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Featured ArticleResearch Articles, Systems/Circuits

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

Ignacio Rebollo and Catherine Tallon-Baudry
Journal of Neuroscience 16 March 2022, 42 (11) 2205-2220; DOI: https://doi.org/10.1523/JNEUROSCI.1285-21.2021
Ignacio Rebollo
1Laboratoire de Neurosciences Cognitives et Computationnelles, Institut National de la Santé et de la Recherche Médicale, Ecole Normale Supérieure, Paris Sciences et Lettres University, Paris 75005, France
2German Institute of Human Nutrition Potsdam-Rehbrücke, Nuthetal 14558, Germany
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Catherine Tallon-Baudry
1Laboratoire de Neurosciences Cognitives et Computationnelles, Institut National de la Santé et de la Recherche Médicale, Ecole Normale Supérieure, Paris Sciences et Lettres University, Paris 75005, France
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Abstract

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.

  • autonomic
  • cortical gradients
  • electrogastrogram
  • gastric
  • phase synchronization
  • resting state networks

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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The Journal of Neuroscience: 42 (11)
Journal of Neuroscience
Vol. 42, Issue 11
16 Mar 2022
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The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest
Ignacio Rebollo, Catherine Tallon-Baudry
Journal of Neuroscience 16 March 2022, 42 (11) 2205-2220; DOI: 10.1523/JNEUROSCI.1285-21.2021

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The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest
Ignacio Rebollo, Catherine Tallon-Baudry
Journal of Neuroscience 16 March 2022, 42 (11) 2205-2220; DOI: 10.1523/JNEUROSCI.1285-21.2021
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Keywords

  • autonomic
  • cortical gradients
  • electrogastrogram
  • gastric
  • phase synchronization
  • resting state networks

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