Multiscale neural features of tonal bilingualism: linking regional differences in brain network degree centrality to neurotransmitter-gene signatures in Bai-Mandarin bilinguals

Understanding neural mechanisms of tonal language processing is crucial for revealing language-specific brain adaptations, particularly in tonal bilinguals. While hemispheric differences have been identified, network-level mechanisms and their underlying multiscale biological bases remain unclear. Using resting-state fMRI data from Bai-Mandarin bilinguals (BMB) and Mandarin monolinguals (MM), this study investigated brain network topology through degree centrality (DC) analysis, followed by neurotransmitter mapping and transcriptomic analyses. BMB exhibited significantly lower DC in the left middle frontal gyrus (MFG), left inferior parietal lobule (IPL), and left middle temporal gyrus (MTG), but higher DC in bilateral medial prefrontal cortex (mPFC). These differences predominantly manifested across higher-order cognitive networks, including the frontoparietal network (FPN), dorsal attention network (DAN), and default mode network (DMN). Neurotransmitter mapping explained 37% of the group-level variance in DC, with significant contributions from serotonin transporter (5-HTT), dopamine receptors (D1, D2), and γ-aminobutyric acid (GABA) systems. Transcriptomic analysis revealed 1,801 genes associated with DC differences (30.07% variance explained), enriched in protein localization, transport, and cellular morphogenesis, with differential expression evident in microglia, excitatory and inhibitory neurons. These findings reveal that tonal bilingualism shapes brain network architecture through coordinated multiscale mechanisms, providing novel insights into the neurobiological basis of tonal language processing.