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Disorganization of language and working memory systems in frontal versus temporal lobe epilepsy
Cognitive impairment is a common comorbidity of epilepsy and adversely impacts people with both frontal lobe (FLE) and temporal lobe (TLE) epilepsy. While its neural substrates have been investigated extensively in TLE, functional imaging studies in FLE are scarce. In this study, we profiled the neu...
Autores principales: | , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9976988/ https://www.ncbi.nlm.nih.gov/pubmed/35511160 http://dx.doi.org/10.1093/brain/awac150 |
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author | Caciagli, Lorenzo Paquola, Casey He, Xiaosong Vollmar, Christian Centeno, Maria Wandschneider, Britta Braun, Urs Trimmel, Karin Vos, Sjoerd B Sidhu, Meneka K Thompson, Pamela J Baxendale, Sallie Winston, Gavin P Duncan, John S Bassett, Dani S Koepp, Matthias J Bernhardt, Boris C |
author_facet | Caciagli, Lorenzo Paquola, Casey He, Xiaosong Vollmar, Christian Centeno, Maria Wandschneider, Britta Braun, Urs Trimmel, Karin Vos, Sjoerd B Sidhu, Meneka K Thompson, Pamela J Baxendale, Sallie Winston, Gavin P Duncan, John S Bassett, Dani S Koepp, Matthias J Bernhardt, Boris C |
author_sort | Caciagli, Lorenzo |
collection | PubMed |
description | Cognitive impairment is a common comorbidity of epilepsy and adversely impacts people with both frontal lobe (FLE) and temporal lobe (TLE) epilepsy. While its neural substrates have been investigated extensively in TLE, functional imaging studies in FLE are scarce. In this study, we profiled the neural processes underlying cognitive impairment in FLE and directly compared FLE and TLE to establish commonalities and differences. We investigated 172 adult participants (56 with FLE, 64 with TLE and 52 controls) using neuropsychological tests and four functional MRI tasks probing expressive language (verbal fluency, verb generation) and working memory (verbal and visuo-spatial). Patient groups were comparable in disease duration and anti-seizure medication load. We devised a multiscale approach to map brain activation and deactivation during cognition and track reorganization in FLE and TLE. Voxel-based analyses were complemented with profiling of task effects across established motifs of functional brain organization: (i) canonical resting-state functional systems; and (ii) the principal functional connectivity gradient, which encodes a continuous transition of regional connectivity profiles, anchoring lower-level sensory and transmodal brain areas at the opposite ends of a spectrum. We show that cognitive impairment in FLE is associated with reduced activation across attentional and executive systems, as well as reduced deactivation of the default mode system, indicative of a large-scale disorganization of task-related recruitment. The imaging signatures of dysfunction in FLE are broadly similar to those in TLE, but some patterns are syndrome-specific: altered default-mode deactivation is more prominent in FLE, while impaired recruitment of posterior language areas during a task with semantic demands is more marked in TLE. Functional abnormalities in FLE and TLE appear overall modulated by disease load. On balance, our study elucidates neural processes underlying language and working memory impairment in FLE, identifies shared and syndrome-specific alterations in the two most common focal epilepsies and sheds light on system behaviour that may be amenable to future remediation strategies. |
format | Online Article Text |
id | pubmed-9976988 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-99769882023-03-02 Disorganization of language and working memory systems in frontal versus temporal lobe epilepsy Caciagli, Lorenzo Paquola, Casey He, Xiaosong Vollmar, Christian Centeno, Maria Wandschneider, Britta Braun, Urs Trimmel, Karin Vos, Sjoerd B Sidhu, Meneka K Thompson, Pamela J Baxendale, Sallie Winston, Gavin P Duncan, John S Bassett, Dani S Koepp, Matthias J Bernhardt, Boris C Brain Original Article Cognitive impairment is a common comorbidity of epilepsy and adversely impacts people with both frontal lobe (FLE) and temporal lobe (TLE) epilepsy. While its neural substrates have been investigated extensively in TLE, functional imaging studies in FLE are scarce. In this study, we profiled the neural processes underlying cognitive impairment in FLE and directly compared FLE and TLE to establish commonalities and differences. We investigated 172 adult participants (56 with FLE, 64 with TLE and 52 controls) using neuropsychological tests and four functional MRI tasks probing expressive language (verbal fluency, verb generation) and working memory (verbal and visuo-spatial). Patient groups were comparable in disease duration and anti-seizure medication load. We devised a multiscale approach to map brain activation and deactivation during cognition and track reorganization in FLE and TLE. Voxel-based analyses were complemented with profiling of task effects across established motifs of functional brain organization: (i) canonical resting-state functional systems; and (ii) the principal functional connectivity gradient, which encodes a continuous transition of regional connectivity profiles, anchoring lower-level sensory and transmodal brain areas at the opposite ends of a spectrum. We show that cognitive impairment in FLE is associated with reduced activation across attentional and executive systems, as well as reduced deactivation of the default mode system, indicative of a large-scale disorganization of task-related recruitment. The imaging signatures of dysfunction in FLE are broadly similar to those in TLE, but some patterns are syndrome-specific: altered default-mode deactivation is more prominent in FLE, while impaired recruitment of posterior language areas during a task with semantic demands is more marked in TLE. Functional abnormalities in FLE and TLE appear overall modulated by disease load. On balance, our study elucidates neural processes underlying language and working memory impairment in FLE, identifies shared and syndrome-specific alterations in the two most common focal epilepsies and sheds light on system behaviour that may be amenable to future remediation strategies. Oxford University Press 2022-05-02 /pmc/articles/PMC9976988/ /pubmed/35511160 http://dx.doi.org/10.1093/brain/awac150 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Original Article Caciagli, Lorenzo Paquola, Casey He, Xiaosong Vollmar, Christian Centeno, Maria Wandschneider, Britta Braun, Urs Trimmel, Karin Vos, Sjoerd B Sidhu, Meneka K Thompson, Pamela J Baxendale, Sallie Winston, Gavin P Duncan, John S Bassett, Dani S Koepp, Matthias J Bernhardt, Boris C Disorganization of language and working memory systems in frontal versus temporal lobe epilepsy |
title | Disorganization of language and working memory systems in frontal versus temporal lobe epilepsy |
title_full | Disorganization of language and working memory systems in frontal versus temporal lobe epilepsy |
title_fullStr | Disorganization of language and working memory systems in frontal versus temporal lobe epilepsy |
title_full_unstemmed | Disorganization of language and working memory systems in frontal versus temporal lobe epilepsy |
title_short | Disorganization of language and working memory systems in frontal versus temporal lobe epilepsy |
title_sort | disorganization of language and working memory systems in frontal versus temporal lobe epilepsy |
topic | Original Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9976988/ https://www.ncbi.nlm.nih.gov/pubmed/35511160 http://dx.doi.org/10.1093/brain/awac150 |
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