Atypical functional connectome hierarchy impacts cognition in temporal lobe epilepsy

Objective Drug‐resistant temporal lobe epilepsy (TLE) is typically associated with hippocampal pathology. However, widespread network alterations are increasingly recognized and suggested to perturb cognitive function in multiple domains. Here we tested (1) whether TLE shows atypical cortical hierar...

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Veröffentlicht in:Epilepsia (Copenhagen) 2021-11, Vol.62 (11), p.2589-2603
Hauptverfasser: Fadaie, Fatemeh, Lee, Hyo M., Caldairou, Benoit, Gill, Ravnoor S., Sziklas, Viviane, Crane, Joelle, Bernhardt, Boris C., Hong, Seok‐Jun, Bernasconi, Andrea, Bernasconi, Neda
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container_issue 11
container_start_page 2589
container_title Epilepsia (Copenhagen)
container_volume 62
creator Fadaie, Fatemeh
Lee, Hyo M.
Caldairou, Benoit
Gill, Ravnoor S.
Sziklas, Viviane
Crane, Joelle
Bernhardt, Boris C.
Hong, Seok‐Jun
Bernasconi, Andrea
Bernasconi, Neda
description Objective Drug‐resistant temporal lobe epilepsy (TLE) is typically associated with hippocampal pathology. However, widespread network alterations are increasingly recognized and suggested to perturb cognitive function in multiple domains. Here we tested (1) whether TLE shows atypical cortical hierarchical organization, differentiating sensory and higher order systems; and (2) whether atypical hierarchy predicts cognitive impairment. Methods We studied 72 well‐characterized drug‐resistant TLE patients and 41 healthy controls, statistically matched for age and sex, using multimodal magnetic resonance imaging analysis and cognitive testing. To model cortical hierarchical organization in vivo, we used a bidirectional stepwise functional connectivity analysis tapping into the differentiation between sensory/unimodal and paralimbic/transmodal cortices. Linear models compared patients to controls. Finally, we assessed associations of functional anomalies to cortical atrophy and microstructural anomalies, as well as clinical and cognitive parameters. Results Compared to controls, TLE presented with bidirectional disruptions of sensory–paralimbic functional organization. Stepwise connectivity remained segregated within paralimbic and salience networks at the top of the hierarchy, and sensorimotor and dorsal attention at the bottom. Whereas paralimbic segregation was associated with atypical cortical myeloarchitecture and hippocampal atrophy, dysconnectivity of sensorimotor cortices reflected diffuse cortical thinning. The degree of abnormal hierarchical organization in sensory‐petal streams covaried, with broad cognitive impairments spanning sensorimotor, attention, fluency, and visuoconstructional ability and memory, and was more marked in patients with longer disease duration and Engel I outcome. Significance Our findings show atypical functional integration between paralimbic/transmodal and sensory/unimodal systems in TLE. Differential associations with paralimbic microstructure and sensorimotor atrophy suggest that system‐level imbalance likely reflects complementary structural processes, but ultimately accounts for a broad spectrum of cognitive impairments. Hierarchical contextualization of cognitive deficits promises to open new avenues for personalized counseling in TLE.
doi_str_mv 10.1111/epi.17032
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However, widespread network alterations are increasingly recognized and suggested to perturb cognitive function in multiple domains. Here we tested (1) whether TLE shows atypical cortical hierarchical organization, differentiating sensory and higher order systems; and (2) whether atypical hierarchy predicts cognitive impairment. Methods We studied 72 well‐characterized drug‐resistant TLE patients and 41 healthy controls, statistically matched for age and sex, using multimodal magnetic resonance imaging analysis and cognitive testing. To model cortical hierarchical organization in vivo, we used a bidirectional stepwise functional connectivity analysis tapping into the differentiation between sensory/unimodal and paralimbic/transmodal cortices. Linear models compared patients to controls. Finally, we assessed associations of functional anomalies to cortical atrophy and microstructural anomalies, as well as clinical and cognitive parameters. Results Compared to controls, TLE presented with bidirectional disruptions of sensory–paralimbic functional organization. Stepwise connectivity remained segregated within paralimbic and salience networks at the top of the hierarchy, and sensorimotor and dorsal attention at the bottom. Whereas paralimbic segregation was associated with atypical cortical myeloarchitecture and hippocampal atrophy, dysconnectivity of sensorimotor cortices reflected diffuse cortical thinning. The degree of abnormal hierarchical organization in sensory‐petal streams covaried, with broad cognitive impairments spanning sensorimotor, attention, fluency, and visuoconstructional ability and memory, and was more marked in patients with longer disease duration and Engel I outcome. Significance Our findings show atypical functional integration between paralimbic/transmodal and sensory/unimodal systems in TLE. Differential associations with paralimbic microstructure and sensorimotor atrophy suggest that system‐level imbalance likely reflects complementary structural processes, but ultimately accounts for a broad spectrum of cognitive impairments. Hierarchical contextualization of cognitive deficits promises to open new avenues for personalized counseling in TLE.</description><identifier>ISSN: 0013-9580</identifier><identifier>EISSN: 1528-1167</identifier><identifier>DOI: 10.1111/epi.17032</identifier><identifier>PMID: 34490890</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Atrophy ; Atrophy - pathology ; brain networks ; Cognition ; Cognitive ability ; Connectome ; Epilepsy ; Epilepsy, Temporal Lobe - complications ; Epilepsy, Temporal Lobe - diagnostic imaging ; Epilepsy, Temporal Lobe - pathology ; Functional morphology ; Hippocampus ; Hippocampus - pathology ; Humans ; Magnetic Resonance Imaging - methods ; MRI ; Patients ; Sensorimotor system ; Sensory integration ; Temporal lobe ; temporal lobe epilepsy</subject><ispartof>Epilepsia (Copenhagen), 2021-11, Vol.62 (11), p.2589-2603</ispartof><rights>2021 International League Against Epilepsy</rights><rights>2021 International League Against Epilepsy.</rights><rights>Copyright © 2021 International League Against Epilepsy</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3532-fb799b0bcca811a42aa69bedaff700952fe657f1ae0512e3acee30f66c8384143</citedby><cites>FETCH-LOGICAL-c3532-fb799b0bcca811a42aa69bedaff700952fe657f1ae0512e3acee30f66c8384143</cites><orcidid>0000-0002-8947-9518 ; 0000-0001-9256-6041 ; 0000-0001-9358-5703</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fepi.17032$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fepi.17032$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,777,781,1412,27905,27906,45555,45556</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34490890$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Fadaie, Fatemeh</creatorcontrib><creatorcontrib>Lee, Hyo M.</creatorcontrib><creatorcontrib>Caldairou, Benoit</creatorcontrib><creatorcontrib>Gill, Ravnoor S.</creatorcontrib><creatorcontrib>Sziklas, Viviane</creatorcontrib><creatorcontrib>Crane, Joelle</creatorcontrib><creatorcontrib>Bernhardt, Boris C.</creatorcontrib><creatorcontrib>Hong, Seok‐Jun</creatorcontrib><creatorcontrib>Bernasconi, Andrea</creatorcontrib><creatorcontrib>Bernasconi, Neda</creatorcontrib><title>Atypical functional connectome hierarchy impacts cognition in temporal lobe epilepsy</title><title>Epilepsia (Copenhagen)</title><addtitle>Epilepsia</addtitle><description>Objective Drug‐resistant temporal lobe epilepsy (TLE) is typically associated with hippocampal pathology. However, widespread network alterations are increasingly recognized and suggested to perturb cognitive function in multiple domains. Here we tested (1) whether TLE shows atypical cortical hierarchical organization, differentiating sensory and higher order systems; and (2) whether atypical hierarchy predicts cognitive impairment. Methods We studied 72 well‐characterized drug‐resistant TLE patients and 41 healthy controls, statistically matched for age and sex, using multimodal magnetic resonance imaging analysis and cognitive testing. To model cortical hierarchical organization in vivo, we used a bidirectional stepwise functional connectivity analysis tapping into the differentiation between sensory/unimodal and paralimbic/transmodal cortices. Linear models compared patients to controls. Finally, we assessed associations of functional anomalies to cortical atrophy and microstructural anomalies, as well as clinical and cognitive parameters. 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Differential associations with paralimbic microstructure and sensorimotor atrophy suggest that system‐level imbalance likely reflects complementary structural processes, but ultimately accounts for a broad spectrum of cognitive impairments. Hierarchical contextualization of cognitive deficits promises to open new avenues for personalized counseling in TLE.</description><subject>Atrophy</subject><subject>Atrophy - pathology</subject><subject>brain networks</subject><subject>Cognition</subject><subject>Cognitive ability</subject><subject>Connectome</subject><subject>Epilepsy</subject><subject>Epilepsy, Temporal Lobe - complications</subject><subject>Epilepsy, Temporal Lobe - diagnostic imaging</subject><subject>Epilepsy, Temporal Lobe - pathology</subject><subject>Functional morphology</subject><subject>Hippocampus</subject><subject>Hippocampus - pathology</subject><subject>Humans</subject><subject>Magnetic Resonance Imaging - methods</subject><subject>MRI</subject><subject>Patients</subject><subject>Sensorimotor system</subject><subject>Sensory integration</subject><subject>Temporal lobe</subject><subject>temporal lobe epilepsy</subject><issn>0013-9580</issn><issn>1528-1167</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp10MtKxDAUBuAgijNeFr6AFNzoonqStE2zHIbxAgO60HVJ44lG2qYmLdK3N-OoC8FsEsiXn5yfkBMKlzSuK-ztJRXA2Q6Z05yVKaWF2CVzAMpTmZcwIwchvAGAKATfJzOeZRJKCXPyuBim3mrVJGbs9GBdF4_adR3qwbWYvFr0yuvXKbFtr_QQ4uVLZzcwsV0yYNs7H580rsYk_qPBPkxHZM-oJuDx935Inq5Xj8vbdH1_c7dcrFPNc85SUwspa6i1ViWlKmNKFbLGZ2WMAJA5M1jkwlCFkFOGXGlEDqYodMnLjGb8kJxvc3vv3kcMQ9XaoLFpVIduDBXLBcR-GIdIz_7QNzf6OOxGSWCUCrlRF1ulvQvBo6l6b1vlp4pCtam6iiNWX1VHe_qdONYtPv_Kn24juNqCj9jK9H9StXq420Z-AgNQiI8</recordid><startdate>202111</startdate><enddate>202111</enddate><creator>Fadaie, Fatemeh</creator><creator>Lee, Hyo M.</creator><creator>Caldairou, Benoit</creator><creator>Gill, Ravnoor S.</creator><creator>Sziklas, Viviane</creator><creator>Crane, Joelle</creator><creator>Bernhardt, Boris C.</creator><creator>Hong, Seok‐Jun</creator><creator>Bernasconi, Andrea</creator><creator>Bernasconi, Neda</creator><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-8947-9518</orcidid><orcidid>https://orcid.org/0000-0001-9256-6041</orcidid><orcidid>https://orcid.org/0000-0001-9358-5703</orcidid></search><sort><creationdate>202111</creationdate><title>Atypical functional connectome hierarchy impacts cognition in temporal lobe epilepsy</title><author>Fadaie, Fatemeh ; 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However, widespread network alterations are increasingly recognized and suggested to perturb cognitive function in multiple domains. Here we tested (1) whether TLE shows atypical cortical hierarchical organization, differentiating sensory and higher order systems; and (2) whether atypical hierarchy predicts cognitive impairment. Methods We studied 72 well‐characterized drug‐resistant TLE patients and 41 healthy controls, statistically matched for age and sex, using multimodal magnetic resonance imaging analysis and cognitive testing. To model cortical hierarchical organization in vivo, we used a bidirectional stepwise functional connectivity analysis tapping into the differentiation between sensory/unimodal and paralimbic/transmodal cortices. Linear models compared patients to controls. Finally, we assessed associations of functional anomalies to cortical atrophy and microstructural anomalies, as well as clinical and cognitive parameters. Results Compared to controls, TLE presented with bidirectional disruptions of sensory–paralimbic functional organization. Stepwise connectivity remained segregated within paralimbic and salience networks at the top of the hierarchy, and sensorimotor and dorsal attention at the bottom. Whereas paralimbic segregation was associated with atypical cortical myeloarchitecture and hippocampal atrophy, dysconnectivity of sensorimotor cortices reflected diffuse cortical thinning. The degree of abnormal hierarchical organization in sensory‐petal streams covaried, with broad cognitive impairments spanning sensorimotor, attention, fluency, and visuoconstructional ability and memory, and was more marked in patients with longer disease duration and Engel I outcome. Significance Our findings show atypical functional integration between paralimbic/transmodal and sensory/unimodal systems in TLE. Differential associations with paralimbic microstructure and sensorimotor atrophy suggest that system‐level imbalance likely reflects complementary structural processes, but ultimately accounts for a broad spectrum of cognitive impairments. Hierarchical contextualization of cognitive deficits promises to open new avenues for personalized counseling in TLE.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>34490890</pmid><doi>10.1111/epi.17032</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-8947-9518</orcidid><orcidid>https://orcid.org/0000-0001-9256-6041</orcidid><orcidid>https://orcid.org/0000-0001-9358-5703</orcidid></addata></record>
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source MEDLINE; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection
subjects Atrophy
Atrophy - pathology
brain networks
Cognition
Cognitive ability
Connectome
Epilepsy
Epilepsy, Temporal Lobe - complications
Epilepsy, Temporal Lobe - diagnostic imaging
Epilepsy, Temporal Lobe - pathology
Functional morphology
Hippocampus
Hippocampus - pathology
Humans
Magnetic Resonance Imaging - methods
MRI
Patients
Sensorimotor system
Sensory integration
Temporal lobe
temporal lobe epilepsy
title Atypical functional connectome hierarchy impacts cognition in temporal lobe epilepsy
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