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Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects

OBJECTIVE: A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and disease, including hedonic food intake and obesity. We performed a tripartite network analysis based on graph theory to test the hypothesis that...

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Autores principales: Osadchiy, Vadim, Labus, Jennifer S., Gupta, Arpana, Jacobs, Jonathan, Ashe-McNalley, Cody, Hsiao, Elaine Y., Mayer, Emeran A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6078307/
https://www.ncbi.nlm.nih.gov/pubmed/30080865
http://dx.doi.org/10.1371/journal.pone.0201772
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author Osadchiy, Vadim
Labus, Jennifer S.
Gupta, Arpana
Jacobs, Jonathan
Ashe-McNalley, Cody
Hsiao, Elaine Y.
Mayer, Emeran A.
author_facet Osadchiy, Vadim
Labus, Jennifer S.
Gupta, Arpana
Jacobs, Jonathan
Ashe-McNalley, Cody
Hsiao, Elaine Y.
Mayer, Emeran A.
author_sort Osadchiy, Vadim
collection PubMed
description OBJECTIVE: A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and disease, including hedonic food intake and obesity. We performed a tripartite network analysis based on graph theory to test the hypothesis that microbiota-derived fecal metabolites are associated with connectivity of key regions of the brain’s extended reward network and clinical measures related to obesity. METHODS: DTI and resting state fMRI imaging was obtained from 63 healthy subjects with and without elevated body mass index (BMI) (29 males and 34 females). Subjects submitted fecal samples, completed questionnaires to assess anxiety and food addiction, and BMI was recorded. RESULTS: The study results demonstrate associations between fecal microbiota-derived indole metabolites (indole, indoleacetic acid, and skatole) with measures of functional and anatomical connectivity of the amygdala, nucleus accumbens, and anterior insula, in addition to BMI, food addiction scores (YFAS) and anxiety symptom scores (HAD Anxiety). CONCLUSIONS: The findings support the hypothesis that gut microbiota-derived indole metabolites may influence hedonic food intake and obesity by acting on the extended reward network, specifically the amygdala-nucleus accumbens circuit and the amygdala-anterior insula circuit. These cross sectional, data-driven results provide valuable information for future mechanistic studies.
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spelling pubmed-60783072018-08-28 Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects Osadchiy, Vadim Labus, Jennifer S. Gupta, Arpana Jacobs, Jonathan Ashe-McNalley, Cody Hsiao, Elaine Y. Mayer, Emeran A. PLoS One Research Article OBJECTIVE: A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and disease, including hedonic food intake and obesity. We performed a tripartite network analysis based on graph theory to test the hypothesis that microbiota-derived fecal metabolites are associated with connectivity of key regions of the brain’s extended reward network and clinical measures related to obesity. METHODS: DTI and resting state fMRI imaging was obtained from 63 healthy subjects with and without elevated body mass index (BMI) (29 males and 34 females). Subjects submitted fecal samples, completed questionnaires to assess anxiety and food addiction, and BMI was recorded. RESULTS: The study results demonstrate associations between fecal microbiota-derived indole metabolites (indole, indoleacetic acid, and skatole) with measures of functional and anatomical connectivity of the amygdala, nucleus accumbens, and anterior insula, in addition to BMI, food addiction scores (YFAS) and anxiety symptom scores (HAD Anxiety). CONCLUSIONS: The findings support the hypothesis that gut microbiota-derived indole metabolites may influence hedonic food intake and obesity by acting on the extended reward network, specifically the amygdala-nucleus accumbens circuit and the amygdala-anterior insula circuit. These cross sectional, data-driven results provide valuable information for future mechanistic studies. Public Library of Science 2018-08-06 /pmc/articles/PMC6078307/ /pubmed/30080865 http://dx.doi.org/10.1371/journal.pone.0201772 Text en © 2018 Osadchiy et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Osadchiy, Vadim
Labus, Jennifer S.
Gupta, Arpana
Jacobs, Jonathan
Ashe-McNalley, Cody
Hsiao, Elaine Y.
Mayer, Emeran A.
Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects
title Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects
title_full Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects
title_fullStr Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects
title_full_unstemmed Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects
title_short Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects
title_sort correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6078307/
https://www.ncbi.nlm.nih.gov/pubmed/30080865
http://dx.doi.org/10.1371/journal.pone.0201772
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