What Can Glioma Patients Teach Us about Language (Re)Organization in the Bilingual Brain: Evidence from fMRI and MEG.

Abstract

Simple SummaryLow-grade glioma (LGG) patients constitute an ideal in vivo pathological model to investigate cerebral neuroplasticity associated with major architectural disruption to the language network. Bilingual LGG patients offer a unique opportunity to study the neural capacity to negotiate L1 and L2 processing before and after the resection of critical language hubs. By combining the spatial resolution of fMRI with the temporal resolution and oscillatory information provided by MEG, we mapped the language network and its functional (re)organization in five Spanish–Basque bilingual patients. Both techniques provide converging evidence that different reshaping patterns occur for L1 and L2 after tumor resection. These changes affect not only language-specific nodes, but also areas associated with executive control mechanisms, underscoring the need for multilingual intraoperative approaches. Understanding neural (re)organization in the bilingual brain is crucial for preserving language function by means of personalized surgical interventions and rehabilitation strategies based on the patient’s linguistic profile.Recent evidence suggests that the presence of brain tumors (e.g., low-grade gliomas) triggers language reorganization. Neuroplasticity mechanisms called into play can transfer linguistic functions from damaged to healthy areas unaffected by the tumor. This phenomenon has been reported in monolingual patients, but much less is known about the neuroplasticity of language in the bilingual brain. A central question is whether processing a first or second language involves the same or different cortical territories and whether damage results in diverse recovery patterns depending on the language involved. This question becomes critical for preserving language areas in bilingual brain-tumor patients to prevent involuntary pathological symptoms following resection. While most studies have focused on intraoperative mapping, here, we go further, reporting clinical cases for five bilingual patients tested before and after tumor resection, using a novel multimethod approach merging neuroimaging information from fMRI and MEG to map the longitudinal reshaping of the language system. Here, we present four main findings. First, all patients preserved linguistic function in both languages after surgery, suggesting that the surgical intervention with intraoperative language mapping was successful in preserving cortical and subcortical structures necessary for brain plasticity at the functional level. Second, we found reorganization of the language network after tumor resection in both languages, mainly reflected by a shift of activity to right hemisphere nodes and the recruitment of ipsilesional left nodes. Third, we found that this reorganization varied according to the language involved, indicating that L1 and L2 follow different reshaping patterns after surgery. Fourth, oscillatory longitudinal effects were correlated with BOLD laterality changes in superior parietal and middle frontal areas. These findings may reflect that neuroplasticity impacts on the compensatory involvement of executive control regions, supporting the allocation of cognitive resources as a consequence of increased attentional demands. Furthermore, these results hint at the complementary role of this neuroimaging approach in language mapping, with fMRI offering excellent spatial localization and MEG providing optimal spectrotemporal resolution.