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Aging Impacts the Overall Connectivity Strength of Regions Critical for Information Transfer Among Brain Networks

Recent studies have demonstrated that connector hubs, regions considered critical for the flow of information across neural systems, are mostly involved in neurodegenerative dementia. Considering that aging can significantly affect the brain’s intrinsic connectivity, identifying aging’s impact on th...

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Autores principales: Bagarinao, Epifanio, Watanabe, Hirohisa, Maesawa, Satoshi, Mori, Daisuke, Hara, Kazuhiro, Kawabata, Kazuya, Yoneyama, Noritaka, Ohdake, Reiko, Imai, Kazunori, Masuda, Michihito, Yokoi, Takamasa, Ogura, Aya, Taoka, Toshiaki, Koyama, Shuji, Tanabe, Hiroki C., Katsuno, Masahisa, Wakabayashi, Toshihiko, Kuzuya, Masafumi, Hoshiyama, Minoru, Isoda, Haruo, Naganawa, Shinji, Ozaki, Norio, Sobue, Gen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7655963/
https://www.ncbi.nlm.nih.gov/pubmed/33192489
http://dx.doi.org/10.3389/fnagi.2020.592469
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author Bagarinao, Epifanio
Watanabe, Hirohisa
Maesawa, Satoshi
Mori, Daisuke
Hara, Kazuhiro
Kawabata, Kazuya
Yoneyama, Noritaka
Ohdake, Reiko
Imai, Kazunori
Masuda, Michihito
Yokoi, Takamasa
Ogura, Aya
Taoka, Toshiaki
Koyama, Shuji
Tanabe, Hiroki C.
Katsuno, Masahisa
Wakabayashi, Toshihiko
Kuzuya, Masafumi
Hoshiyama, Minoru
Isoda, Haruo
Naganawa, Shinji
Ozaki, Norio
Sobue, Gen
author_facet Bagarinao, Epifanio
Watanabe, Hirohisa
Maesawa, Satoshi
Mori, Daisuke
Hara, Kazuhiro
Kawabata, Kazuya
Yoneyama, Noritaka
Ohdake, Reiko
Imai, Kazunori
Masuda, Michihito
Yokoi, Takamasa
Ogura, Aya
Taoka, Toshiaki
Koyama, Shuji
Tanabe, Hiroki C.
Katsuno, Masahisa
Wakabayashi, Toshihiko
Kuzuya, Masafumi
Hoshiyama, Minoru
Isoda, Haruo
Naganawa, Shinji
Ozaki, Norio
Sobue, Gen
author_sort Bagarinao, Epifanio
collection PubMed
description Recent studies have demonstrated that connector hubs, regions considered critical for the flow of information across neural systems, are mostly involved in neurodegenerative dementia. Considering that aging can significantly affect the brain’s intrinsic connectivity, identifying aging’s impact on these regions’ overall connection strength is important to differentiate changes associated with healthy aging from neurodegenerative disorders. Using resting state functional magnetic resonance imaging data from a carefully selected cohort of 175 healthy volunteers aging from 21 to 86 years old, we computed an intrinsic connectivity contrast (ICC) metric, which quantifies a region’s overall connectivity strength, for whole brain, short-range, and long-range connections and examined age-related changes of this metric over the adult lifespan. We have identified a limited number of hub regions with ICC values that showed significant negative relationship with age. These include the medial precentral/midcingulate gyri and insula with both their short-range and long-range (and thus whole-brain) ICC values negatively associated with age, and the angular, middle frontal, and posterior cingulate gyri with their long-range ICC values mainly involved. Seed-based connectivity analyses further confirmed that these regions are connector hubs with connectivity profile that strongly overlapped with multiple large-scale brain networks. General cognitive performance was not associated with these hubs’ ICC values. These findings suggest that even healthy aging could negatively impact the efficiency of regions critical for facilitating information transfer among different functional brain networks. The extent of the regions involved, however, was limited.
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spelling pubmed-76559632020-11-13 Aging Impacts the Overall Connectivity Strength of Regions Critical for Information Transfer Among Brain Networks Bagarinao, Epifanio Watanabe, Hirohisa Maesawa, Satoshi Mori, Daisuke Hara, Kazuhiro Kawabata, Kazuya Yoneyama, Noritaka Ohdake, Reiko Imai, Kazunori Masuda, Michihito Yokoi, Takamasa Ogura, Aya Taoka, Toshiaki Koyama, Shuji Tanabe, Hiroki C. Katsuno, Masahisa Wakabayashi, Toshihiko Kuzuya, Masafumi Hoshiyama, Minoru Isoda, Haruo Naganawa, Shinji Ozaki, Norio Sobue, Gen Front Aging Neurosci Neuroscience Recent studies have demonstrated that connector hubs, regions considered critical for the flow of information across neural systems, are mostly involved in neurodegenerative dementia. Considering that aging can significantly affect the brain’s intrinsic connectivity, identifying aging’s impact on these regions’ overall connection strength is important to differentiate changes associated with healthy aging from neurodegenerative disorders. Using resting state functional magnetic resonance imaging data from a carefully selected cohort of 175 healthy volunteers aging from 21 to 86 years old, we computed an intrinsic connectivity contrast (ICC) metric, which quantifies a region’s overall connectivity strength, for whole brain, short-range, and long-range connections and examined age-related changes of this metric over the adult lifespan. We have identified a limited number of hub regions with ICC values that showed significant negative relationship with age. These include the medial precentral/midcingulate gyri and insula with both their short-range and long-range (and thus whole-brain) ICC values negatively associated with age, and the angular, middle frontal, and posterior cingulate gyri with their long-range ICC values mainly involved. Seed-based connectivity analyses further confirmed that these regions are connector hubs with connectivity profile that strongly overlapped with multiple large-scale brain networks. General cognitive performance was not associated with these hubs’ ICC values. These findings suggest that even healthy aging could negatively impact the efficiency of regions critical for facilitating information transfer among different functional brain networks. The extent of the regions involved, however, was limited. Frontiers Media S.A. 2020-10-28 /pmc/articles/PMC7655963/ /pubmed/33192489 http://dx.doi.org/10.3389/fnagi.2020.592469 Text en Copyright © 2020 Bagarinao, Watanabe, Maesawa, Mori, Hara, Kawabata, Yoneyama, Ohdake, Imai, Masuda, Yokoi, Ogura, Taoka, Koyama, Tanabe, Katsuno, Wakabayashi, Kuzuya, Hoshiyama, Isoda, Naganawa, Ozaki and Sobue. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Bagarinao, Epifanio
Watanabe, Hirohisa
Maesawa, Satoshi
Mori, Daisuke
Hara, Kazuhiro
Kawabata, Kazuya
Yoneyama, Noritaka
Ohdake, Reiko
Imai, Kazunori
Masuda, Michihito
Yokoi, Takamasa
Ogura, Aya
Taoka, Toshiaki
Koyama, Shuji
Tanabe, Hiroki C.
Katsuno, Masahisa
Wakabayashi, Toshihiko
Kuzuya, Masafumi
Hoshiyama, Minoru
Isoda, Haruo
Naganawa, Shinji
Ozaki, Norio
Sobue, Gen
Aging Impacts the Overall Connectivity Strength of Regions Critical for Information Transfer Among Brain Networks
title Aging Impacts the Overall Connectivity Strength of Regions Critical for Information Transfer Among Brain Networks
title_full Aging Impacts the Overall Connectivity Strength of Regions Critical for Information Transfer Among Brain Networks
title_fullStr Aging Impacts the Overall Connectivity Strength of Regions Critical for Information Transfer Among Brain Networks
title_full_unstemmed Aging Impacts the Overall Connectivity Strength of Regions Critical for Information Transfer Among Brain Networks
title_short Aging Impacts the Overall Connectivity Strength of Regions Critical for Information Transfer Among Brain Networks
title_sort aging impacts the overall connectivity strength of regions critical for information transfer among brain networks
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7655963/
https://www.ncbi.nlm.nih.gov/pubmed/33192489
http://dx.doi.org/10.3389/fnagi.2020.592469
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