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Spontaneous fluctuations in neural responses to heartbeats predict visual detection

Nature Neuroscience volume 17, pages 612–618 (2014)Cite this article

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Abstract

Spontaneous fluctuations of ongoing neural activity substantially affect sensory and cognitive performance. Because bodily signals are constantly relayed up to the neocortex, neural responses to bodily signals are likely to shape ongoing activity. Here, using magnetoencephalography, we show that in humans, neural events locked to heartbeats before stimulus onset predict the detection of a faint visual grating in the posterior right inferior parietal lobule and the ventral anterior cingulate cortex, two regions that have multiple functional correlates and that belong to the same resting-state network. Neither fluctuations in measured bodily parameters nor overall cortical excitability could account for this finding. Neural events locked to heartbeats therefore shape visual conscious experience, potentially by contributing to the neural maps of the organism that might underlie subjectivity. Beyond conscious vision, our results show that neural events locked to a basic physiological input such as heartbeats underlie behaviorally relevant differential activation in multifunctional cortical areas.

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Figure 1: Experimental paradigm and rationale.
Figure 2: Post-decisional heart slowing.
Figure 3: Neural events locked to heartbeats before stimulus onset predicted conscious perception of the stimulus.
Figure 4: Neural sources of the differential response to heartbeats.
Figure 5: Pupil diameter, alpha power and warning-evoked response do not predict detection (n = 17).

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Acknowledgements

This work was supported by Agence Nationale de la Recherche grants ANR-BLAN-12-BSH2-0002-01 to C.T.B., ANR-10-LABX-0087 IEC and ANR-10-IDEX-0001-02 PSL*. We thank E. Koechlin for useful suggestions on the manuscript and C. Gitton for excellent technical support during data acquisition.

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Authors and Affiliations

  1. Cognitive Neuroscience Laboratory, Institut National de la Santé et de la Recherche Médicale (INSERM)–École Normale Supérieure (ENS), Paris, France

    Hyeong-Dong Park, Stéphanie Correia & Catherine Tallon-Baudry

  2. Cenir, Centre National de la Recherche Scientifique (CNRS)–Université Pierre-et-Marie-Curie (UPMC)-INSERM, Paris, France

    Antoine Ducorps

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Contributions

H.-D.P. and C.T.-B. designed the experiment. H.-D.P. and S.C. acquired the data. H.-D.P., A.D. and C.T.-B. analyzed the data. H.-D.P. and C.T.-B. wrote the paper.

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Correspondence to Catherine Tallon-Baudry.

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Integrated supplementary information

Supplementary Figure 1 Mean interbeat interval variability.

Data are presented from the interbeat interval during which the warning signal appeared on the screen until interbeat intervals after response delivery. Interbeat interval variability decreased after stimulus onset (* p<0.05), but did not differ between hits and misses (Greenhouse-Geisser corrected 2-way ANOVA with factors Consciousness and Time, main effect of Time F2.0,32.0=11.7, p=2.10—4; main effect of Consciousness F1,16=0.9, p=0.36; interaction F2.39,38.24=2.0, p=0.13). Error bars represent s.e.m.

Supplementary Figure 2 Neural responses to hearbeats in subjects with fast or slow heart rate.

Mean time course across the cluster in hits and misses, in subjects with (a) short (n=9, mean IBI 730 ms) or (b) long (n=8, mean IBI 886 ms) interbeat intervals (IBI). Neural responses to heartbeats within the cluster significantly differed between hits and misses in both groups (short IBI group, t8=3.76, p=0.006; long IBI group, t7=3.19, p=0.015). Longer IBIs did not delay the effect, indicating that the effect corresponds to a differential response to the preceding heartbeat rather than a preparation of the next heartbeat. Error bars represent s.e.m.

Supplementary Figure 3 T-locked electrocardiogram, grand-average across subjects.

Top, vertical derivation. Bottom, horizontal derivation. We did not find any significant difference between hits and misses.

Supplementary Figure 4 Influence of cardiac artefact correction using independent component analysis (ICA) on prestimulus heartbeat-evoked responses.

(a) Topographical map of the difference between prestimulus heartbeat-evoked responses in hits and misses, grand-averaged across 17 subjects, in the 135—171 ms time window, after ICA correction, on magnetometer signals. The topography of the difference was not affected by ICA correction. (b) T-locked magnetic fields at the sensor indicated in white in A, before (top) and after (bottom) ICA correction. The R and T waves could barely be observed on ICA corrected data, but the significant difference between hits and misses in the 135—171 ms time window (shaded area) was preserved. The overall shift toward more negative values in ICA-corrected data is due to data mean-centering by ICA. (c) Amplitude of the prestimulus heartbeat-evoked response, averaged across the cluster separately in hits and misses, and during a separate resting session with eyes open, after ICA correction. The heart-evoked response in the 135—171 ms cluster significantly differed between hits and misses (paired t-test, t16= 4.81, p=2.10—4). It was larger in hits than during rest (paired t-test, t16=3.46, p=0.003) and smaller in misses than during rest (paired t-test, t16=2.39, p=0.03). Because ICA extracts from MEG data the shape of each participant's heartbeat, this analysis further shows that the effect is not dependent on subject-specific heartbeat morphology. Error bars represent s.e.m.

Supplementary Figure 5 Distribution of respiration phase in hits and misses at stimulus onset.

Each point represents a subject and a condition. No preferential phase emerged (Raighley test for non-uniformity of circular data), neither in hits (p=0.81) nor in misses (p=0.67).

Supplementary Figure 6 Prestimulus peripheral blood pressure in hits and misses.

Blood pressure (arbitrary units) was computed over those heartbeats used to compute the heartbeat-evoked neural activity. (a) Time course of pressure, separately in hits and misses. (b) Difference between systolic and diastolic pressure, separately in hits and misses. No significant difference between hits and misses could be found in systolic, diastolic, nor difference between systolic and diastolic pressure. Error bars represent s.e.m.

Supplementary Figure 7 Peripheral blood pressure throughout a trial.

The difference between systolic and diastolic pressure in arbitrary units was measured on the heartbeat preceding warning onset, preceding stimulus onset, preceding response, as well as the first (R+1) and second (R+2) heartbeats following response. Blood pressure evolved in the course of a trial, but did not differ between hits and misses (Greenhouse-Geisser corrected 2-way ANOVA with factors Consciousness and Time, main effect of Time F2.27,22.71=4,15, p=0.025; main effect of Consciousness F1,10=2.14, p=0.17; interaction F1.85,18.54=1.52, p=0.25; paired t-test between hits and misses before stimulus onset: t10=1.50, p=0.16). Error bars represent standard errors of the mean.

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Park, HD., Correia, S., Ducorps, A. et al. Spontaneous fluctuations in neural responses to heartbeats predict visual detection. Nat Neurosci 17, 612–618 (2014). https://doi.org/10.1038/nn.3671

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