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Reorganization of brain structural networks in aging: A longitudinal study

Normal aging is characterized by structural and functional changes in the brain contributing to cognitive decline. Structural connectivity (SC) describes the anatomical backbone linking distinct functional subunits of the brain and disruption of this communication is thought to be one of the potenti...

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Autores principales: Coelho, Ana, Fernandes, Henrique M., Magalhães, Ricardo, Moreira, Pedro S., Marques, Paulo, Soares, José M., Amorim, Liliana, Portugal‐Nunes, Carlos, Castanho, Teresa, Santos, Nadine Correia, Sousa, Nuno
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8248023/
https://www.ncbi.nlm.nih.gov/pubmed/33527512
http://dx.doi.org/10.1002/jnr.24795
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author Coelho, Ana
Fernandes, Henrique M.
Magalhães, Ricardo
Moreira, Pedro S.
Marques, Paulo
Soares, José M.
Amorim, Liliana
Portugal‐Nunes, Carlos
Castanho, Teresa
Santos, Nadine Correia
Sousa, Nuno
author_facet Coelho, Ana
Fernandes, Henrique M.
Magalhães, Ricardo
Moreira, Pedro S.
Marques, Paulo
Soares, José M.
Amorim, Liliana
Portugal‐Nunes, Carlos
Castanho, Teresa
Santos, Nadine Correia
Sousa, Nuno
author_sort Coelho, Ana
collection PubMed
description Normal aging is characterized by structural and functional changes in the brain contributing to cognitive decline. Structural connectivity (SC) describes the anatomical backbone linking distinct functional subunits of the brain and disruption of this communication is thought to be one of the potential contributors for the age‐related deterioration observed in cognition. Several studies already explored brain network's reorganization during aging, but most focused on average connectivity of the whole‐brain or in specific networks, such as the resting‐state networks. Here, we aimed to characterize longitudinal changes of white matter (WM) structural brain networks, through the identification of sub‐networks with significantly altered connectivity along time. Then, we tested associations between longitudinal changes in network connectivity and cognition. We also assessed longitudinal changes in topological properties of the networks. For this, older adults were evaluated at two timepoints, with a mean interval time of 52.8 months (SD = 7.24). WM structural networks were derived from diffusion magnetic resonance imaging, and cognitive status from neurocognitive testing. Our results show age‐related changes in brain SC, characterized by both decreases and increases in connectivity weight. Interestingly, decreases occur in intra‐hemispheric connections formed mainly by association fibers, while increases occur mostly in inter‐hemispheric connections and involve association, commissural, and projection fibers, supporting the last‐in‐first‐out hypothesis. Regarding topology, two hubs were lost, alongside with a decrease in connector‐hub inter‐modular connectivity, reflecting reduced integration. Simultaneously, there was an increase in the number of provincial hubs, suggesting increased segregation. Overall, these results confirm that aging triggers a reorganization of the brain structural network.
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spelling pubmed-82480232021-07-02 Reorganization of brain structural networks in aging: A longitudinal study Coelho, Ana Fernandes, Henrique M. Magalhães, Ricardo Moreira, Pedro S. Marques, Paulo Soares, José M. Amorim, Liliana Portugal‐Nunes, Carlos Castanho, Teresa Santos, Nadine Correia Sousa, Nuno J Neurosci Res Research Articles Normal aging is characterized by structural and functional changes in the brain contributing to cognitive decline. Structural connectivity (SC) describes the anatomical backbone linking distinct functional subunits of the brain and disruption of this communication is thought to be one of the potential contributors for the age‐related deterioration observed in cognition. Several studies already explored brain network's reorganization during aging, but most focused on average connectivity of the whole‐brain or in specific networks, such as the resting‐state networks. Here, we aimed to characterize longitudinal changes of white matter (WM) structural brain networks, through the identification of sub‐networks with significantly altered connectivity along time. Then, we tested associations between longitudinal changes in network connectivity and cognition. We also assessed longitudinal changes in topological properties of the networks. For this, older adults were evaluated at two timepoints, with a mean interval time of 52.8 months (SD = 7.24). WM structural networks were derived from diffusion magnetic resonance imaging, and cognitive status from neurocognitive testing. Our results show age‐related changes in brain SC, characterized by both decreases and increases in connectivity weight. Interestingly, decreases occur in intra‐hemispheric connections formed mainly by association fibers, while increases occur mostly in inter‐hemispheric connections and involve association, commissural, and projection fibers, supporting the last‐in‐first‐out hypothesis. Regarding topology, two hubs were lost, alongside with a decrease in connector‐hub inter‐modular connectivity, reflecting reduced integration. Simultaneously, there was an increase in the number of provincial hubs, suggesting increased segregation. Overall, these results confirm that aging triggers a reorganization of the brain structural network. John Wiley and Sons Inc. 2021-02-02 2021-05 /pmc/articles/PMC8248023/ /pubmed/33527512 http://dx.doi.org/10.1002/jnr.24795 Text en © 2021 The Authors. Journal of Neuroscience Research published by Wiley Periodicals LLC https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Coelho, Ana
Fernandes, Henrique M.
Magalhães, Ricardo
Moreira, Pedro S.
Marques, Paulo
Soares, José M.
Amorim, Liliana
Portugal‐Nunes, Carlos
Castanho, Teresa
Santos, Nadine Correia
Sousa, Nuno
Reorganization of brain structural networks in aging: A longitudinal study
title Reorganization of brain structural networks in aging: A longitudinal study
title_full Reorganization of brain structural networks in aging: A longitudinal study
title_fullStr Reorganization of brain structural networks in aging: A longitudinal study
title_full_unstemmed Reorganization of brain structural networks in aging: A longitudinal study
title_short Reorganization of brain structural networks in aging: A longitudinal study
title_sort reorganization of brain structural networks in aging: a longitudinal study
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8248023/
https://www.ncbi.nlm.nih.gov/pubmed/33527512
http://dx.doi.org/10.1002/jnr.24795
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