Respiration aligns perception with neural excitability

  1. Daniel S Kluger  Is a corresponding author
  2. Elio Balestrieri
  3. Niko A Busch
  4. Joachim Gross
  1. University of Münster, Germany

Abstract

Recent studies from the field of interoception have highlighted the link between bodily and neural rhythms during action, perception, and cognition. The mechanisms underlying functional body-brain coupling, however, are poorly understood, as are the ways in which they modulate behaviour. We acquired respiration and human magnetoencephalography (MEG) data from a near-threshold spatial detection task to investigate the trivariate relationship between respiration, neural excitability, and performance. Respiration was found to significantly modulate perceptual sensitivity as well as posterior alpha power (8 - 13 Hz), a well-established proxy of cortical excitability. In turn, alpha suppression prior to detected vs undetected targets underscored the behavioural benefits of heightened excitability. Notably, respiration-locked excitability changes were maximised at a respiration phase lag of around -30° and thus temporally preceded performance changes. In line with interoceptive inference accounts, these results suggest that respiration actively aligns sampling of sensory information with transient cycles of heightened excitability to facilitate performance.

Data availability

The anonymised data supporting the findings of this study are openly available from on the Open Science Framework (https://osf.io/ajuzh/).

Article and author information

Author details

  1. Daniel S Kluger

    University of Münster, Münster, Germany
    For correspondence
    daniel.kluger@uni-muenster.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0691-794X
  2. Elio Balestrieri

    University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Niko A Busch

    University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4837-0345
  4. Joachim Gross

    University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.

Funding

Interdisciplinary Center for Clinical Research, University of Münster (Gro3/001/19)

  • Joachim Gross

Deutsche Forschungsgemeinschaft (GR2024/5-1)

  • Joachim Gross

Deutsche Forschungsgemeinschaft (BU2400/9-1)

  • Niko A Busch

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

Ethics

Human subjects: All participants gave written informed consent prior to all experimental procedures. The study was approved by the local ethics committee of the University of Muenster (approval ID 2018-068-f-S) and complied with the Declaration of Helsinki.

Reviewing Editor

  1. Jonas Obleser, University of Lübeck, Germany

Publication history

  1. Preprint posted: March 25, 2021 (view preprint)
  2. Received: June 2, 2021
  3. Accepted: December 13, 2021
  4. Accepted Manuscript published: December 14, 2021 (version 1)
  5. Version of Record published: January 17, 2022 (version 2)

Copyright

© 2021, Kluger 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

  • 2,634
    Page views
  • 398
    Downloads
  • 23
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. Daniel S Kluger
  2. Elio Balestrieri
  3. Niko A Busch
  4. Joachim Gross
(2021)
Respiration aligns perception with neural excitability
eLife 10:e70907.
https://doi.org/10.7554/eLife.70907

Further reading

    1. Neuroscience
    Abraham Katzen, Hui-Kuan Chung ... Shawn R Lockery
    Research Article Updated

    In value-based decision making, options are selected according to subjective values assigned by the individual to available goods and actions. Despite the importance of this faculty of the mind, the neural mechanisms of value assignments, and how choices are directed by them, remain obscure. To investigate this problem, we used a classic measure of utility maximization, the Generalized Axiom of Revealed Preference, to quantify internal consistency of food preferences in Caenorhabditis elegans, a nematode worm with a nervous system of only 302 neurons. Using a novel combination of microfluidics and electrophysiology, we found that C. elegans food choices fulfill the necessary and sufficient conditions for utility maximization, indicating that nematodes behave as if they maintain, and attempt to maximize, an underlying representation of subjective value. Food choices are well-fit by a utility function widely used to model human consumers. Moreover, as in many other animals, subjective values in C. elegans are learned, a process we find requires intact dopamine signaling. Differential responses of identified chemosensory neurons to foods with distinct growth potentials are amplified by prior consumption of these foods, suggesting that these neurons may be part of a value-assignment system. The demonstration of utility maximization in an organism with a very small nervous system sets a new lower bound on the computational requirements for utility maximization and offers the prospect of an essentially complete explanation of value-based decision making at single neuron resolution in this organism.

    1. Neuroscience
    Yuan-hao Wu, Ella Podvalny, Biyu J He
    Research Article Updated

    While there is a wealth of knowledge about core object recognition—our ability to recognize clear, high-contrast object images—how the brain accomplishes object recognition tasks under increased uncertainty remains poorly understood. We investigated the spatiotemporal neural dynamics underlying object recognition under increased uncertainty by combining MEG and 7 Tesla (7T) fMRI in humans during a threshold-level object recognition task. We observed an early, parallel rise of recognition-related signals across ventral visual and frontoparietal regions that preceded the emergence of category-related information. Recognition-related signals in ventral visual regions were best explained by a two-state representational format whereby brain activity bifurcated for recognized and unrecognized images. By contrast, recognition-related signals in frontoparietal regions exhibited a reduced representational space for recognized images, yet with sharper category information. These results provide a spatiotemporally resolved view of neural activity supporting object recognition under uncertainty, revealing a pattern distinct from that underlying core object recognition.