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Longitudinal association of executive function and structural network controllability in the aging brain
Executive function encompasses effortful cognitive processes that are particularly susceptible to aging. Functional brain networks supporting executive function—such as the frontoparietal control network and the multiple demand system—have been extensively investigated. However, it remains unclear h...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Springer International Publishing
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9886719/ https://www.ncbi.nlm.nih.gov/pubmed/36269506 http://dx.doi.org/10.1007/s11357-022-00676-3 |
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author | Tang, Rongxiang Elman, Jeremy A. Franz, Carol E. Dale, Anders M. Eyler, Lisa T. Fennema-Notestine, Christine Hagler, Donald J. Lyons, Michael J. Panizzon, Matthew S. Puckett, Olivia K. Kremen, William S. |
author_facet | Tang, Rongxiang Elman, Jeremy A. Franz, Carol E. Dale, Anders M. Eyler, Lisa T. Fennema-Notestine, Christine Hagler, Donald J. Lyons, Michael J. Panizzon, Matthew S. Puckett, Olivia K. Kremen, William S. |
author_sort | Tang, Rongxiang |
collection | PubMed |
description | Executive function encompasses effortful cognitive processes that are particularly susceptible to aging. Functional brain networks supporting executive function—such as the frontoparietal control network and the multiple demand system—have been extensively investigated. However, it remains unclear how structural networks facilitate and constrain the dynamics of functional networks to contribute to aging-related executive function declines. We examined whether changes in structural network modal controllability—a network’s ability to facilitate effortful brain state transitions that support cognitive functions—are associated with changes in executive function cross-sectionally and longitudinally. Diffusion-weighted imaging and neuropsychological testing were conducted at two time points (Time 1: ages 56 to 66, N = 172; Time 2: ages 61 to 70, N = 267) in community-dwelling men from the Vietnam Era Twin Study of Aging. An executive function factor score was computed from six neuropsychological tasks. Structural networks constructed from white matter connectivity were used to estimate modal controllability in control network and multiple demand system. We showed that higher modal controllability in control network and multiple demand system was associated with better executive function at Time 2, after controlling for age, young adult general cognitive ability, and physical health status. Moreover, changes in executive function over a period of 5 to 6 years (Time 1-Time 2, N = 105) were associated with changes in modal controllability of the multiple demand system and weakly in the control network over the same time period. These findings suggest that changes in the ability of structural brain networks in facilitating effortful brain state transitions may be a key neural mechanism underlying aging-related executive function declines and cognitive aging. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11357-022-00676-3. |
format | Online Article Text |
id | pubmed-9886719 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Springer International Publishing |
record_format | MEDLINE/PubMed |
spelling | pubmed-98867192023-02-01 Longitudinal association of executive function and structural network controllability in the aging brain Tang, Rongxiang Elman, Jeremy A. Franz, Carol E. Dale, Anders M. Eyler, Lisa T. Fennema-Notestine, Christine Hagler, Donald J. Lyons, Michael J. Panizzon, Matthew S. Puckett, Olivia K. Kremen, William S. GeroScience Original Article Executive function encompasses effortful cognitive processes that are particularly susceptible to aging. Functional brain networks supporting executive function—such as the frontoparietal control network and the multiple demand system—have been extensively investigated. However, it remains unclear how structural networks facilitate and constrain the dynamics of functional networks to contribute to aging-related executive function declines. We examined whether changes in structural network modal controllability—a network’s ability to facilitate effortful brain state transitions that support cognitive functions—are associated with changes in executive function cross-sectionally and longitudinally. Diffusion-weighted imaging and neuropsychological testing were conducted at two time points (Time 1: ages 56 to 66, N = 172; Time 2: ages 61 to 70, N = 267) in community-dwelling men from the Vietnam Era Twin Study of Aging. An executive function factor score was computed from six neuropsychological tasks. Structural networks constructed from white matter connectivity were used to estimate modal controllability in control network and multiple demand system. We showed that higher modal controllability in control network and multiple demand system was associated with better executive function at Time 2, after controlling for age, young adult general cognitive ability, and physical health status. Moreover, changes in executive function over a period of 5 to 6 years (Time 1-Time 2, N = 105) were associated with changes in modal controllability of the multiple demand system and weakly in the control network over the same time period. These findings suggest that changes in the ability of structural brain networks in facilitating effortful brain state transitions may be a key neural mechanism underlying aging-related executive function declines and cognitive aging. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11357-022-00676-3. Springer International Publishing 2022-10-21 /pmc/articles/PMC9886719/ /pubmed/36269506 http://dx.doi.org/10.1007/s11357-022-00676-3 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Original Article Tang, Rongxiang Elman, Jeremy A. Franz, Carol E. Dale, Anders M. Eyler, Lisa T. Fennema-Notestine, Christine Hagler, Donald J. Lyons, Michael J. Panizzon, Matthew S. Puckett, Olivia K. Kremen, William S. Longitudinal association of executive function and structural network controllability in the aging brain |
title | Longitudinal association of executive function and structural network controllability in the aging brain |
title_full | Longitudinal association of executive function and structural network controllability in the aging brain |
title_fullStr | Longitudinal association of executive function and structural network controllability in the aging brain |
title_full_unstemmed | Longitudinal association of executive function and structural network controllability in the aging brain |
title_short | Longitudinal association of executive function and structural network controllability in the aging brain |
title_sort | longitudinal association of executive function and structural network controllability in the aging brain |
topic | Original Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9886719/ https://www.ncbi.nlm.nih.gov/pubmed/36269506 http://dx.doi.org/10.1007/s11357-022-00676-3 |
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