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The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest

Bodily rhythms appear as novel scaffolding mechanisms orchestrating the spatiotemporal organization of spontaneous brain activity. Here, we follow-up on the discovery of the gastric resting-state network (Rebollo et al., 2018), composed of brain regions in which the fMRI signal is phase-synchronized...

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Autores principales: Rebollo, Ignacio, Tallon-Baudry, Catherine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8936619/
https://www.ncbi.nlm.nih.gov/pubmed/35074866
http://dx.doi.org/10.1523/JNEUROSCI.1285-21.2021
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author Rebollo, Ignacio
Tallon-Baudry, Catherine
author_facet Rebollo, Ignacio
Tallon-Baudry, Catherine
author_sort Rebollo, Ignacio
collection PubMed
description Bodily rhythms appear as novel scaffolding mechanisms orchestrating the spatiotemporal organization of spontaneous brain activity. Here, we follow-up on the discovery of the gastric resting-state network (Rebollo et al., 2018), composed of brain regions in which the fMRI signal is phase-synchronized to the slow (0.05 Hz) electrical rhythm of the stomach. Using a larger sample size (n = 63 human participants, both genders), we further characterize the anatomy and effect sizes of gastric-brain coupling across resting-state networks, a fine grained cortical parcellation, as well as along the main gradients of cortical organization. Most (67%) of the gastric network is included in the somato-motor-auditory (38%) and visual (29%) resting state networks (RSNs). Gastric brain coupling also occurs in the granular insula and, to a lesser extent, in the piriform cortex. Thus, all sensory and motor cortices corresponding to both exteroceptive and interoceptive modalities are coupled to the gastric rhythm during rest. Conversely, little gastric-brain coupling occurs in cognitive networks and transmodal regions. These results suggest not only that gastric rhythm and sensory-motor processes are likely to interact, but also that gastric-brain coupling might be a mechanism of sensory and motor integration that mostly bypasses cognition, complementing the classical hierarchical organization of the human brain. SIGNIFICANCE STATEMENT While there is growing interest for brain-body communication in general and brain-viscera communication in particular, little is known about how the brain interacts with the gastric rhythm, the slow electrical rhythm continuously produced in the stomach. Here, we show in human participants at rest that the gastric network, composed of brain regions synchronized with delays to the gastric rhythm, includes all motor and sensory (vision, audition, touch and interoception, olfaction) regions, but only few of the transmodal regions associated with higher-level cognition. Such results prompt for a reconsideration of the classical view of cortical organization, where the different sensory modalities are considered as relatively independent modules.
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spelling pubmed-89366192022-09-16 The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest Rebollo, Ignacio Tallon-Baudry, Catherine J Neurosci Research Articles Bodily rhythms appear as novel scaffolding mechanisms orchestrating the spatiotemporal organization of spontaneous brain activity. Here, we follow-up on the discovery of the gastric resting-state network (Rebollo et al., 2018), composed of brain regions in which the fMRI signal is phase-synchronized to the slow (0.05 Hz) electrical rhythm of the stomach. Using a larger sample size (n = 63 human participants, both genders), we further characterize the anatomy and effect sizes of gastric-brain coupling across resting-state networks, a fine grained cortical parcellation, as well as along the main gradients of cortical organization. Most (67%) of the gastric network is included in the somato-motor-auditory (38%) and visual (29%) resting state networks (RSNs). Gastric brain coupling also occurs in the granular insula and, to a lesser extent, in the piriform cortex. Thus, all sensory and motor cortices corresponding to both exteroceptive and interoceptive modalities are coupled to the gastric rhythm during rest. Conversely, little gastric-brain coupling occurs in cognitive networks and transmodal regions. These results suggest not only that gastric rhythm and sensory-motor processes are likely to interact, but also that gastric-brain coupling might be a mechanism of sensory and motor integration that mostly bypasses cognition, complementing the classical hierarchical organization of the human brain. SIGNIFICANCE STATEMENT While there is growing interest for brain-body communication in general and brain-viscera communication in particular, little is known about how the brain interacts with the gastric rhythm, the slow electrical rhythm continuously produced in the stomach. Here, we show in human participants at rest that the gastric network, composed of brain regions synchronized with delays to the gastric rhythm, includes all motor and sensory (vision, audition, touch and interoception, olfaction) regions, but only few of the transmodal regions associated with higher-level cognition. Such results prompt for a reconsideration of the classical view of cortical organization, where the different sensory modalities are considered as relatively independent modules. Society for Neuroscience 2022-03-16 /pmc/articles/PMC8936619/ /pubmed/35074866 http://dx.doi.org/10.1523/JNEUROSCI.1285-21.2021 Text en Copyright © 2022 Rebollo and Tallon-Baudry https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Rebollo, Ignacio
Tallon-Baudry, Catherine
The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest
title The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest
title_full The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest
title_fullStr The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest
title_full_unstemmed The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest
title_short The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest
title_sort sensory and motor components of the cortical hierarchy are coupled to the rhythm of the stomach during rest
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8936619/
https://www.ncbi.nlm.nih.gov/pubmed/35074866
http://dx.doi.org/10.1523/JNEUROSCI.1285-21.2021
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