TY - JOUR
T1 - The longitudinal relation between executive functioning and multilayer network topology in glioma patients
AU - van Lingen, Marike R.
AU - Breedt, Lucas C.
AU - Geurts, Jeroen J. G.
AU - Hillebrand, Arjan
AU - Klein, Martin
AU - Kouwenhoven, Mathilde C. M.
AU - Kulik, Shanna D.
AU - Reijneveld, Jaap C.
AU - Stam, Cornelis J.
AU - de Witt Hamer, Philip C.
AU - Zimmermann, Mona L. M.
AU - Santos, Fernando A. N.
AU - Douw, Linda
N1 - Funding Information: This study was funded by a Branco Weiss Fellowship, the Dutch Research Council (Veni 016.146.086 and Vidi 198.015), and EpilepsieNL (grants 08–08 and 09–09). Publisher Copyright: © 2023, The Author(s).
PY - 2023/8
Y1 - 2023/8
N2 - 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. R2 = 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. R2 = 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.
AB - 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. R2 = 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. R2 = 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.
KW - Cognition
KW - Eigenvector centrality
KW - Functional connectivity
KW - Graph theory
KW - Network neuroscience
UR - http://www.scopus.com/inward/record.url?scp=85153086132&partnerID=8YFLogxK
U2 - https://doi.org/10.1007/s11682-023-00770-w
DO - https://doi.org/10.1007/s11682-023-00770-w
M3 - Article
C2 - 37067658
SN - 1931-7557
VL - 17
SP - 425
EP - 435
JO - Brain Imaging and Behavior
JF - Brain Imaging and Behavior
IS - 4
ER -