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Respiratory entrainment of units in the mouse parietal cortex depends on vigilance state

Synchronous oscillations are essential for coordinated activity in neuronal networks and, hence, for behavior and cognition. While most network oscillations are generated within the central nervous system, recent evidence shows that rhythmic body processes strongly influence activity patterns throug...

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Autores principales: Jung, Felix, Yanovsky, Yevgenij, Brankačk, Jurij, Tort, Adriano B. L., Draguhn, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9816213/
https://www.ncbi.nlm.nih.gov/pubmed/35982341
http://dx.doi.org/10.1007/s00424-022-02727-2
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author Jung, Felix
Yanovsky, Yevgenij
Brankačk, Jurij
Tort, Adriano B. L.
Draguhn, Andreas
author_facet Jung, Felix
Yanovsky, Yevgenij
Brankačk, Jurij
Tort, Adriano B. L.
Draguhn, Andreas
author_sort Jung, Felix
collection PubMed
description Synchronous oscillations are essential for coordinated activity in neuronal networks and, hence, for behavior and cognition. While most network oscillations are generated within the central nervous system, recent evidence shows that rhythmic body processes strongly influence activity patterns throughout the brain. A major factor is respiration (Resp), which entrains multiple brain regions at the mesoscopic (local field potential) and single-cell levels. However, it is largely unknown how such Resp-driven rhythms interact or compete with internal brain oscillations, especially those with similar frequency domains. In mice, Resp and theta (θ) oscillations have overlapping frequencies and co-occur in various brain regions. Here, we investigated the effects of Resp and θ on neuronal discharges in the mouse parietal cortex during four behavioral states which either show prominent θ (REM sleep and active waking (AW)) or lack significant θ (NREM sleep and waking immobility (WI)). We report a pronounced state-dependence of spike modulation by both rhythms. During REM sleep, θ effects on unit discharges dominate, while during AW, Resp has a larger influence, despite the concomitant presence of θ oscillations. In most states, unit modulation by θ or Resp increases with mean firing rate. The preferred timing of Resp-entrained discharges (inspiration versus expiration) varies between states, indicating state-specific and different underlying mechanisms. Our findings show that neurons in an associative cortex area are differentially and state-dependently modulated by two fundamentally different processes: brain-endogenous θ oscillations and rhythmic somatic feedback signals from Resp. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00424-022-02727-2.
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spelling pubmed-98162132023-01-07 Respiratory entrainment of units in the mouse parietal cortex depends on vigilance state Jung, Felix Yanovsky, Yevgenij Brankačk, Jurij Tort, Adriano B. L. Draguhn, Andreas Pflugers Arch Original Article Synchronous oscillations are essential for coordinated activity in neuronal networks and, hence, for behavior and cognition. While most network oscillations are generated within the central nervous system, recent evidence shows that rhythmic body processes strongly influence activity patterns throughout the brain. A major factor is respiration (Resp), which entrains multiple brain regions at the mesoscopic (local field potential) and single-cell levels. However, it is largely unknown how such Resp-driven rhythms interact or compete with internal brain oscillations, especially those with similar frequency domains. In mice, Resp and theta (θ) oscillations have overlapping frequencies and co-occur in various brain regions. Here, we investigated the effects of Resp and θ on neuronal discharges in the mouse parietal cortex during four behavioral states which either show prominent θ (REM sleep and active waking (AW)) or lack significant θ (NREM sleep and waking immobility (WI)). We report a pronounced state-dependence of spike modulation by both rhythms. During REM sleep, θ effects on unit discharges dominate, while during AW, Resp has a larger influence, despite the concomitant presence of θ oscillations. In most states, unit modulation by θ or Resp increases with mean firing rate. The preferred timing of Resp-entrained discharges (inspiration versus expiration) varies between states, indicating state-specific and different underlying mechanisms. Our findings show that neurons in an associative cortex area are differentially and state-dependently modulated by two fundamentally different processes: brain-endogenous θ oscillations and rhythmic somatic feedback signals from Resp. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00424-022-02727-2. Springer Berlin Heidelberg 2022-08-19 2023 /pmc/articles/PMC9816213/ /pubmed/35982341 http://dx.doi.org/10.1007/s00424-022-02727-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Original Article
Jung, Felix
Yanovsky, Yevgenij
Brankačk, Jurij
Tort, Adriano B. L.
Draguhn, Andreas
Respiratory entrainment of units in the mouse parietal cortex depends on vigilance state
title Respiratory entrainment of units in the mouse parietal cortex depends on vigilance state
title_full Respiratory entrainment of units in the mouse parietal cortex depends on vigilance state
title_fullStr Respiratory entrainment of units in the mouse parietal cortex depends on vigilance state
title_full_unstemmed Respiratory entrainment of units in the mouse parietal cortex depends on vigilance state
title_short Respiratory entrainment of units in the mouse parietal cortex depends on vigilance state
title_sort respiratory entrainment of units in the mouse parietal cortex depends on vigilance state
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9816213/
https://www.ncbi.nlm.nih.gov/pubmed/35982341
http://dx.doi.org/10.1007/s00424-022-02727-2
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