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Functional brain rewiring and altered cortical stability in ulcerative colitis

Despite recent advances, there is still a major need to better understand the interactions between brain function and chronic gut inflammation and its clinical implications. Alterations in executive function have previously been identified in several chronic inflammatory conditions, including inflam...

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Autores principales: Wang, Hao, Labus, Jennifer S., Griffin, Fiona, Gupta, Arpana, Bhatt, Ravi R., Sauk, Jenny S., Turkiewicz, Joanna, Bernstein, Charles N., Kornelsen, Jennifer, Mayer, Emeran A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9095465/
https://www.ncbi.nlm.nih.gov/pubmed/35046525
http://dx.doi.org/10.1038/s41380-021-01421-6
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author Wang, Hao
Labus, Jennifer S.
Griffin, Fiona
Gupta, Arpana
Bhatt, Ravi R.
Sauk, Jenny S.
Turkiewicz, Joanna
Bernstein, Charles N.
Kornelsen, Jennifer
Mayer, Emeran A.
author_facet Wang, Hao
Labus, Jennifer S.
Griffin, Fiona
Gupta, Arpana
Bhatt, Ravi R.
Sauk, Jenny S.
Turkiewicz, Joanna
Bernstein, Charles N.
Kornelsen, Jennifer
Mayer, Emeran A.
author_sort Wang, Hao
collection PubMed
description Despite recent advances, there is still a major need to better understand the interactions between brain function and chronic gut inflammation and its clinical implications. Alterations in executive function have previously been identified in several chronic inflammatory conditions, including inflammatory bowel diseases. Inflammation-associated brain alterations can be captured by connectome analysis. Here, we used the resting-state fMRI data from 222 participants comprising three groups (ulcerative colitis (UC), irritable bowel syndrome (IBS), and healthy controls (HC), N = 74 each) to investigate the alterations in functional brain wiring and cortical stability in UC compared to the two control groups and identify possible correlations of these alterations with clinical parameters. Globally, UC participants showed increased functional connectivity and decreased modularity compared to IBS and HC groups. Regionally, UC showed decreased eigenvector centrality in the executive control network (UC < IBS < HC) and increased eigenvector centrality in the visual network (UC > IBS > HC). UC also showed increased connectivity in dorsal attention, somatomotor network, and visual networks, and these enhanced subnetwork connectivities were able to distinguish UC participants from HCs and IBS with high accuracy. Dynamic functional connectome analysis revealed that UC showed enhanced cortical stability in the medial prefrontal cortex (mPFC), which correlated with severe depression and anxiety-related measures. None of the observed brain changes were correlated with disease duration. Together, these findings are consistent with compromised functioning of networks involved in executive function and sensory integration in UC.
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spelling pubmed-90954652022-05-13 Functional brain rewiring and altered cortical stability in ulcerative colitis Wang, Hao Labus, Jennifer S. Griffin, Fiona Gupta, Arpana Bhatt, Ravi R. Sauk, Jenny S. Turkiewicz, Joanna Bernstein, Charles N. Kornelsen, Jennifer Mayer, Emeran A. Mol Psychiatry Article Despite recent advances, there is still a major need to better understand the interactions between brain function and chronic gut inflammation and its clinical implications. Alterations in executive function have previously been identified in several chronic inflammatory conditions, including inflammatory bowel diseases. Inflammation-associated brain alterations can be captured by connectome analysis. Here, we used the resting-state fMRI data from 222 participants comprising three groups (ulcerative colitis (UC), irritable bowel syndrome (IBS), and healthy controls (HC), N = 74 each) to investigate the alterations in functional brain wiring and cortical stability in UC compared to the two control groups and identify possible correlations of these alterations with clinical parameters. Globally, UC participants showed increased functional connectivity and decreased modularity compared to IBS and HC groups. Regionally, UC showed decreased eigenvector centrality in the executive control network (UC < IBS < HC) and increased eigenvector centrality in the visual network (UC > IBS > HC). UC also showed increased connectivity in dorsal attention, somatomotor network, and visual networks, and these enhanced subnetwork connectivities were able to distinguish UC participants from HCs and IBS with high accuracy. Dynamic functional connectome analysis revealed that UC showed enhanced cortical stability in the medial prefrontal cortex (mPFC), which correlated with severe depression and anxiety-related measures. None of the observed brain changes were correlated with disease duration. Together, these findings are consistent with compromised functioning of networks involved in executive function and sensory integration in UC. Nature Publishing Group UK 2022-01-19 2022 /pmc/articles/PMC9095465/ /pubmed/35046525 http://dx.doi.org/10.1038/s41380-021-01421-6 Text en © The Author(s) 2021 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
Wang, Hao
Labus, Jennifer S.
Griffin, Fiona
Gupta, Arpana
Bhatt, Ravi R.
Sauk, Jenny S.
Turkiewicz, Joanna
Bernstein, Charles N.
Kornelsen, Jennifer
Mayer, Emeran A.
Functional brain rewiring and altered cortical stability in ulcerative colitis
title Functional brain rewiring and altered cortical stability in ulcerative colitis
title_full Functional brain rewiring and altered cortical stability in ulcerative colitis
title_fullStr Functional brain rewiring and altered cortical stability in ulcerative colitis
title_full_unstemmed Functional brain rewiring and altered cortical stability in ulcerative colitis
title_short Functional brain rewiring and altered cortical stability in ulcerative colitis
title_sort functional brain rewiring and altered cortical stability in ulcerative colitis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9095465/
https://www.ncbi.nlm.nih.gov/pubmed/35046525
http://dx.doi.org/10.1038/s41380-021-01421-6
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