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Modulatory dynamics of periodic and aperiodic activity in respiration-brain coupling

Author

Listed:
  • Daniel S. Kluger

    (University of Münster
    University of Münster)

  • Carina Forster

    (Max Planck Institute for Human Cognitive and Brain Sciences
    Charité – Universitätsmedizin Berlin, Einstein Center for Neurosciences
    Charité – Universitätsmedizin Berlin, Bernstein Center for Computational Neuroscience)

  • Omid Abbasi

    (University of Münster)

  • Nikos Chalas

    (University of Münster
    University of Münster)

  • Arno Villringer

    (Max Planck Institute for Human Cognitive and Brain Sciences
    Charité – Universitätsmedizin Berlin, Einstein Center for Neurosciences
    Humboldt-Universität zu Berlin, Faculty of Philosophy, Berlin School of Mind and Brain, MindBrainBody Institute)

  • Joachim Gross

    (University of Münster
    University of Münster)

Abstract

Bodily rhythms such as respiration are increasingly acknowledged to modulate neural oscillations underlying human action, perception, and cognition. Conversely, the link between respiration and aperiodic brain activity – a non-oscillatory reflection of excitation-inhibition (E:I) balance – has remained unstudied. Aiming to disentangle potential respiration-related dynamics of periodic and aperiodic activity, we applied recently developed algorithms of time-resolved parameter estimation to resting-state MEG and EEG data from two labs (total N = 78 participants). We provide evidence that fluctuations of aperiodic brain activity (1/f slope) are phase-locked to the respiratory cycle, which suggests that spontaneous state shifts of excitation-inhibition balance are at least partly influenced by peripheral bodily signals. Moreover, differential temporal dynamics in their coupling to non-oscillatory and oscillatory activity raise the possibility of a functional distinction in the way each component is related to respiration. Our findings highlight the role of respiration as a physiological influence on brain signalling.

Suggested Citation

  • Daniel S. Kluger & Carina Forster & Omid Abbasi & Nikos Chalas & Arno Villringer & Joachim Gross, 2023. "Modulatory dynamics of periodic and aperiodic activity in respiration-brain coupling," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40250-9
    DOI: 10.1038/s41467-023-40250-9
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    References listed on IDEAS

    as
    1. Nikolaos Karalis & Anton Sirota, 2022. "Breathing coordinates cortico-hippocampal dynamics in mice during offline states," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    2. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    3. Alexander V. Gourine & Enrique Llaudet & Nicholas Dale & K. Michael Spyer, 2005. "ATP is a mediator of chemosensory transduction in the central nervous system," Nature, Nature, vol. 436(7047), pages 108-111, July.
    4. Ofer Perl & Aharon Ravia & Mica Rubinson & Ami Eisen & Timna Soroka & Nofar Mor & Lavi Secundo & Noam Sobel, 2019. "Human non-olfactory cognition phase-locked with inhalation," Nature Human Behaviour, Nature, vol. 3(5), pages 501-512, May.
    5. Matthew F. Glasser & Timothy S. Coalson & Emma C. Robinson & Carl D. Hacker & John Harwell & Essa Yacoub & Kamil Ugurbil & Jesper Andersson & Christian F. Beckmann & Mark Jenkinson & Stephen M. Smith , 2016. "A multi-modal parcellation of human cerebral cortex," Nature, Nature, vol. 536(7615), pages 171-178, August.
    6. Mingshan Xue & Bassam V. Atallah & Massimo Scanziani, 2014. "Equalizing excitation–inhibition ratios across visual cortical neurons," Nature, Nature, vol. 511(7511), pages 596-600, July.
    7. J. Ito & S. Roy & Y. Liu & Y. Cao & M. Fletcher & L. Lu & J.D. Boughter & S. Grün & D.H. Heck, 2014. "Whisker barrel cortex delta oscillations and gamma power in the awake mouse are linked to respiration," Nature Communications, Nature, vol. 5(1), pages 1-10, May.
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