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Integrating multimodal and multiscale connectivity blueprints of the human cerebral cortex in health and disease

The brain is composed of disparate neural populations that communicate and interact with one another. Although fiber bundles, similarities in molecular architecture, and synchronized neural activity all reflect how brain regions potentially interact with one another, a comprehensive study of how all...

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Autores principales: Hansen, Justine Y., Shafiei, Golia, Voigt, Katharina, Liang, Emma X., Cox, Sylvia M. L., Leyton, Marco, Jamadar, Sharna D., Misic, Bratislav
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10553842/
https://www.ncbi.nlm.nih.gov/pubmed/37747886
http://dx.doi.org/10.1371/journal.pbio.3002314
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author Hansen, Justine Y.
Shafiei, Golia
Voigt, Katharina
Liang, Emma X.
Cox, Sylvia M. L.
Leyton, Marco
Jamadar, Sharna D.
Misic, Bratislav
author_facet Hansen, Justine Y.
Shafiei, Golia
Voigt, Katharina
Liang, Emma X.
Cox, Sylvia M. L.
Leyton, Marco
Jamadar, Sharna D.
Misic, Bratislav
author_sort Hansen, Justine Y.
collection PubMed
description The brain is composed of disparate neural populations that communicate and interact with one another. Although fiber bundles, similarities in molecular architecture, and synchronized neural activity all reflect how brain regions potentially interact with one another, a comprehensive study of how all these interregional relationships jointly reflect brain structure and function remains missing. Here, we systematically integrate 7 multimodal, multiscale types of interregional similarity (“connectivity modes”) derived from gene expression, neurotransmitter receptor density, cellular morphology, glucose metabolism, haemodynamic activity, and electrophysiology in humans. We first show that for all connectivity modes, feature similarity decreases with distance and increases when regions are structurally connected. Next, we show that connectivity modes exhibit unique and diverse connection patterns, hub profiles, spatial gradients, and modular organization. Throughout, we observe a consistent primacy of molecular connectivity modes—namely correlated gene expression and receptor similarity—that map onto multiple phenomena, including the rich club and patterns of abnormal cortical thickness across 13 neurological, psychiatric, and neurodevelopmental disorders. Finally, to construct a single multimodal wiring map of the human cortex, we fuse all 7 connectivity modes and show that the fused network maps onto major organizational features of the cortex including structural connectivity, intrinsic functional networks, and cytoarchitectonic classes. Altogether, this work contributes to the integrative study of interregional relationships in the human cerebral cortex.
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spelling pubmed-105538422023-10-06 Integrating multimodal and multiscale connectivity blueprints of the human cerebral cortex in health and disease Hansen, Justine Y. Shafiei, Golia Voigt, Katharina Liang, Emma X. Cox, Sylvia M. L. Leyton, Marco Jamadar, Sharna D. Misic, Bratislav PLoS Biol Research Article The brain is composed of disparate neural populations that communicate and interact with one another. Although fiber bundles, similarities in molecular architecture, and synchronized neural activity all reflect how brain regions potentially interact with one another, a comprehensive study of how all these interregional relationships jointly reflect brain structure and function remains missing. Here, we systematically integrate 7 multimodal, multiscale types of interregional similarity (“connectivity modes”) derived from gene expression, neurotransmitter receptor density, cellular morphology, glucose metabolism, haemodynamic activity, and electrophysiology in humans. We first show that for all connectivity modes, feature similarity decreases with distance and increases when regions are structurally connected. Next, we show that connectivity modes exhibit unique and diverse connection patterns, hub profiles, spatial gradients, and modular organization. Throughout, we observe a consistent primacy of molecular connectivity modes—namely correlated gene expression and receptor similarity—that map onto multiple phenomena, including the rich club and patterns of abnormal cortical thickness across 13 neurological, psychiatric, and neurodevelopmental disorders. Finally, to construct a single multimodal wiring map of the human cortex, we fuse all 7 connectivity modes and show that the fused network maps onto major organizational features of the cortex including structural connectivity, intrinsic functional networks, and cytoarchitectonic classes. Altogether, this work contributes to the integrative study of interregional relationships in the human cerebral cortex. Public Library of Science 2023-09-25 /pmc/articles/PMC10553842/ /pubmed/37747886 http://dx.doi.org/10.1371/journal.pbio.3002314 Text en © 2023 Hansen et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://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
Hansen, Justine Y.
Shafiei, Golia
Voigt, Katharina
Liang, Emma X.
Cox, Sylvia M. L.
Leyton, Marco
Jamadar, Sharna D.
Misic, Bratislav
Integrating multimodal and multiscale connectivity blueprints of the human cerebral cortex in health and disease
title Integrating multimodal and multiscale connectivity blueprints of the human cerebral cortex in health and disease
title_full Integrating multimodal and multiscale connectivity blueprints of the human cerebral cortex in health and disease
title_fullStr Integrating multimodal and multiscale connectivity blueprints of the human cerebral cortex in health and disease
title_full_unstemmed Integrating multimodal and multiscale connectivity blueprints of the human cerebral cortex in health and disease
title_short Integrating multimodal and multiscale connectivity blueprints of the human cerebral cortex in health and disease
title_sort integrating multimodal and multiscale connectivity blueprints of the human cerebral cortex in health and disease
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10553842/
https://www.ncbi.nlm.nih.gov/pubmed/37747886
http://dx.doi.org/10.1371/journal.pbio.3002314
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