CoChat
Sign Up
Cited by 276Heart Rate Variability and Autonomic ControlTactile and Sensory InteractionsPsychosomatic Disorders and Their Treatments

Heart–brain interactions shape somatosensory perception and evoked potentials

Open access
Al, Esra, Iliopoulos, Fivos, Forschack, Norman, Nierhaus, Till, Grund, Martin, Motyka, Paweł, Gaebler, Michael, Nikulin, Vadim V. +1 more·2020·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.1915629117PMC PMC7229654

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

Significance: Our brain continuously receives signals from the body and the environment. Although we are mostly unaware of internal bodily processes, such as our heartbeats, they can affect our perception. Here, we show two distinct ways in which the heartbeat modulates conscious perception. First, increased heartbeat-evoked neural activity before stimulation is followed by decreased somatosensory detection. This effect can be explained by subjects adopting a more conservative decision criterion, which is accompanied by changes in early and late somatosensory-evoked responses. Second, stimulus timing during the cardiac cycle affects sensitivity but not criterion for somatosensory stimuli, which is reflected only in late somatosensory-evoked responses. We propose that these heartbeat-related modulations are connected to fluctuations of interoceptive attention and (unconscious) predictive coding mechanisms.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1073/pnas.1915629117

Cites

18 of 18 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • In the somatosensory domain, findings are mostly congruent with the pulsed inhibition hypothesis.

    “In the somatosensory domain, findings are mostly congruent with the pulsed inhibition hypothesis 35,36,58,59 ;”

    From Interoceptive rhythms in the brain (2023) · cites this paper as [58]

  • HERs predict the likelihood of the conscious detection of a visual or somatosensory stimulus at threshold, covary with subjective pain perception, and reliably index residual consciousness in postcomatose patients.

    “HERs could index the subject of conscious experience, since they predict the likelihood of the conscious detection of a visual 33 or somatosensory 58 stimulus at threshold, covary with subjective pain perception 112 , and reliably index residual consciousness in postcomatose patients 113 .”

    From Interoceptive rhythms in the brain (2023) · cites this paper as [58]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 55

  1. [1]Arieli A., Sterkin A., Grinvald A., Aertsen A., Dynamics of ongoing activity: Explanation of the large variability in evoked cortical responses. Science 273, 1868– 1871 (1996). 8791593
  2. [2]van Dijk H., Schoffelen J.-M., Oostenveld R., Jensen O., Prestimulus oscillatory activity in the alpha band predicts visual discrimination ability. J. Neurosci. 28, 1816– 1823 (2008). 18287498 PMC6671447
  3. [3]Blankenburg F., Imperceptible stimuli and sensory processing impediment. Science 299, 1864 (2003). 12649475
  4. [4]Weisz N., Prestimulus oscillatory power and connectivity patterns predispose conscious somatosensory perception. Proc. Natl. Acad. Sci. U.S.A. 111, E417– E425 (2014). 24474792 PMC3910583
  5. [6]Saxon S. A., Detection of near threshold signals during four phases of cardiac cycle. Ala. J. Med. Sci. 7, 427– 430 (1970). 5532273
  6. [7]Sandman C. A., McCanne T. R., Kaiser D. N., Diamond B., Heart rate and cardiac phase influences on visual perception. J. Comp. Physiol. Psychol. 91, 189– 202 (1977). 838914
  7. [8]Elliott R., Graf V., Visual sensitivity as a function of phase of cardiac cycle. Psychophysiology 9, 357– 361 (1972). 5034123
  8. [9]Delfini L. F., Campos J. J., Signal detection and the “cardiac arousal cycle”. Psychophysiology 9, 484– 491 (1972). 5075578
  9. [10]Motyka P., Interactions between cardiac activity and conscious somatosensory perception. Psychophysiology 56, e13424 (2019). 31245848
  10. [11]Edwards L., Ring C., McIntyre D., Winer J. B., Martin U., Sensory detection thresholds are modulated across the cardiac cycle: Evidence that cutaneous sensibility is greatest for systolic stimulation. Psychophysiology 46, 252– 256 (2009). 19207192
  11. [12]Walker B. B., Sandman C. A., Visual evoked potentials change as heart rate and carotid pressure change. Psychophysiology 19, 520– 527 (1982). 7134357
  12. [13]Sandman C. A., Augmentation of the auditory event related potentials of the brain during diastole. Int. J. Psychophysiol. 2, 111– 119 (1984). 6542913
  13. [14]Park H.-D., Correia S., Ducorps A., Tallon-Baudry C., Spontaneous fluctuations in neural responses to heartbeats predict visual detection. Nat. Neurosci. 17, 612– 618 (2014). 24609466
  14. [15]Kern M., Aertsen A., Schulze-Bonhage A., Ball T., Heart cycle-related effects on event-related potentials, spectral power changes, and connectivity patterns in the human ECoG. Neuroimage 81, 178– 190 (2013). 23684883
  15. [16]Montoya P., Schandry R., Müller A., Heartbeat evoked potentials (HEP): Topography and influence of cardiac awareness and focus of attention. Electroencephalogr. Clin. Neurophysiol. 88, 163– 172 (1993). 7684965
  16. [17]Pollatos O., Schandry R., Accuracy of heartbeat perception is reflected in the amplitude of the heartbeat-evoked brain potential. Psychophysiology 41, 476– 482 (2004). 15102134
  17. [18]Green D. M., Swets J. A., Signal Detection Theory and Psychophysics (Wiley, 1966).
  18. [19]Pewsey A., Neuhäuser M., Ruxton G., Circular Statistics in R (Oxford University Press, 2013).
  19. [20]Auksztulewicz R., Blankenburg F., Subjective rating of weak tactile stimuli is parametrically encoded in event-related potentials. J. Neurosci. 33, 11878– 11887 (2013). 23864677 PMC6794058
  20. [22]Hirvonen J., Palva S., Cortical localization of phase and amplitude dynamics predicting access to somatosensory awareness. Hum. Brain Mapp. 37, 311– 326 (2016). 26485310 PMC6867440
  21. [23]Schandry R., Sparrer B., Weitkunat R., From the heart to the brain: A study of heartbeat contingent scalp potentials. Int. J. Neurosci. 30, 261– 275 (1986). 3793380
  22. [24]Schandry R., Weitkunat R., Enhancement of heartbeat-related brain potentials through cardiac awareness training. Int. J. Neurosci. 53, 243– 253 (1990). 2265945
  23. [25]Kriegeskorte N., Simmons W. K., Bellgowan P. S. F., Baker C. I., Circular analysis in systems neuroscience: The dangers of double dipping. Nat. Neurosci. 12, 535– 540 (2009). 19396166 PMC2841687
  24. [26]Iemi L., Chaumon M., Crouzet S. M., Busch N. A., Spontaneous neural oscillations bias perception by modulating baseline excitability. J. Neurosci. 37, 807– 819 (2017). 28123017 PMC6597018
  25. [27]Forschack N., Nierhaus T., Müller M. M., Villringer A., Alpha-band brain oscillations shape the processing of perceptible as well as imperceptible somatosensory stimuli during selective attention. J. Neurosci. 37, 6983– 6994 (2017). 28630252 PMC6705724
  26. [28]Schubert R., Haufe S., Blankenburg F., Villringer A., Curio G., Now you’ll feel it, now you won’t: EEG rhythms predict the effectiveness of perceptual masking. J. Cogn. Neurosci. 21, 2407– 2419 (2009). 19199408
  27. [29]Haegens S., Nácher V., Luna R., Romo R., Jensen O., α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking. Proc. Natl. Acad. Sci. U.S.A. 108, 19377– 19382 (2011). 22084106 PMC3228466
  28. [30]Gray M. A., Minati L., Paoletti G., Critchley H. D., Baroreceptor activation attenuates attentional effects on pain-evoked potentials. Pain 151, 853– 861 (2010). 20965656 PMC3038268
  29. [31]Barrett L. F., Simmons W. K., Interoceptive predictions in the brain. Nat. Rev. Neurosci. 16, 419– 429 (2015). 26016744 PMC4731102
  30. [33]Macefield V. G., Cardiovascular and respiratory modulation of tactile afferents in the human finger pad. Exp. Physiol. 88, 617– 625 (2003). 12955162
  31. [34]van Velzen M. H. N., Loeve A. J., Niehof S. P., Mik E. G., Increasing accuracy of pulse transit time measurements by automated elimination of distorted photoplethysmography waves. Med. Biol. Eng. Comput. 55, 1989– 2000 (2017). 28361357 PMC5644691
  32. [35]Allen M., Levy A., Parr T., Friston K. J., In the body’s eye: The computational anatomy of interoceptive inference. bioRxiv:10.1101/603928 (10 April 2019). PMC9506608 36099315 · DOI
  33. [37]Friston K., A theory of cortical responses. Philos. Trans. R. Soc. B 360, 815– 836 (2005). PMC1569488 15937014
  34. [38]Dehaene S., Sergent C., Changeux J.-P., A neuronal network model linking subjective reports and objective physiological data during conscious perception. Proc. Natl. Acad. Sci. U.S.A. 100, 8520– 8525 (2003). 12829797 PMC166261
  35. [39]Auksztulewicz R., Spitzer B., Blankenburg F., Recurrent neural processing and somatosensory awareness. J. Neurosci. 32, 799– 805 (2012). 22262878 PMC6621140
  36. [41]van Vugt B., The threshold for conscious report: Signal loss and response bias in visual and frontal cortex. Science 360, 537– 542 (2018). 29567809
  37. [42]Schandry R., Montoya P., Event-related brain potentials and the processing of cardiac activity. Biol. Psychol. 42, 75– 85 (1996). 8770371
  38. [43]Gray M. A., A cortical potential reflecting cardiac function. Proc. Natl. Acad. Sci. U.S.A. 104, 6818– 6823 (2007). 17420478 PMC1871868
  39. [45]Schubert R., Spatial attention related SEP amplitude modulations covary with BOLD signal in S1–A simultaneous EEG–fMRI study. Cereb. Cortex 18, 2686– 2700 (2008). 18372293
  40. [47]García-Cordero I., Attention, in and out: Scalp-level and intracranial EEG correlates of interoception and exteroception. Front. Neurosci. 11, 411 (2017). 28769749 PMC5515904
  41. [49]Dehaene S., Changeux J.-P., Ongoing spontaneous activity controls access to consciousness: A neuronal model for inattentional blindness. PLoS Biol. 3, e141 (2005). 15819609 PMC1074751
  42. [50]Khalsa S. S., Rudrauf D., Feinstein J. S., Tranel D., The pathways of interoceptive awareness. Nat. Neurosci. 12, 1494– 1496 (2009). 19881506 PMC2787640
  43. [52]Pollatos O., Kirsch W., Schandry R., Brain structures involved in interoceptive awareness and cardioafferent signal processing: A dipole source localization study. Hum. Brain Mapp. 26, 54– 64 (2005). 15852466 PMC6871699
  44. [53]Jones S. R., Cued spatial attention drives functionally relevant modulation of the mu rhythm in primary somatosensory cortex. J. Neurosci. 30, 13760– 13765 (2010). 20943916 PMC2970512
  45. [54]Craddock M., Poliakoff E., El-Deredy W., Klepousniotou E., Lloyd D. M., Pre-stimulus alpha oscillations over somatosensory cortex predict tactile misperceptions. Neuropsychologia 96, 9– 18 (2017). 28041948
  46. [56]Rau H., Elbert T., Psychophysiology of arterial baroreceptors and the etiology of hypertension. Biol. Psychol. 57, 179– 201 (2001). 11454439
  47. [57]Park H.-D., Blanke O., Heartbeat-evoked cortical responses: Underlying mechanisms, functional roles, and methodological considerations. Neuroimage 197, 502– 511 (2019). 31051293
  48. [58]Taskin B., Holtze S., Krause T., Villringer A., Inhibitory impact of subliminal electrical finger stimulation on SI representation and perceptual sensitivity of an adjacent finger. Neuroimage 39, 1307– 1313 (2008). 18024161
  49. [59]Ehrenstein W. H., Ehrenstein A., Psychophysical Methods (Springer, 1999).
  50. [63]Vázquez-Seisdedos C. R., Neto J. E., Marañón Reyes E. J., Klautau A., Limão de Oliveira R. C., New approach for T-wave end detection on electrocardiogram: Performance in noisy conditions. Biomed. Eng. Online 10, 77 (2011). 21906317 PMC3201026
  51. [64]Delorme A., Makeig S., EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134, 9– 21 (2004). 15102499
  52. [65]Oostenveld R., Fries P., Maris E., Schoffelen J.-M., FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci. 2011, 156869 (2011). 21253357 PMC3021840
  53. [67]Zhang Y., Ding M., Detection of a weak somatosensory stimulus: Role of the prestimulus mu rhythm and its top-down modulation. J. Cogn. Neurosci. 22, 307– 322 (2010). 19400673
  54. [68]Nierhaus T., Imperceptible somatosensory stimulation alters sensorimotor background rhythm and connectivity. J. Neurosci. 35, 5917– 5925 (2015). 25878264 PMC6605170
  55. [69]Macmillan N., Creelman D., Detection Theory: A User’s Guide (Psychology Press, 2004).

Cited by

Sorted by citations

Authors
Al, E., Iliopoulos, F., Forschack, N., Nierhaus, T., Grund, M., Motyka, P., Gaebler, M., Nikulin, V. V., & Villringer, A.
Affiliations
  • Humboldt-Universität zu Berlin (DE)
  • Max Planck Institute for Human Development (DE)
  • Max Planck Institute for Human Cognitive and Brain Sciences (DE)
  • University of Warsaw (PL)
  • National Research University Higher School of Economics (RU)
Corresponding author
  • Al, Esra
  • Villringer, Arno
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2020-04-27
Volume
117
Issue
19
Pages
10575-10584
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.1915629117
PMC
PMC7229654
OpenAlex
W3018854448
Cited by
276
References
18
Citations by year
2026: 41 · 2025: 55 · 2024: 42 · 2023: 54 · 2022: 47 · 2021: 28 · 2020: 8 · 2018: 1
FWCI
21.19
Type
journal article
Language
en
Update notices
correction (2020-07-20)
Open access
Licence
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
Funders
  • Deutsche Forschungsgemeinschaft (GRK 2386, project 9, MU 972/25-1)
  • Bundesministerium für Forschung und Technologie (13GW0206B)
Topics
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
  • Health Sciences › Medicine › Psychiatry and Mental health › Psychosomatic Disorders and Their Treatments
Keywords
heart-brain interaction, cardiac interoception, heartbeat-evoked potentials, somatosensory perception, somatosensory evoked potentials, cardiac cycle timing, perceptual sensitivity, detection bias, P300, predictive coding, alpha oscillations, conscious perception
MeSH terms
Adult, Attention, Awareness, Brain, Brain Mapping, Consciousness, Electrocardiography, Electroencephalography, Evoked Potentials, Evoked Potentials, Somatosensory, Female, Heart, Heart Rate, Humans, Male, Perception, Somatosensory Cortex, Interoception

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review