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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| creator | 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 |
| 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. |
| doi_str_mv | 10.1007/s11682-023-00770-w |
| format | Article |
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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.</description><identifier>ISSN: 1931-7557</identifier><identifier>EISSN: 1931-7565</identifier><identifier>DOI: 10.1007/s11682-023-00770-w</identifier><identifier>PMID: 37067658</identifier><language>eng</language><publisher>New York: Springer US</publisher><subject>Biomedical and Life Sciences ; Biomedicine ; Brain cancer ; Brain tumors ; Chemotherapy ; Eigenvectors ; Epilepsy ; Executive function ; Glioma ; Integration ; Magnetoencephalography ; Multilayers ; Network topologies ; Neural networks ; Neuropsychology ; Neuroradiology ; Neurosciences ; Psychiatry ; Regression analysis ; Tumors</subject><ispartof>Brain imaging and behavior, 2023-08, Vol.17 (4), p.425-435</ispartof><rights>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.</rights><rights>2023. The Author(s).</rights><rights>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. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c475t-1995557d9e365a85fa4e057c2a32a42c29162eaaecbf847132f42175cf7f6d193</citedby><cites>FETCH-LOGICAL-c475t-1995557d9e365a85fa4e057c2a32a42c29162eaaecbf847132f42175cf7f6d193</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s11682-023-00770-w$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s11682-023-00770-w$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37067658$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>van Lingen, Marike R.</creatorcontrib><creatorcontrib>Breedt, Lucas C.</creatorcontrib><creatorcontrib>Geurts, Jeroen J.G.</creatorcontrib><creatorcontrib>Hillebrand, Arjan</creatorcontrib><creatorcontrib>Klein, Martin</creatorcontrib><creatorcontrib>Kouwenhoven, Mathilde C.M.</creatorcontrib><creatorcontrib>Kulik, Shanna D.</creatorcontrib><creatorcontrib>Reijneveld, Jaap C.</creatorcontrib><creatorcontrib>Stam, Cornelis J.</creatorcontrib><creatorcontrib>De Witt Hamer, Philip C.</creatorcontrib><creatorcontrib>Zimmermann, Mona L.M.</creatorcontrib><creatorcontrib>Santos, Fernando A.N.</creatorcontrib><creatorcontrib>Douw, Linda</creatorcontrib><title>The longitudinal relation between executive functioning and multilayer network topology in glioma patients</title><title>Brain imaging and behavior</title><addtitle>Brain Imaging and Behavior</addtitle><addtitle>Brain Imaging Behav</addtitle><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.</description><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Brain cancer</subject><subject>Brain tumors</subject><subject>Chemotherapy</subject><subject>Eigenvectors</subject><subject>Epilepsy</subject><subject>Executive function</subject><subject>Glioma</subject><subject>Integration</subject><subject>Magnetoencephalography</subject><subject>Multilayers</subject><subject>Network topologies</subject><subject>Neural networks</subject><subject>Neuropsychology</subject><subject>Neuroradiology</subject><subject>Neurosciences</subject><subject>Psychiatry</subject><subject>Regression 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B.V</general><scope>C6C</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7RV</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB0</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20230801</creationdate><title>The longitudinal 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function</topic><topic>Glioma</topic><topic>Integration</topic><topic>Magnetoencephalography</topic><topic>Multilayers</topic><topic>Network topologies</topic><topic>Neural networks</topic><topic>Neuropsychology</topic><topic>Neuroradiology</topic><topic>Neurosciences</topic><topic>Psychiatry</topic><topic>Regression analysis</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>van Lingen, Marike R.</creatorcontrib><creatorcontrib>Breedt, Lucas C.</creatorcontrib><creatorcontrib>Geurts, Jeroen J.G.</creatorcontrib><creatorcontrib>Hillebrand, Arjan</creatorcontrib><creatorcontrib>Klein, Martin</creatorcontrib><creatorcontrib>Kouwenhoven, Mathilde C.M.</creatorcontrib><creatorcontrib>Kulik, Shanna D.</creatorcontrib><creatorcontrib>Reijneveld, Jaap C.</creatorcontrib><creatorcontrib>Stam, Cornelis J.</creatorcontrib><creatorcontrib>De Witt Hamer, Philip C.</creatorcontrib><creatorcontrib>Zimmermann, Mona 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J.G.</au><au>Hillebrand, Arjan</au><au>Klein, Martin</au><au>Kouwenhoven, Mathilde C.M.</au><au>Kulik, Shanna D.</au><au>Reijneveld, Jaap C.</au><au>Stam, Cornelis J.</au><au>De Witt Hamer, Philip C.</au><au>Zimmermann, Mona L.M.</au><au>Santos, Fernando A.N.</au><au>Douw, Linda</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The longitudinal relation between executive functioning and multilayer network topology in glioma patients</atitle><jtitle>Brain imaging and behavior</jtitle><stitle>Brain Imaging and Behavior</stitle><addtitle>Brain Imaging Behav</addtitle><date>2023-08-01</date><risdate>2023</risdate><volume>17</volume><issue>4</issue><spage>425</spage><epage>435</epage><pages>425-435</pages><issn>1931-7557</issn><eissn>1931-7565</eissn><abstract>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.</abstract><cop>New York</cop><pub>Springer US</pub><pmid>37067658</pmid><doi>10.1007/s11682-023-00770-w</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| source | SpringerLink Journals - AutoHoldings |
| subjects | Biomedical and Life Sciences Biomedicine Brain cancer Brain tumors Chemotherapy Eigenvectors Epilepsy Executive function Glioma Integration Magnetoencephalography Multilayers Network topologies Neural networks Neuropsychology Neuroradiology Neurosciences Psychiatry Regression analysis Tumors |
| title | The longitudinal relation between executive functioning and multilayer network topology in glioma patients |
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