Abstract

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.

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