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

• Main Authors: Amoruso, L. (Author), Carreiras, M. (Author), Geng, S. (Author), Gil-Robles, S. (Author), Gisbert-Muñoz, S. (Author), Molinaro, N. (Author), Pomposo, I. (Author), Quiñones, I. (Author), Timofeeva, P. (Author)
• Format: Article
• Language: English
• Published: John Wiley and Sons Inc 2021
• Subjects: adult; Adult; alpha rhythm; arcuate fasciculus; Article; astrocytoma; beta rhythm; Beta Rhythm; brain cortex; Brain Neoplasms; brain rhythms; brain tumor; brain tumors; cancer surgery; cavernous hemangioma; Cerebral Cortex; clinical article; controlled study; craniotomy; dorsal region; female; Female; head position; hemisphere; human; Humans; language; language network; Longitudinal Studies; longitudinal study; magnetoencephalography; Magnetoencephalography; male; Male; middle aged; Middle Aged; middle frontal gyrus; nerve cell plasticity; Neuronal Plasticity; neuroplasticity; nuclear magnetic resonance imaging; occipitofrontal fasciculus; oscillation; pathology; pathophysiology; physiology; premotor cortex; preoperative evaluation; priority journal; psycholinguistics; Psycholinguistics; quality of life; speech; superior longitudinal fasciculus; tumor volume; ventral region; white matter; White Matter; young adult; Young Adult
• Online Access: View Fulltext in Publisher

 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. © 2020 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.