Cargando…

Heart–brain interactions shape somatosensory perception and evoked potentials

Even though humans are mostly not aware of their heartbeats, several heartbeat-related effects have been reported to influence conscious perception. It is not clear whether these effects are distinct or related phenomena, or whether they are early sensory effects or late decisional processes. Combin...

Descripción completa

Detalles Bibliográficos
Autores principales: Al, Esra, Iliopoulos, Fivos, Forschack, Norman, Nierhaus, Till, Grund, Martin, Motyka, Paweł, Gaebler, Michael, Nikulin, Vadim V., Villringer, Arno
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7229654/
https://www.ncbi.nlm.nih.gov/pubmed/32341167
http://dx.doi.org/10.1073/pnas.1915629117
_version_ 1783534804500742144
author Al, Esra
Iliopoulos, Fivos
Forschack, Norman
Nierhaus, Till
Grund, Martin
Motyka, Paweł
Gaebler, Michael
Nikulin, Vadim V.
Villringer, Arno
author_facet Al, Esra
Iliopoulos, Fivos
Forschack, Norman
Nierhaus, Till
Grund, Martin
Motyka, Paweł
Gaebler, Michael
Nikulin, Vadim V.
Villringer, Arno
author_sort Al, Esra
collection PubMed
description Even though humans are mostly not aware of their heartbeats, several heartbeat-related effects have been reported to influence conscious perception. It is not clear whether these effects are distinct or related phenomena, or whether they are early sensory effects or late decisional processes. Combining electroencephalography and electrocardiography, along with signal detection theory analyses, we identify two distinct heartbeat-related influences on conscious perception differentially related to early vs. late somatosensory processing. First, an effect on early sensory processing was found for the heartbeat-evoked potential (HEP), a marker of cardiac interoception. The amplitude of the prestimulus HEP negatively correlated with localization and detection of somatosensory stimuli, reflecting a more conservative detection bias (criterion). Importantly, higher HEP amplitudes were followed by decreases in early (P50) as well as late (N140, P300) somatosensory-evoked potential (SEP) amplitudes. Second, stimulus timing along the cardiac cycle also affected perception. During systole, stimuli were detected and correctly localized less frequently, relating to a shift in perceptual sensitivity. This perceptual attenuation was accompanied by the suppression of only late SEP components (P300) and was stronger for individuals with a more stable heart rate. Both heart-related effects were independent of alpha oscillations’ influence on somatosensory processing. We explain cardiac cycle timing effects in a predictive coding account and suggest that HEP-related effects might reflect spontaneous shifts between interoception and exteroception or modulations of general attentional resources. Thus, our results provide a general conceptual framework to explain how internal signals can be integrated into our conscious perception of the world.
format Online
Article
Text
id pubmed-7229654
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-72296542020-05-26 Heart–brain interactions shape somatosensory perception and evoked potentials Al, Esra Iliopoulos, Fivos Forschack, Norman Nierhaus, Till Grund, Martin Motyka, Paweł Gaebler, Michael Nikulin, Vadim V. Villringer, Arno Proc Natl Acad Sci U S A Biological Sciences Even though humans are mostly not aware of their heartbeats, several heartbeat-related effects have been reported to influence conscious perception. It is not clear whether these effects are distinct or related phenomena, or whether they are early sensory effects or late decisional processes. Combining electroencephalography and electrocardiography, along with signal detection theory analyses, we identify two distinct heartbeat-related influences on conscious perception differentially related to early vs. late somatosensory processing. First, an effect on early sensory processing was found for the heartbeat-evoked potential (HEP), a marker of cardiac interoception. The amplitude of the prestimulus HEP negatively correlated with localization and detection of somatosensory stimuli, reflecting a more conservative detection bias (criterion). Importantly, higher HEP amplitudes were followed by decreases in early (P50) as well as late (N140, P300) somatosensory-evoked potential (SEP) amplitudes. Second, stimulus timing along the cardiac cycle also affected perception. During systole, stimuli were detected and correctly localized less frequently, relating to a shift in perceptual sensitivity. This perceptual attenuation was accompanied by the suppression of only late SEP components (P300) and was stronger for individuals with a more stable heart rate. Both heart-related effects were independent of alpha oscillations’ influence on somatosensory processing. We explain cardiac cycle timing effects in a predictive coding account and suggest that HEP-related effects might reflect spontaneous shifts between interoception and exteroception or modulations of general attentional resources. Thus, our results provide a general conceptual framework to explain how internal signals can be integrated into our conscious perception of the world. National Academy of Sciences 2020-05-12 2020-04-27 /pmc/articles/PMC7229654/ /pubmed/32341167 http://dx.doi.org/10.1073/pnas.1915629117 Text en Copyright © 2020 the Author(s). Published by PNAS. http://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Al, Esra
Iliopoulos, Fivos
Forschack, Norman
Nierhaus, Till
Grund, Martin
Motyka, Paweł
Gaebler, Michael
Nikulin, Vadim V.
Villringer, Arno
Heart–brain interactions shape somatosensory perception and evoked potentials
title Heart–brain interactions shape somatosensory perception and evoked potentials
title_full Heart–brain interactions shape somatosensory perception and evoked potentials
title_fullStr Heart–brain interactions shape somatosensory perception and evoked potentials
title_full_unstemmed Heart–brain interactions shape somatosensory perception and evoked potentials
title_short Heart–brain interactions shape somatosensory perception and evoked potentials
title_sort heart–brain interactions shape somatosensory perception and evoked potentials
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7229654/
https://www.ncbi.nlm.nih.gov/pubmed/32341167
http://dx.doi.org/10.1073/pnas.1915629117
work_keys_str_mv AT alesra heartbraininteractionsshapesomatosensoryperceptionandevokedpotentials
AT iliopoulosfivos heartbraininteractionsshapesomatosensoryperceptionandevokedpotentials
AT forschacknorman heartbraininteractionsshapesomatosensoryperceptionandevokedpotentials
AT nierhaustill heartbraininteractionsshapesomatosensoryperceptionandevokedpotentials
AT grundmartin heartbraininteractionsshapesomatosensoryperceptionandevokedpotentials
AT motykapaweł heartbraininteractionsshapesomatosensoryperceptionandevokedpotentials
AT gaeblermichael heartbraininteractionsshapesomatosensoryperceptionandevokedpotentials
AT nikulinvadimv heartbraininteractionsshapesomatosensoryperceptionandevokedpotentials
AT villringerarno heartbraininteractionsshapesomatosensoryperceptionandevokedpotentials