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The left frontal cortex supports reserve in aging by enhancing functional network efficiency

BACKGROUND: Recent evidence derived from functional magnetic resonance imaging (fMRI) studies suggests that functional hubs (i.e., highly connected brain regions) are important for mental health. We found recently that global connectivity of a hub in the left frontal cortex (LFC connectivity) is ass...

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Autores principales: Franzmeier, Nicolai, Hartmann, Julia, Taylor, Alexander N. W., Araque-Caballero, Miguel Á., Simon-Vermot, Lee, Kambeitz-Ilankovic, Lana, Bürger, Katharina, Catak, Cihan, Janowitz, Daniel, Müller, Claudia, Ertl-Wagner, Birgit, Stahl, Robert, Dichgans, Martin, Duering, Marco, Ewers, Michael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5838935/
https://www.ncbi.nlm.nih.gov/pubmed/29510747
http://dx.doi.org/10.1186/s13195-018-0358-y
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author Franzmeier, Nicolai
Hartmann, Julia
Taylor, Alexander N. W.
Araque-Caballero, Miguel Á.
Simon-Vermot, Lee
Kambeitz-Ilankovic, Lana
Bürger, Katharina
Catak, Cihan
Janowitz, Daniel
Müller, Claudia
Ertl-Wagner, Birgit
Stahl, Robert
Dichgans, Martin
Duering, Marco
Ewers, Michael
author_facet Franzmeier, Nicolai
Hartmann, Julia
Taylor, Alexander N. W.
Araque-Caballero, Miguel Á.
Simon-Vermot, Lee
Kambeitz-Ilankovic, Lana
Bürger, Katharina
Catak, Cihan
Janowitz, Daniel
Müller, Claudia
Ertl-Wagner, Birgit
Stahl, Robert
Dichgans, Martin
Duering, Marco
Ewers, Michael
author_sort Franzmeier, Nicolai
collection PubMed
description BACKGROUND: Recent evidence derived from functional magnetic resonance imaging (fMRI) studies suggests that functional hubs (i.e., highly connected brain regions) are important for mental health. We found recently that global connectivity of a hub in the left frontal cortex (LFC connectivity) is associated with relatively preserved memory abilities and higher levels of protective factors (education, IQ) in normal aging and Alzheimer’s disease. These results suggest that LFC connectivity supports reserve capacity, alleviating memory decline. An open question, however, is why LFC connectivity is beneficial and supports memory function in the face of neurodegeneration. We hypothesized that higher LFC connectivity is associated with enhanced efficiency in connected major networks involved in episodic memory. We further hypothesized that higher LFC-related network efficiency predicts higher memory abilities. METHODS: We assessed fMRI during a face-name association learning task performed by 26 healthy, cognitively normal elderly participants. Using beta-series correlation analysis, we computed task-related LFC connectivity to key memory networks, including the default mode network (DMN) and dorsal attention network (DAN). Network efficiency within the DMN and DAN was estimated by the graph theoretical small-worldness statistic. We applied linear regression analyses to test the association between LFC connectivity with the DMN/DAN and small-worldness of these networks. Mediation analysis was applied to test LFC connectivity to the DMN and DAN as a mediator of the association between education and higher DMN and DAN small-worldness. Last, we tested network small-worldness as a predictor of memory performance. RESULTS: We found that higher LFC connectivity to the DMN and DAN during successful memory encoding and recognition was associated with higher small-worldness of those networks. Higher task-related LFC connectivity mediated the association between education and higher small-worldness in the DMN and DAN. Further, higher small-worldness of these networks predicted better performance in the memory task. CONCLUSIONS: The present results suggest that higher education-related LFC connectivity to key memory networks during a memory task is associated with higher network efficiency and thus enhanced reserve of memory abilities in aging. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13195-018-0358-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-58389352018-03-09 The left frontal cortex supports reserve in aging by enhancing functional network efficiency Franzmeier, Nicolai Hartmann, Julia Taylor, Alexander N. W. Araque-Caballero, Miguel Á. Simon-Vermot, Lee Kambeitz-Ilankovic, Lana Bürger, Katharina Catak, Cihan Janowitz, Daniel Müller, Claudia Ertl-Wagner, Birgit Stahl, Robert Dichgans, Martin Duering, Marco Ewers, Michael Alzheimers Res Ther Research BACKGROUND: Recent evidence derived from functional magnetic resonance imaging (fMRI) studies suggests that functional hubs (i.e., highly connected brain regions) are important for mental health. We found recently that global connectivity of a hub in the left frontal cortex (LFC connectivity) is associated with relatively preserved memory abilities and higher levels of protective factors (education, IQ) in normal aging and Alzheimer’s disease. These results suggest that LFC connectivity supports reserve capacity, alleviating memory decline. An open question, however, is why LFC connectivity is beneficial and supports memory function in the face of neurodegeneration. We hypothesized that higher LFC connectivity is associated with enhanced efficiency in connected major networks involved in episodic memory. We further hypothesized that higher LFC-related network efficiency predicts higher memory abilities. METHODS: We assessed fMRI during a face-name association learning task performed by 26 healthy, cognitively normal elderly participants. Using beta-series correlation analysis, we computed task-related LFC connectivity to key memory networks, including the default mode network (DMN) and dorsal attention network (DAN). Network efficiency within the DMN and DAN was estimated by the graph theoretical small-worldness statistic. We applied linear regression analyses to test the association between LFC connectivity with the DMN/DAN and small-worldness of these networks. Mediation analysis was applied to test LFC connectivity to the DMN and DAN as a mediator of the association between education and higher DMN and DAN small-worldness. Last, we tested network small-worldness as a predictor of memory performance. RESULTS: We found that higher LFC connectivity to the DMN and DAN during successful memory encoding and recognition was associated with higher small-worldness of those networks. Higher task-related LFC connectivity mediated the association between education and higher small-worldness in the DMN and DAN. Further, higher small-worldness of these networks predicted better performance in the memory task. CONCLUSIONS: The present results suggest that higher education-related LFC connectivity to key memory networks during a memory task is associated with higher network efficiency and thus enhanced reserve of memory abilities in aging. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13195-018-0358-y) contains supplementary material, which is available to authorized users. BioMed Central 2018-03-06 /pmc/articles/PMC5838935/ /pubmed/29510747 http://dx.doi.org/10.1186/s13195-018-0358-y Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Franzmeier, Nicolai
Hartmann, Julia
Taylor, Alexander N. W.
Araque-Caballero, Miguel Á.
Simon-Vermot, Lee
Kambeitz-Ilankovic, Lana
Bürger, Katharina
Catak, Cihan
Janowitz, Daniel
Müller, Claudia
Ertl-Wagner, Birgit
Stahl, Robert
Dichgans, Martin
Duering, Marco
Ewers, Michael
The left frontal cortex supports reserve in aging by enhancing functional network efficiency
title The left frontal cortex supports reserve in aging by enhancing functional network efficiency
title_full The left frontal cortex supports reserve in aging by enhancing functional network efficiency
title_fullStr The left frontal cortex supports reserve in aging by enhancing functional network efficiency
title_full_unstemmed The left frontal cortex supports reserve in aging by enhancing functional network efficiency
title_short The left frontal cortex supports reserve in aging by enhancing functional network efficiency
title_sort left frontal cortex supports reserve in aging by enhancing functional network efficiency
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5838935/
https://www.ncbi.nlm.nih.gov/pubmed/29510747
http://dx.doi.org/10.1186/s13195-018-0358-y
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