Neural underpinning of a respiration-associated resting-state fMRI network

  1. Wenyu Tu
  2. Nanyin Zhang  Is a corresponding author
  1. Pennsylvania State University, United States

Abstract

Respiration can induce motion and CO2 fluctuation during resting-state fMRI (rsfMRI) scans, which will lead to non-neural artifacts in the rsfMRI signal. In the meantime, as a crucial physiologic process, respiration that can directly drive neural activity change in the brain, and may thereby modulate the rsfMRI signal. Nonetheless, this potential neural component in the respiration-fMRI relationship is largely unexplored. To elucidate this issue, here we simultaneously recorded the electrophysiology, rsfMRI and respiration signals in rats. Our data show that respiration is indeed associated with neural activity changes, evidenced by a phase-locking relationship between slow respiration variations and the gamma-band power of the electrophysiologic signal recorded in the anterior cingulate cortex. Intriguingly, slow respiration variations are also linked to a characteristic rsfMRI network, which is mediated by gamma-band neural activity. In addition, this respiration-related brain network disappears when brain-wide neural activity is silenced at an iso-electrical state, while the respiration is maintained, further confirming the necessary role of neural activity in this network. Taken together, this study identifies a respiration-related brain network underpinned by neural activity, which represents a novel component in the respiration-rsfMRI relationship that is distinct from respiration-related rsfMRI artifacts. It opens a new avenue for investigating the interactions between respiration, neural activity and resting-state brain networks in both healthy and diseased conditions.

Data availability

All data for this study have been deposited to NITRIC repository.

The following data sets were generated
    1. Tu W
    2. Zhang
    3. N
    (2022) Electrophysiology, resting state fMRI and respiration in rats
    NeuroImaging Tools and Resources Collaboratory (NITRC), https://www.nitrc.org/docman/?group_id=1582.

Article and author information

Author details

  1. Wenyu Tu

    The Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Nanyin Zhang

    Department of Biomedical Engineering, Pennsylvania State University, University Park, United States
    For correspondence
    nuz2@psu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5824-9058

Funding

National Institute of Neurological Disorders and Stroke (R01NS085200)

  • Nanyin Zhang

National Institute of Mental Health (RF1MH114224)

  • Nanyin Zhang

National Institute of General Medical Sciences (R01GM141792)

  • Nanyin Zhang

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

Ethics

Animal experimentation: The present study was approved by the Pennsylvania State University Institutional Animal Care and Use Committee (IACUC) with the protocol number of PRAMS201343583.

Reviewing Editor

  1. Karla L Miller, University of Oxford, United Kingdom

Publication history

  1. Received: July 1, 2022
  2. Preprint posted: July 13, 2022 (view preprint)
  3. Accepted: October 13, 2022
  4. Accepted Manuscript published: October 20, 2022 (version 1)
  5. Version of Record published: November 9, 2022 (version 2)

Copyright

© 2022, Tu & Zhang

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.

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  1. Wenyu Tu
  2. Nanyin Zhang
(2022)
Neural underpinning of a respiration-associated resting-state fMRI network
eLife 11:e81555.
https://doi.org/10.7554/eLife.81555
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