Unveiling the neuroplastic capacity of the bilingual brain: insights from healthy and pathological individuals.

Research on the neural imprint of dual-language experience, crucial for understanding how the brain processes dominant and non-dominant languages, remains inconclusive. Conflicting evidence suggests either similarity or distinction in neural processing, with implications for bilingual patients with brain tumors. Preserving dual-language functions after surgery requires considering pre-diagnosis neuroplastic changes. Here, we combine univariate and multivariate fMRI methodologies to test a group of healthy Spanish-Basque bilinguals and a group of bilingual patients with gliomas affecting the language-dominant hemisphere while they overtly produced sentences in either their dominant or non-dominant language. Findings from healthy participants revealed the presence of a shared neural system for both languages, while also identifying regions with distinct language-dependent activation and lateralization patterns. Specifically, while the dominant language engaged a more left-lateralized network, speech production in the non-dominant language relied on the recruitment of a bilateral basal ganglia-thalamo-cortical circuit. Notably, based on language lateralization patterns, we were able to robustly decode (AUC: 0.80 ± 0.18) the language being used. Conversely, bilingual patients exhibited bilateral activation patterns for both languages. For the dominant language, regions such as the cerebellum, thalamus, and caudate acted in concert with the sparsely activated language-specific nodes. In the case of the non-dominant language, the recruitment of the default mode network was notably prominent. These results demonstrate the compensatory engagement of non-language-specific networks in the preservation of bilingual speech production, even in the face of pathological conditions. Overall, our findings underscore the pervasive impact of dual-language experience on brain functional (re)organization, both in health and disease.

Grey Matter Reshaping of Language-Related Regions Depends on Tumor Lateralization.

A brain tumor in the left hemisphere can decrease language laterality as assessed through fMRI. However, it remains unclear whether or not this decreased language laterality is associated with a structural reshaping of the grey matter, particularly within the language network. Here, we examine if the disruption of the language hubs exclusively affects the macrostructural properties of the contralateral homologues or whether it affects both hemispheres. This study uses voxel-based morphometry applied to high-resolution MR T1-weighted MPRAGE images from 31 adult patients' left hemisphere, which is dominant for language. Eighteen patients had brain tumors in the left hemisphere, and thirteen had tumors in the right hemisphere. A cohort of 71 healthy individuals matched with respect to age and sex was used as a baseline. We defined 10 ROIs per hemisphere involved in language function. Two separate repeated-measure ANOVAs were conducted with the volume per region as the dependent variable. For the patients, tumor lateralization (right versus left) served as a between-subject factor. The current study demonstrated that the presence of a brain tumor generates global volumetric changes affecting the left language regions and their contralateral homologues. These changes are mediated by the lateralization of the lesion. Our findings suggest that functional mechanisms are supported by the rearrangement of the grey matter.

Grey matter reshaping of language-related regions depends on tumor lateralization.

A brain tumor in the left hemisphere can decrease language laterality as assessed with fMRI. However, it remains unclear whether or not this decreased language laterality is associated with a structural reshaping of the grey matter, particularly within the language network. Here, we examine if the disruption of language hubs exclusively affects macrostructural properties of contralateral homologues (as suggested by previous research), or whether it affects both hemispheres. This study uses voxel-based morphometry applied to high-resolution MR T1-weighted MPRAGE images from 31 adult patients left-dominant for language. Eighteen patients had brain tumors in the left hemisphere, and 13 had tumors in the right hemisphere. A cohort of 71 healthy individuals matched on age and sex was used as a baseline. We defined 10 ROIs per hemisphere known to subserve language function. Two separate repeated-measures ANOVAs were conducted with the volume per region as the dependent variables. For the patients, tumor lateralization (right versus left) served as a between-subject factor. The current study demonstrated that the presence of a brain tumor generates a global volumetric change affecting left language regions and their contralateral homologues. These changes are mediated by the lateralization of the lesion. Our findings suggest that compensatory functional mechanisms are supported by the rearrangement of the grey matter, although future longitudinal research should determine the temporal course of such changes.

MULTIMAP: Multilingual picture naming test for mapping eloquent areas during awake surgeries.

Picture naming tasks are currently the gold standard for identifying and preserving language-related areas during awake brain surgery. With multilingual populations increasing worldwide, patients frequently need to be tested in more than one language. There is still no reliable testing instrument, as the available batteries have been developed for specific languages. Heterogeneity in the selection criteria for stimuli leads to differences, for example, in the size, color, image quality, and even names associated with pictures, making direct cross-linguistic comparisons difficult. Here we present MULTIMAP, a new multilingual picture naming test for mapping eloquent areas during awake brain surgery. Recognizing that the distinction between nouns and verbs is necessary for detailed and precise language mapping, MULTIMAP consists of a database of 218 standardized color pictures representing both objects and actions. These images have been tested for name agreement with speakers of Spanish, Basque, Catalan, Italian, French, English, German, Mandarin Chinese, and Arabic, and have been controlled for relevant linguistic features in cross-language combinations. The MULTIMAP test for objects and verbs represents an alternative to the Oral Denomination 80 (DO 80) monolingual pictorial set currently used in language mapping, providing an open-source, standardized set of up-to-date pictures, where relevant linguistic variables across several languages have been taken into account in picture creation and selection.

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 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.