The impact of bilingualism on brain structure and function is a significant area of research. While bilingualism is known to enhance cognitive abilities like working memory, cognitive control, and attention, the underlying neural mechanisms remain unclear. The age of second language acquisition (AoA) is a crucial factor, as earlier acquisition often correlates with greater cognitive benefits. This study aimed to investigate how AoA influences the functional organization of the brain in bilingual individuals. Previous neuroimaging studies have implicated specific brain regions, white matter tracts, and resting-state networks in bilingual processing, but a comprehensive understanding of whole-brain network organization and the role of the cortico-cerebellar pathway is lacking. The research question focuses on whether early versus late second language learning affects the global and local organization of whole-brain functional networks. The hypothesis is that early second language learning enhances global whole-brain efficiency and modularity, with a significant contribution from cortico-cerebellar circuits. The study's importance lies in elucidating the neural mechanisms behind the cognitive benefits of bilingualism and the impact of developmental timing on brain plasticity.

Extensive research supports the cognitive advantages of bilingualism, particularly in areas such as executive function and working memory. However, the neural correlates of these benefits remain under investigation. Studies have shown functional and structural changes in language-related areas (left frontal and temporal regions), fronto-parietal systems, and the cerebellum. The cerebellum's role in language processing, including motor coordination, cognitive functions, and syntactic processing, is increasingly recognized. Existing neuroimaging research has focused on specific brain areas or white matter tracts but hasn't fully explored whole-brain network properties in relation to AoA. The current study addresses this gap by applying whole-brain network analyses, moving beyond localized studies to examine global network efficiency and modularity. This approach provides a more comprehensive understanding of how bilingualism affects brain organization across multiple regions and systems.

This study employed a retrospective analysis of resting-state fMRI data from 151 participants (19 monolinguals, 59 late bilinguals, 34 early bilinguals, and 39 simultaneous bilinguals). Data acquisition utilized a 3-Tesla Siemens scanner with a 32-channel head coil. Resting-state fMRI consisted of T2-weighted echo-planar imaging (EPI) sequences. Participants were instructed to keep their eyes open and fixate on a cross. High-resolution T1-weighted images (MPRAGE sequence) were also acquired for anatomical reference. Functional data preprocessing involved standard steps using the CONN toolbox, including realignment, unwarping, outlier identification, segmentation, normalization to MNI space, and smoothing with a 6mm FWHM Gaussian kernel. Confounding effects from physiological noise (aCompCor), motion parameters, and identified outlier scans were regressed from the fMRI time series. Brain network features, including global efficiency (E) and modularity (Q), were assessed using graph theoretical analyses on 374 brain regions (333 cortical, 15 subcortical, 26 cerebellar) from CONN's Harvard-Oxford template. These regions were further divided into 14 modules. Functional connectivity between each pair of regions was computed as the Pearson's correlation of their fMRI signals, followed by Fisher's r-to-z transformation. Negative edges were discarded before calculating E and Q using weighted formulas. Pairwise group differences in functional connectivity were tested using Network-Based Statistics (NBS). Statistical analyses included ANOVAs to compare group differences in global efficiency and modularity, and correlations to examine the relationship between AoA and network measures.

The study's key findings demonstrate that early and simultaneous bilinguals exhibit significantly higher global efficiency compared to monolinguals. This difference was not observed in late bilinguals. No significant group differences were found for modularity. A significant negative correlation between AoA and global efficiency was found within the bilingual group, indicating that earlier AoA is associated with higher network efficiency. Network-based statistics (NBS) analyses revealed that this enhanced efficiency in early and simultaneous bilinguals is primarily due to increased functional connectivity between the cerebellum and several association networks, including the default mode, dorsal and ventral attention, fronto-parietal, and sensorimotor-hand networks. Simultaneous bilinguals showed stronger connectivity between the cerebellum and these association networks compared to monolinguals. Early bilinguals showed similar, but slightly less extensive, cerebellar connectivity enhancements. Further analysis revealed that a significantly higher proportion of these increased connections in simultaneous bilinguals were inter-hemispheric rather than intra-hemispheric. No significant relationships were found between global efficiency, modularity, or functional connectivity and L2 proficiency, years of bilingual experience, or music training.

The results support the hypothesis that early bilingual experience enhances the global efficiency of brain networks. The finding that increased connectivity between the cerebellum and cortical association networks underlies this enhanced efficiency highlights the importance of cortico-cerebellar circuits in bilingual language processing. The lack of an effect for modularity suggests that the cognitive advantages of bilingualism may not be related to increased specialization of brain regions, but rather to the enhanced integration and interaction between different brain modules. The negative correlation between AoA and global efficiency emphasizes the role of early language exposure in shaping brain network organization. The finding that neither L2 proficiency nor years of experience influenced network measures suggests that the critical factor is the timing of language acquisition during a sensitive period of development. These results extend previous research by demonstrating the importance of the cortico-cerebellar system and interhemispheric connectivity in the bilingual brain. The study contributes to a deeper understanding of how language learning experience shapes brain architecture and optimizes information processing.

This study demonstrates that early and simultaneous bilingualism enhances global brain network efficiency, primarily driven by increased inter-hemispheric cortico-cerebellar connectivity. The age of second language acquisition is a key factor, highlighting the importance of early language exposure for optimizing brain network organization. Future research could explore the impact of learning multiple languages beyond two, investigate the influence of specific language pairs, and further investigate the microstructural and biochemical mechanisms contributing to these network changes.

The retrospective nature of the study and the reliance on self-reported AoA are limitations. The sample, while large, was primarily composed of French-English bilinguals in Montreal, limiting the generalizability of findings to other bilingual populations or language pairs. The study focused on functional connectivity, and future research could integrate structural connectivity data to provide a more complete picture of brain organization in bilinguals.