Conscious processing of global and local auditory irregularities causes differentiated heartbeat-evoked responses

Recent research suggests that brain-heart interactions are associated with perceptual and self-consciousness. In this line, the neural responses to visceral inputs have been hypothesized to play a leading role in shaping our subjective experience. This study aims to investigate whether the contextua...

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Main Authors: Diego Candia-Rivera, Federico Raimondo, Pauline Pérez, Lionel Naccache, Catherine Tallon-Baudry, Jacobo D Sitt
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/75352
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author Diego Candia-Rivera
Federico Raimondo
Pauline Pérez
Lionel Naccache
Catherine Tallon-Baudry
Jacobo D Sitt
author_facet Diego Candia-Rivera
Federico Raimondo
Pauline Pérez
Lionel Naccache
Catherine Tallon-Baudry
Jacobo D Sitt
author_sort Diego Candia-Rivera
collection DOAJ
description Recent research suggests that brain-heart interactions are associated with perceptual and self-consciousness. In this line, the neural responses to visceral inputs have been hypothesized to play a leading role in shaping our subjective experience. This study aims to investigate whether the contextual processing of auditory irregularities modulates both direct neuronal responses to the auditory stimuli (ERPs) and the neural responses to heartbeats, as measured with heartbeat-evoked responses (HERs). HERs were computed in patients with disorders of consciousness, diagnosed with a minimally conscious state or unresponsive wakefulness syndrome. We tested whether HERs reflect conscious auditory perception, which can potentially provide additional information for the consciousness diagnosis. EEG recordings were taken during the local-global paradigm, which evaluates the capacity of a patient to detect the appearance of auditory irregularities at local (short-term) and global (long-term) levels. The results show that local and global effects produce distinct ERPs and HERs, which can help distinguish between the minimally conscious state and unresponsive wakefulness syndrome patients. Furthermore, we found that ERP and HER responses were not correlated suggesting that independent neuronal mechanisms are behind them. These findings suggest that HER modulations in response to auditory irregularities, especially local irregularities, may be used as a novel neural marker of consciousness and may aid in the bedside diagnosis of disorders of consciousness with a more cost-effective option than neuroimaging methods.
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spelling doaj.art-1f5def43f02242aba32ad822b3b8a45b2023-11-15T14:47:48ZengeLife Sciences Publications LtdeLife2050-084X2023-10-011210.7554/eLife.75352Conscious processing of global and local auditory irregularities causes differentiated heartbeat-evoked responsesDiego Candia-Rivera0https://orcid.org/0000-0002-4043-217XFederico Raimondo1https://orcid.org/0000-0003-4087-8259Pauline Pérez2Lionel Naccache3Catherine Tallon-Baudry4https://orcid.org/0000-0001-8480-5831Jacobo D Sitt5https://orcid.org/0000-0002-3878-4846Laboratoire de Neurosciences Cognitives et Computationnelles, Département d’Etudes Cognitives, École Normale Supérieure, INSERM, Université PSL, Paris, France; Sorbonne Université, Paris Brain Institute (ICM), INRIA, CNRS, INSERM, AP-HP, Hôpital Pitié-Salpêtrière, Paris, FranceSorbonne Université, Paris Brain Institute (ICM), INRIA, CNRS, INSERM, AP-HP, Hôpital Pitié-Salpêtrière, Paris, France; Institute of Neuroscience and Medicine (INM-7: Brain and Behaviour), Forschungszentrum Jülich, Jülich, Germany; Institute of Systems Neuroscience, Heinrich Heine University Düsseldorf, Düsseldorf, GermanySorbonne Université, Paris Brain Institute (ICM), INRIA, CNRS, INSERM, AP-HP, Hôpital Pitié-Salpêtrière, Paris, France; AP-HP, Hôpital de la Pitié Salpêtrière, Neuro ICU, DMU Neurosciences, Paris, FranceSorbonne Université, Paris Brain Institute (ICM), INRIA, CNRS, INSERM, AP-HP, Hôpital Pitié-Salpêtrière, Paris, France; Pitié-Salpêtrière Faculty of Medicine, Pierre and Marie Curie University, Sorbonne Universities, Paris, France; INSERM, National Institute of Health and Medical Research, Paris, France; Department of Neurology, Pitié-Salpêtrière Hospital Group, Public Hospital Network of Paris, Paris, France; Department of Neurophysiology, Pitié-Salpêtrière Hospital Group, Public Hospital Network of Paris, Paris, FranceLaboratoire de Neurosciences Cognitives et Computationnelles, Département d’Etudes Cognitives, École Normale Supérieure, INSERM, Université PSL, Paris, FranceSorbonne Université, Paris Brain Institute (ICM), INRIA, CNRS, INSERM, AP-HP, Hôpital Pitié-Salpêtrière, Paris, France; INSERM, National Institute of Health and Medical Research, Paris, FranceRecent research suggests that brain-heart interactions are associated with perceptual and self-consciousness. In this line, the neural responses to visceral inputs have been hypothesized to play a leading role in shaping our subjective experience. This study aims to investigate whether the contextual processing of auditory irregularities modulates both direct neuronal responses to the auditory stimuli (ERPs) and the neural responses to heartbeats, as measured with heartbeat-evoked responses (HERs). HERs were computed in patients with disorders of consciousness, diagnosed with a minimally conscious state or unresponsive wakefulness syndrome. We tested whether HERs reflect conscious auditory perception, which can potentially provide additional information for the consciousness diagnosis. EEG recordings were taken during the local-global paradigm, which evaluates the capacity of a patient to detect the appearance of auditory irregularities at local (short-term) and global (long-term) levels. The results show that local and global effects produce distinct ERPs and HERs, which can help distinguish between the minimally conscious state and unresponsive wakefulness syndrome patients. Furthermore, we found that ERP and HER responses were not correlated suggesting that independent neuronal mechanisms are behind them. These findings suggest that HER modulations in response to auditory irregularities, especially local irregularities, may be used as a novel neural marker of consciousness and may aid in the bedside diagnosis of disorders of consciousness with a more cost-effective option than neuroimaging methods.https://elifesciences.org/articles/75352consciousnessbrain-heart interactionsheartbeat-evoked responsesperceptiondisorders of consciousness
spellingShingle Diego Candia-Rivera
Federico Raimondo
Pauline Pérez
Lionel Naccache
Catherine Tallon-Baudry
Jacobo D Sitt
Conscious processing of global and local auditory irregularities causes differentiated heartbeat-evoked responses
eLife
consciousness
brain-heart interactions
heartbeat-evoked responses
perception
disorders of consciousness
title Conscious processing of global and local auditory irregularities causes differentiated heartbeat-evoked responses
title_full Conscious processing of global and local auditory irregularities causes differentiated heartbeat-evoked responses
title_fullStr Conscious processing of global and local auditory irregularities causes differentiated heartbeat-evoked responses
title_full_unstemmed Conscious processing of global and local auditory irregularities causes differentiated heartbeat-evoked responses
title_short Conscious processing of global and local auditory irregularities causes differentiated heartbeat-evoked responses
title_sort conscious processing of global and local auditory irregularities causes differentiated heartbeat evoked responses
topic consciousness
brain-heart interactions
heartbeat-evoked responses
perception
disorders of consciousness
url https://elifesciences.org/articles/75352
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