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

  1. Diego Candia-Rivera  Is a corresponding author
  2. Federico Raimondo
  3. Pauline Pérez
  4. Lionel Naccache
  5. Catherine Tallon-Baudry
  6. Jacobo Diego Sitt  Is a corresponding author
  1. École normale supérieure, INSERM, PSL Research University, France
  2. Sorbonne Université - ICM, Inserm U1127, CNRS UMR 7225, France

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

Article and author information

Author details

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4043-217X
  2. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4087-8259
  3. 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.
  4. 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.
  5. Catherine Tallon-Baudry

    École normale supérieure, INSERM, PSL Research University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8480-5831
  6. 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

© 2023, Candia-Rivera et al.

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.

Metrics

  • 1,045
    views
  • 209
    downloads
  • 6
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Diego Candia-Rivera
  2. Federico Raimondo
  3. Pauline Pérez
  4. Lionel Naccache
  5. Catherine Tallon-Baudry
  6. Jacobo Diego Sitt
(2023)
Conscious processing of global and local auditory irregularities causes differentiated heartbeat-evoked responses
eLife 12:e75352.
https://doi.org/10.7554/eLife.75352

Share this article

https://doi.org/10.7554/eLife.75352

Further reading

    1. Neuroscience
    Paul I Jaffe, Gustavo X Santiago-Reyes ... Russell A Poldrack
    Research Article

    Evidence accumulation models (EAMs) are the dominant framework for modeling response time (RT) data from speeded decision-making tasks. While providing a good quantitative description of RT data in terms of abstract perceptual representations, EAMs do not explain how the visual system extracts these representations in the first place. To address this limitation, we introduce the visual accumulator model (VAM), in which convolutional neural network models of visual processing and traditional EAMs are jointly fitted to trial-level RTs and raw (pixel-space) visual stimuli from individual subjects in a unified Bayesian framework. Models fitted to large-scale cognitive training data from a stylized flanker task captured individual differences in congruency effects, RTs, and accuracy. We find evidence that the selection of task-relevant information occurs through the orthogonalization of relevant and irrelevant representations, demonstrating how our framework can be used to relate visual representations to behavioral outputs. Together, our work provides a probabilistic framework for both constraining neural network models of vision with behavioral data and studying how the visual system extracts representations that guide decisions.

    1. Neuroscience
    Aneri Soni, Michael J Frank
    Research Article

    How and why is working memory (WM) capacity limited? Traditional cognitive accounts focus either on limitations on the number or items that can be stored (slots models), or loss of precision with increasing load (resource models). Here, we show that a neural network model of prefrontal cortex and basal ganglia can learn to reuse the same prefrontal populations to store multiple items, leading to resource-like constraints within a slot-like system, and inducing a trade-off between quantity and precision of information. Such ‘chunking’ strategies are adapted as a function of reinforcement learning and WM task demands, mimicking human performance and normative models. Moreover, adaptive performance requires a dynamic range of dopaminergic signals to adjust striatal gating policies, providing a new interpretation of WM difficulties in patient populations such as Parkinson’s disease, ADHD, and schizophrenia. These simulations also suggest a computational rather than anatomical limit to WM capacity.