Role of the postinspiratory complex in regulating swallow-breathing coordination and other laryngeal behaviors

  1. Alyssa D Huff
  2. Marlusa K Amarante
  3. Luiz M Oliveira
  4. Jan-Marino Ramirez  Is a corresponding author
  1. Seattle Children's Research Institute, United States

Abstract

Breathing needs to be tightly coordinated with upper airway behaviors, such as swallowing. Discoordination leads to aspiration pneumonia, the leading cause of death in neurodegenerative disease. Here we study the role of the Postinspiratory Complex (PiCo) in coordinating breathing and swallowing. Using optogenetic approaches in freely breathing- anesthetized ChATcre:Ai32, Vglut2cre:Ai32 and intersectional recombination of ChATcre:Vglut2FlpO:ChR2 mice reveals PiCo mediates airway protective behaviors. Activation of PiCo during inspiration or the beginning of postinspiration triggers swallow behavior in an all-or-nothing manner, while there is a higher probability for stimulating only laryngeal activation when activated further into expiration. Laryngeal activation is dependent on stimulation duration. Sufficient bilateral PiCo activation is necessary for preserving the physiologic swallow motor sequence, since activation of only a few PiCo neurons or unilateral activation leads to blurred upper airway behavioral responses. We believe PiCo acts as an interface between the swallow pattern generator and the preBötzinger complex to coordinate swallow and breathing. Investigating PiCo's role in swallow and laryngeal coordination will aid in understanding discoordination with breathing in neurological diseases.

Data availability

All data is publicly available (10.6084/m9.figshare.21909819).

The following data sets were generated

Article and author information

Author details

  1. Alyssa D Huff

    Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2817-251X
  2. Marlusa K Amarante

    Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Luiz M Oliveira

    Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jan-Marino Ramirez

    Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, United States
    For correspondence
    jan.ramirez@seattlechildrens.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5626-3999

Funding

National Institutes of Health (HL090554)

  • Jan-Marino Ramirez

National Institutes of Health (HL144801)

  • Jan-Marino Ramirez

National Institutes of Health (HL151389)

  • Jan-Marino Ramirez

National Institutes of Health (HL160102-01)

  • Alyssa D Huff

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

Reviewing Editor

  1. Muriel Thoby-Brisson, CNRS Université de Bordeaux, France

Ethics

Animal experimentation: All experiments and animal procedures were approved by the Seattle Children's Research Institute's Animal Care and Use Committee and were conducted in accordance with the National Institutes of Health guidelines.(IACUC #0058)

Version history

  1. Received: January 11, 2023
  2. Preprint posted: January 20, 2023 (view preprint)
  3. Accepted: June 1, 2023
  4. Accepted Manuscript published: June 5, 2023 (version 1)
  5. Version of Record published: June 13, 2023 (version 2)
  6. Version of Record updated: June 21, 2023 (version 3)

Copyright

© 2023, Huff 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.

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  1. Alyssa D Huff
  2. Marlusa K Amarante
  3. Luiz M Oliveira
  4. Jan-Marino Ramirez
(2023)
Role of the postinspiratory complex in regulating swallow-breathing coordination and other laryngeal behaviors
eLife 12:e86103.
https://doi.org/10.7554/eLife.86103

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https://doi.org/10.7554/eLife.86103