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The longitudinal relation between executive functioning and multilayer network topology in glioma patients

Many patients with glioma, primary brain tumors, suffer from poorly understood executive functioning deficits before and/or after tumor resection. We aimed to test whether frontoparietal network centrality of multilayer networks, allowing for integration across multiple frequencies, relates to and p...

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Autores principales: van Lingen, Marike R., Breedt, Lucas C., Geurts, Jeroen J.G., Hillebrand, Arjan, Klein, Martin, Kouwenhoven, Mathilde C.M., Kulik, Shanna D., Reijneveld, Jaap C., Stam, Cornelis J., De Witt Hamer, Philip C., Zimmermann, Mona L.M., Santos, Fernando A.N., Douw, Linda
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10435610/
https://www.ncbi.nlm.nih.gov/pubmed/37067658
http://dx.doi.org/10.1007/s11682-023-00770-w
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author van Lingen, Marike R.
Breedt, Lucas C.
Geurts, Jeroen J.G.
Hillebrand, Arjan
Klein, Martin
Kouwenhoven, Mathilde C.M.
Kulik, Shanna D.
Reijneveld, Jaap C.
Stam, Cornelis J.
De Witt Hamer, Philip C.
Zimmermann, Mona L.M.
Santos, Fernando A.N.
Douw, Linda
author_facet van Lingen, Marike R.
Breedt, Lucas C.
Geurts, Jeroen J.G.
Hillebrand, Arjan
Klein, Martin
Kouwenhoven, Mathilde C.M.
Kulik, Shanna D.
Reijneveld, Jaap C.
Stam, Cornelis J.
De Witt Hamer, Philip C.
Zimmermann, Mona L.M.
Santos, Fernando A.N.
Douw, Linda
author_sort van Lingen, Marike R.
collection PubMed
description Many patients with glioma, primary brain tumors, suffer from poorly understood executive functioning deficits before and/or after tumor resection. We aimed to test whether frontoparietal network centrality of multilayer networks, allowing for integration across multiple frequencies, relates to and predicts executive functioning in glioma. Patients with glioma (n = 37) underwent resting-state magnetoencephalography and neuropsychological tests assessing word fluency, inhibition, and set shifting before (T1) and one year after tumor resection (T2). We constructed binary multilayer networks comprising six layers, with each layer representing frequency-specific functional connectivity between source-localized time series of 78 cortical regions. Average frontoparietal network multilayer eigenvector centrality, a measure for network integration, was calculated at both time points. Regression analyses were used to investigate associations with executive functioning. At T1, lower multilayer integration (p = 0.017) and epilepsy (p = 0.006) associated with poorer set shifting (adj. R(2) = 0.269). Decreasing multilayer integration (p = 0.022) and not undergoing chemotherapy at T2 (p = 0.004) related to deteriorating set shifting over time (adj. R(2) = 0.283). No significant associations were found for word fluency or inhibition, nor did T1 multilayer integration predict changes in executive functioning. As expected, our results establish multilayer integration of the frontoparietal network as a cross-sectional and longitudinal correlate of executive functioning in glioma patients. However, multilayer integration did not predict postoperative changes in executive functioning, which together with the fact that this correlate is also found in health and other diseases, limits its specific clinical relevance in glioma. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11682-023-00770-w.
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spelling pubmed-104356102023-08-19 The longitudinal relation between executive functioning and multilayer network topology in glioma patients van Lingen, Marike R. Breedt, Lucas C. Geurts, Jeroen J.G. Hillebrand, Arjan Klein, Martin Kouwenhoven, Mathilde C.M. Kulik, Shanna D. Reijneveld, Jaap C. Stam, Cornelis J. De Witt Hamer, Philip C. Zimmermann, Mona L.M. Santos, Fernando A.N. Douw, Linda Brain Imaging Behav Article Many patients with glioma, primary brain tumors, suffer from poorly understood executive functioning deficits before and/or after tumor resection. We aimed to test whether frontoparietal network centrality of multilayer networks, allowing for integration across multiple frequencies, relates to and predicts executive functioning in glioma. Patients with glioma (n = 37) underwent resting-state magnetoencephalography and neuropsychological tests assessing word fluency, inhibition, and set shifting before (T1) and one year after tumor resection (T2). We constructed binary multilayer networks comprising six layers, with each layer representing frequency-specific functional connectivity between source-localized time series of 78 cortical regions. Average frontoparietal network multilayer eigenvector centrality, a measure for network integration, was calculated at both time points. Regression analyses were used to investigate associations with executive functioning. At T1, lower multilayer integration (p = 0.017) and epilepsy (p = 0.006) associated with poorer set shifting (adj. R(2) = 0.269). Decreasing multilayer integration (p = 0.022) and not undergoing chemotherapy at T2 (p = 0.004) related to deteriorating set shifting over time (adj. R(2) = 0.283). No significant associations were found for word fluency or inhibition, nor did T1 multilayer integration predict changes in executive functioning. As expected, our results establish multilayer integration of the frontoparietal network as a cross-sectional and longitudinal correlate of executive functioning in glioma patients. However, multilayer integration did not predict postoperative changes in executive functioning, which together with the fact that this correlate is also found in health and other diseases, limits its specific clinical relevance in glioma. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11682-023-00770-w. Springer US 2023-04-17 2023 /pmc/articles/PMC10435610/ /pubmed/37067658 http://dx.doi.org/10.1007/s11682-023-00770-w Text en © The Author(s) 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law. 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 Article
van Lingen, Marike R.
Breedt, Lucas C.
Geurts, Jeroen J.G.
Hillebrand, Arjan
Klein, Martin
Kouwenhoven, Mathilde C.M.
Kulik, Shanna D.
Reijneveld, Jaap C.
Stam, Cornelis J.
De Witt Hamer, Philip C.
Zimmermann, Mona L.M.
Santos, Fernando A.N.
Douw, Linda
The longitudinal relation between executive functioning and multilayer network topology in glioma patients
title The longitudinal relation between executive functioning and multilayer network topology in glioma patients
title_full The longitudinal relation between executive functioning and multilayer network topology in glioma patients
title_fullStr The longitudinal relation between executive functioning and multilayer network topology in glioma patients
title_full_unstemmed The longitudinal relation between executive functioning and multilayer network topology in glioma patients
title_short The longitudinal relation between executive functioning and multilayer network topology in glioma patients
title_sort longitudinal relation between executive functioning and multilayer network topology in glioma patients
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10435610/
https://www.ncbi.nlm.nih.gov/pubmed/37067658
http://dx.doi.org/10.1007/s11682-023-00770-w
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