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Distinct Slow-Wave Activity Patterns in Resting-State Electroencephalography and Their Relation to Language Functioning in Low-Grade Glioma and Meningioma Patients

INTRODUCTION: Brain tumours frequently cause language impairments and are also likely to co-occur with localised abnormal slow-wave brain activity. However, it is unclear whether this applies specifically to low-grade brain tumours. We investigate slow-wave activity in resting-state electroencephalo...

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Autores principales: Wolthuis, Nienke, Bosma, Ingeborg, Bastiaanse, Roelien, Cherian, Perumpillichira J., Smits, Marion, Veenstra, Wencke, Wagemakers, Michiel, Vincent, Arnaud, Satoer, Djaina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8986989/
https://www.ncbi.nlm.nih.gov/pubmed/35399357
http://dx.doi.org/10.3389/fnhum.2022.748128
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author Wolthuis, Nienke
Bosma, Ingeborg
Bastiaanse, Roelien
Cherian, Perumpillichira J.
Smits, Marion
Veenstra, Wencke
Wagemakers, Michiel
Vincent, Arnaud
Satoer, Djaina
author_facet Wolthuis, Nienke
Bosma, Ingeborg
Bastiaanse, Roelien
Cherian, Perumpillichira J.
Smits, Marion
Veenstra, Wencke
Wagemakers, Michiel
Vincent, Arnaud
Satoer, Djaina
author_sort Wolthuis, Nienke
collection PubMed
description INTRODUCTION: Brain tumours frequently cause language impairments and are also likely to co-occur with localised abnormal slow-wave brain activity. However, it is unclear whether this applies specifically to low-grade brain tumours. We investigate slow-wave activity in resting-state electroencephalography (EEG) in low-grade glioma and meningioma patients, and its relation to pre- and postoperative language functioning. METHOD: Patients with a glioma (N = 15) infiltrating the language-dominant hemisphere and patients with a meningioma (N = 10) with mass effect on this hemisphere underwent extensive language testing before and 1 year after surgery. EEG was registered preoperatively, postoperatively (glioma patients only), and once in healthy individuals. Slow-wave activity in delta- and theta- frequency bands was evaluated visually and quantitatively by spectral power at three levels over the scalp: the whole brain, the affected hemisphere, and the affected region. RESULTS: Glioma patients had increased delta activity (affected area) and increased theta activity (all levels) before and after surgery. In these patients, increased preoperative theta activity was related to the presence of language impairment, especially to poor word retrieval and grammatical performance. Preoperative slow-wave activity was also related to postoperative language outcomes. Meningioma patients showed no significant increase in EEG slow-wave activity compared to healthy individuals, but they presented with word retrieval, grammatical, and writing problems preoperatively, as well as with writing impairments postoperatively. DISCUSSION: Although the brain-tumour pathology in low-grade gliomas and meningiomas has a different effect on resting-state brain activity, patients with low-grade gliomas and meningiomas both suffer from language impairments. Increased theta activity in glioma patients can be considered as a language-impairment marker, with prognostic value for language outcome after surgery.
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spelling pubmed-89869892022-04-08 Distinct Slow-Wave Activity Patterns in Resting-State Electroencephalography and Their Relation to Language Functioning in Low-Grade Glioma and Meningioma Patients Wolthuis, Nienke Bosma, Ingeborg Bastiaanse, Roelien Cherian, Perumpillichira J. Smits, Marion Veenstra, Wencke Wagemakers, Michiel Vincent, Arnaud Satoer, Djaina Front Hum Neurosci Human Neuroscience INTRODUCTION: Brain tumours frequently cause language impairments and are also likely to co-occur with localised abnormal slow-wave brain activity. However, it is unclear whether this applies specifically to low-grade brain tumours. We investigate slow-wave activity in resting-state electroencephalography (EEG) in low-grade glioma and meningioma patients, and its relation to pre- and postoperative language functioning. METHOD: Patients with a glioma (N = 15) infiltrating the language-dominant hemisphere and patients with a meningioma (N = 10) with mass effect on this hemisphere underwent extensive language testing before and 1 year after surgery. EEG was registered preoperatively, postoperatively (glioma patients only), and once in healthy individuals. Slow-wave activity in delta- and theta- frequency bands was evaluated visually and quantitatively by spectral power at three levels over the scalp: the whole brain, the affected hemisphere, and the affected region. RESULTS: Glioma patients had increased delta activity (affected area) and increased theta activity (all levels) before and after surgery. In these patients, increased preoperative theta activity was related to the presence of language impairment, especially to poor word retrieval and grammatical performance. Preoperative slow-wave activity was also related to postoperative language outcomes. Meningioma patients showed no significant increase in EEG slow-wave activity compared to healthy individuals, but they presented with word retrieval, grammatical, and writing problems preoperatively, as well as with writing impairments postoperatively. DISCUSSION: Although the brain-tumour pathology in low-grade gliomas and meningiomas has a different effect on resting-state brain activity, patients with low-grade gliomas and meningiomas both suffer from language impairments. Increased theta activity in glioma patients can be considered as a language-impairment marker, with prognostic value for language outcome after surgery. Frontiers Media S.A. 2022-03-24 /pmc/articles/PMC8986989/ /pubmed/35399357 http://dx.doi.org/10.3389/fnhum.2022.748128 Text en Copyright © 2022 Wolthuis, Bosma, Bastiaanse, Cherian, Smits, Veenstra, Wagemakers, Vincent and Satoer. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Human Neuroscience
Wolthuis, Nienke
Bosma, Ingeborg
Bastiaanse, Roelien
Cherian, Perumpillichira J.
Smits, Marion
Veenstra, Wencke
Wagemakers, Michiel
Vincent, Arnaud
Satoer, Djaina
Distinct Slow-Wave Activity Patterns in Resting-State Electroencephalography and Their Relation to Language Functioning in Low-Grade Glioma and Meningioma Patients
title Distinct Slow-Wave Activity Patterns in Resting-State Electroencephalography and Their Relation to Language Functioning in Low-Grade Glioma and Meningioma Patients
title_full Distinct Slow-Wave Activity Patterns in Resting-State Electroencephalography and Their Relation to Language Functioning in Low-Grade Glioma and Meningioma Patients
title_fullStr Distinct Slow-Wave Activity Patterns in Resting-State Electroencephalography and Their Relation to Language Functioning in Low-Grade Glioma and Meningioma Patients
title_full_unstemmed Distinct Slow-Wave Activity Patterns in Resting-State Electroencephalography and Their Relation to Language Functioning in Low-Grade Glioma and Meningioma Patients
title_short Distinct Slow-Wave Activity Patterns in Resting-State Electroencephalography and Their Relation to Language Functioning in Low-Grade Glioma and Meningioma Patients
title_sort distinct slow-wave activity patterns in resting-state electroencephalography and their relation to language functioning in low-grade glioma and meningioma patients
topic Human Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8986989/
https://www.ncbi.nlm.nih.gov/pubmed/35399357
http://dx.doi.org/10.3389/fnhum.2022.748128
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