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Oscillatory and structural signatures of language plasticity in brain tumor patients: A longitudinal study

Recent evidence suggests that damage to the language network triggers its functional reorganization. Yet, the spectro‐temporal fingerprints of this plastic rearrangement and its relation to anatomical changes is less well understood. Here, we combined magnetoencephalographic recordings with a proxy...

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Autores principales: Amoruso, Lucia, Geng, Shuang, Molinaro, Nicola, Timofeeva, Polina, Gisbert‐Muñoz, Sandra, Gil‐Robles, Santiago, Pomposo, Iñigo, Quiñones, Ileana, Carreiras, Manuel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7978121/
https://www.ncbi.nlm.nih.gov/pubmed/33368838
http://dx.doi.org/10.1002/hbm.25328
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author Amoruso, Lucia
Geng, Shuang
Molinaro, Nicola
Timofeeva, Polina
Gisbert‐Muñoz, Sandra
Gil‐Robles, Santiago
Pomposo, Iñigo
Quiñones, Ileana
Carreiras, Manuel
author_facet Amoruso, Lucia
Geng, Shuang
Molinaro, Nicola
Timofeeva, Polina
Gisbert‐Muñoz, Sandra
Gil‐Robles, Santiago
Pomposo, Iñigo
Quiñones, Ileana
Carreiras, Manuel
author_sort Amoruso, Lucia
collection PubMed
description Recent evidence suggests that damage to the language network triggers its functional reorganization. Yet, the spectro‐temporal fingerprints of this plastic rearrangement and its relation to anatomical changes is less well understood. Here, we combined magnetoencephalographic recordings with a proxy measure of white matter to investigate oscillatory activity supporting language plasticity and its relation to structural reshaping. First, cortical dynamics were acquired in a group of healthy controls during object and action naming. Results showed segregated beta (13–28 Hz) power decreases in left ventral and dorsal pathways, in a time‐window associated to lexico‐semantic processing (~250–500 ms). Six patients with left tumors invading either ventral or dorsal regions performed the same naming task before and 3 months after surgery for tumor resection. When longitudinally comparing patients' responses we found beta compensation mimicking the category‐based segregation showed by controls, with ventral and dorsal damage leading to selective compensation for object and action naming, respectively. At the structural level, all patients showed preoperative changes in white matter tracts possibly linked to plasticity triggered by tumor growth. Furthermore, in some patients, structural changes were also evident after surgery and showed associations with longitudinal changes in beta power lateralization toward the contralesional hemisphere. Overall, our findings support the existence of anatomo‐functional dependencies in language reorganization and highlight the potential role of oscillatory markers in tracking longitudinal plasticity in brain tumor patients. By doing so, they provide valuable information for mapping preoperative and postoperative neural reshaping and plan surgical strategies to preserve language function and patient's quality of life.
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spelling pubmed-79781212021-03-23 Oscillatory and structural signatures of language plasticity in brain tumor patients: A longitudinal study Amoruso, Lucia Geng, Shuang Molinaro, Nicola Timofeeva, Polina Gisbert‐Muñoz, Sandra Gil‐Robles, Santiago Pomposo, Iñigo Quiñones, Ileana Carreiras, Manuel Hum Brain Mapp Research Articles Recent evidence suggests that damage to the language network triggers its functional reorganization. Yet, the spectro‐temporal fingerprints of this plastic rearrangement and its relation to anatomical changes is less well understood. Here, we combined magnetoencephalographic recordings with a proxy measure of white matter to investigate oscillatory activity supporting language plasticity and its relation to structural reshaping. First, cortical dynamics were acquired in a group of healthy controls during object and action naming. Results showed segregated beta (13–28 Hz) power decreases in left ventral and dorsal pathways, in a time‐window associated to lexico‐semantic processing (~250–500 ms). Six patients with left tumors invading either ventral or dorsal regions performed the same naming task before and 3 months after surgery for tumor resection. When longitudinally comparing patients' responses we found beta compensation mimicking the category‐based segregation showed by controls, with ventral and dorsal damage leading to selective compensation for object and action naming, respectively. At the structural level, all patients showed preoperative changes in white matter tracts possibly linked to plasticity triggered by tumor growth. Furthermore, in some patients, structural changes were also evident after surgery and showed associations with longitudinal changes in beta power lateralization toward the contralesional hemisphere. Overall, our findings support the existence of anatomo‐functional dependencies in language reorganization and highlight the potential role of oscillatory markers in tracking longitudinal plasticity in brain tumor patients. By doing so, they provide valuable information for mapping preoperative and postoperative neural reshaping and plan surgical strategies to preserve language function and patient's quality of life. John Wiley & Sons, Inc. 2020-12-24 /pmc/articles/PMC7978121/ /pubmed/33368838 http://dx.doi.org/10.1002/hbm.25328 Text en © 2020 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Research Articles
Amoruso, Lucia
Geng, Shuang
Molinaro, Nicola
Timofeeva, Polina
Gisbert‐Muñoz, Sandra
Gil‐Robles, Santiago
Pomposo, Iñigo
Quiñones, Ileana
Carreiras, Manuel
Oscillatory and structural signatures of language plasticity in brain tumor patients: A longitudinal study
title Oscillatory and structural signatures of language plasticity in brain tumor patients: A longitudinal study
title_full Oscillatory and structural signatures of language plasticity in brain tumor patients: A longitudinal study
title_fullStr Oscillatory and structural signatures of language plasticity in brain tumor patients: A longitudinal study
title_full_unstemmed Oscillatory and structural signatures of language plasticity in brain tumor patients: A longitudinal study
title_short Oscillatory and structural signatures of language plasticity in brain tumor patients: A longitudinal study
title_sort oscillatory and structural signatures of language plasticity in brain tumor patients: a longitudinal study
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7978121/
https://www.ncbi.nlm.nih.gov/pubmed/33368838
http://dx.doi.org/10.1002/hbm.25328
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