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Parieto-occipital ERP indicators of gut mechanosensation in humans

Understanding the neural processes governing the human gut-brain connection has been challenging due to the inaccessibility of the body’s interior. Here, we investigated neural responses to gastrointestinal sensation using a minimally invasive mechanosensory probe by quantifying brain, stomach, and...

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Autores principales: Mayeli, Ahmad, Al Zoubi, Obada, White, Evan J., Chappelle, Sheridan, Kuplicki, Rayus, Morton, Alexa, Bruce, Jaimee, Smith, Ryan, Feinstein, Justin S., Bodurka, Jerzy, Paulus, Martin P., Khalsa, Sahib S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10264354/
https://www.ncbi.nlm.nih.gov/pubmed/37311748
http://dx.doi.org/10.1038/s41467-023-39058-4
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author Mayeli, Ahmad
Al Zoubi, Obada
White, Evan J.
Chappelle, Sheridan
Kuplicki, Rayus
Morton, Alexa
Bruce, Jaimee
Smith, Ryan
Feinstein, Justin S.
Bodurka, Jerzy
Paulus, Martin P.
Khalsa, Sahib S.
author_facet Mayeli, Ahmad
Al Zoubi, Obada
White, Evan J.
Chappelle, Sheridan
Kuplicki, Rayus
Morton, Alexa
Bruce, Jaimee
Smith, Ryan
Feinstein, Justin S.
Bodurka, Jerzy
Paulus, Martin P.
Khalsa, Sahib S.
author_sort Mayeli, Ahmad
collection PubMed
description Understanding the neural processes governing the human gut-brain connection has been challenging due to the inaccessibility of the body’s interior. Here, we investigated neural responses to gastrointestinal sensation using a minimally invasive mechanosensory probe by quantifying brain, stomach, and perceptual responses following the ingestion of a vibrating capsule. Participants successfully perceived capsule stimulation under two vibration conditions (normal and enhanced), as evidenced by above chance accuracy scores. Perceptual accuracy improved significantly during the enhanced relative to normal stimulation, which was associated with faster stimulation detection and reduced reaction time variability. Capsule stimulation induced late neural responses in parieto-occipital electrodes near the midline. Moreover, these ‘gastric evoked potentials’ showed intensity-dependent increases in amplitude and were significantly correlated with perceptual accuracy. Our results replicated in a separate experiment, and abdominal X-ray imaging localized most capsule stimulations to the gastroduodenal segments. Combined with our prior observation that a Bayesian model is capable of estimating computational parameters of gut-brain mechanosensation, these findings highlight a unique form of enterically-focused sensory monitoring within the human brain, with implications for understanding gut feelings and gut-brain interactions in healthy and clinical populations.
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spelling pubmed-102643542023-06-15 Parieto-occipital ERP indicators of gut mechanosensation in humans Mayeli, Ahmad Al Zoubi, Obada White, Evan J. Chappelle, Sheridan Kuplicki, Rayus Morton, Alexa Bruce, Jaimee Smith, Ryan Feinstein, Justin S. Bodurka, Jerzy Paulus, Martin P. Khalsa, Sahib S. Nat Commun Article Understanding the neural processes governing the human gut-brain connection has been challenging due to the inaccessibility of the body’s interior. Here, we investigated neural responses to gastrointestinal sensation using a minimally invasive mechanosensory probe by quantifying brain, stomach, and perceptual responses following the ingestion of a vibrating capsule. Participants successfully perceived capsule stimulation under two vibration conditions (normal and enhanced), as evidenced by above chance accuracy scores. Perceptual accuracy improved significantly during the enhanced relative to normal stimulation, which was associated with faster stimulation detection and reduced reaction time variability. Capsule stimulation induced late neural responses in parieto-occipital electrodes near the midline. Moreover, these ‘gastric evoked potentials’ showed intensity-dependent increases in amplitude and were significantly correlated with perceptual accuracy. Our results replicated in a separate experiment, and abdominal X-ray imaging localized most capsule stimulations to the gastroduodenal segments. Combined with our prior observation that a Bayesian model is capable of estimating computational parameters of gut-brain mechanosensation, these findings highlight a unique form of enterically-focused sensory monitoring within the human brain, with implications for understanding gut feelings and gut-brain interactions in healthy and clinical populations. Nature Publishing Group UK 2023-06-13 /pmc/articles/PMC10264354/ /pubmed/37311748 http://dx.doi.org/10.1038/s41467-023-39058-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Mayeli, Ahmad
Al Zoubi, Obada
White, Evan J.
Chappelle, Sheridan
Kuplicki, Rayus
Morton, Alexa
Bruce, Jaimee
Smith, Ryan
Feinstein, Justin S.
Bodurka, Jerzy
Paulus, Martin P.
Khalsa, Sahib S.
Parieto-occipital ERP indicators of gut mechanosensation in humans
title Parieto-occipital ERP indicators of gut mechanosensation in humans
title_full Parieto-occipital ERP indicators of gut mechanosensation in humans
title_fullStr Parieto-occipital ERP indicators of gut mechanosensation in humans
title_full_unstemmed Parieto-occipital ERP indicators of gut mechanosensation in humans
title_short Parieto-occipital ERP indicators of gut mechanosensation in humans
title_sort parieto-occipital erp indicators of gut mechanosensation in humans
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10264354/
https://www.ncbi.nlm.nih.gov/pubmed/37311748
http://dx.doi.org/10.1038/s41467-023-39058-4
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