDR-corrected p < 0.05). In C, D, the ratio of IBIs at S + 1 and S + 2 relative to Stimulus are shown for unconfident/confident misses and hits. The boxplots indicate the median (centered line), the 25th/75th percentiles (box), 1.5 times the interquartile range or the maximum value if smaller (whiskers), and outliers (dots beyond the whisker range). The asterisks between the boxplots indicate significant t tests (FDR-corrected p < 0.05).

  • Figure 6.
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    Figure 6.

    Pulse wave and detection relative to cardiac cycle. A, Mean pulse waves measured at the left middle finger across all participants (red thick line) and for each participant (colored thin lines) locked to preceding R-peak. B, First derivative of the mean pulse waves indicating the onset of the arriving pulse wave in the finger. The time window with the lowest detection rate is indicated with vertical thick black lines. C, Detection rate of near-threshold trials in 50-ms stimulus onset intervals since preceding R-peak. The black dots indicate the mean across participants. The blue line is the locally smoothed loess curve with a 95% confidence interval (gray) across these means.

  • Figure 7.
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    Figure 7.

    Circular distribution of mean stimulus onsets relative to the respiratory cycle for (A) correct rejections (green), (B) misses (purple), and (C) hits (red). Zero degree corresponds to expiration onset. Each dot indicates the mean angle of one participant. The gray lines originating in the center of the inner circle represent the resultant lengths Ri for each participant's mean angle. A longer line indicates a less dispersed intraindividual distribution (Vi = 1 – Ri). The direction of the arrow in the center indicates the mean angle across the participants while the arrow length represents the mean resultant length R. The line around the inner circle shows the density distribution of these mean angles. The resulting p value of the Rayleigh test of uniformity is noted below. D, Histogram of respiration phases. Cumulative number of trials across all trials and participants for the relative position of the stimulus onset within the respiratory cycle binned in 20° intervals from 0° to 360°. The Rayleigh test across all trials and participants was significant (R = 0.18, p = 2 × 10−291). E, Detection rates for each quadrant of the respiratory cycle. Lines with p values above the boxplots indicate significant FDR-corrected t tests of all possible combinations. F, IBI differences for each eighth of the respiratory cycle relative to the first eighth (0°–45°). The boxplots (E, F) indicate the median (centered line), the 25th/75th percentiles (box), 1.5 times the interquartile range or the maximum value if smaller (whiskers), and outliers (dots beyond the whisker range).

  • Figure 8.
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    Figure 8.

    Mean respiratory cycle duration in seconds for correct rejections (green), misses (purple), and hits (red). The boxplots indicate the median (centered line), the 25th/75th percentiles (box), 1.5 times the interquartile range or the maximum value if smaller (whiskers), and outliers (dots beyond the whisker range). Significant post hoc t tests are indicated above the boxplot with a black bar and the respective FDR-corrected p value.

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The Journal of Neuroscience: 42 (4)
Journal of Neuroscience
Vol. 42, Issue 4
26 Jan 2022
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Respiration, Heartbeat, and Conscious Tactile Perception
Martin Grund, Esra Al, Marc Pabst, Alice Dabbagh, Tilman Stephani, Till Nierhaus, Michael Gaebler, Arno Villringer
Journal of Neuroscience 26 January 2022, 42 (4) 643-656; DOI: 10.1523/JNEUROSCI.0592-21.2021

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Respiration, Heartbeat, and Conscious Tactile Perception
Martin Grund, Esra Al, Marc Pabst, Alice Dabbagh, Tilman Stephani, Till Nierhaus, Michael Gaebler, Arno Villringer
Journal of Neuroscience 26 January 2022, 42 (4) 643-656; DOI: 10.1523/JNEUROSCI.0592-21.2021
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Keywords

  • cardiac cycle
  • electrocardiogram
  • interoception
  • photoplethysmography
  • respiration
  • tactile perception

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