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

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Abstract

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.

Data availability

The data used in this study can be made available upon reasonable request. Because of the sensitive nature of the clinical information concerning the patients, the ethics protocol does not allow open data sharing.To access the raw data, the potential interested researcher would need to contact the corresponding authors of the study. Together they would need to ask for an authorization from the local ethics committee, CPP Île de France 1 (Paris, France).The codes and pre-processed data are available at https://github.com/diegocandiar/brain_heart_doc

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Author details

Diego Candia-Rivera

École normale supérieure, INSERM, PSL Research University, Paris, France

For correspondence
diego.candiarivera@icm-institute.org

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4043-217X
Federico Raimondo

Paris Brain Institute, Sorbonne Université - ICM, Inserm U1127, CNRS UMR 7225, Paris, France

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4087-8259
Pauline Pérez

Paris Brain Institute, Sorbonne Université - ICM, Inserm U1127, CNRS UMR 7225, Paris, France

Competing interests
The authors declare that no competing interests exist.
Lionel Naccache

Paris Brain Institute, Sorbonne Université - ICM, Inserm U1127, CNRS UMR 7225, Paris, France

Competing interests
The authors declare that no competing interests exist.
Catherine Tallon-Baudry

École normale supérieure, INSERM, PSL Research University, Paris, France

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8480-5831
Jacobo Diego Sitt

Paris Brain Institute, Sorbonne Université - ICM, Inserm U1127, CNRS UMR 7225, Paris, France

For correspondence
jacobo.sitt@inserm.fr

Competing interests
The authors declare that no competing interests exist.

Funding

CIFAR (-)

Catherine Tallon-Baudry

ANR (ANR-17-EURE-0017)

Catherine Tallon-Baudry

ANR (ANR-10- IAIHU-06)

Jacobo Diego Sitt

Sorbonne Université (EMERGENCE)

Jacobo Diego Sitt

European Commission (JTC2019)

Jacobo Diego Sitt

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: The study was approved by the ethics committee of CPP Île de France 1 (Paris, France). Informed consent was signed by the patients' legal representatives for approval of participation in the study, as required by the declaration of Helsinki. (NEURO-DoC/HAO-84 006/20130409 and M-NEURO-DoC/NCT04534777).

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.