Dynamic brain architectures in local brain activity and functional network efficiency associate with efficient reading in bilinguals

The human brain is organized as a dynamic network, in which both regional brain activity and inter-regional connectivity support high-level cognitive processes, such as reading. However, it is still largely unknown how the functional brain network organizes to enable fast and effortless reading processing in the native language (L1) but not in a non-proficient second language (L2), and whether the mechanisms underlying local activity are associated with connectivity dynamics in large-scale brain networks. In the present study, we combined activation-based and multivariate graph-theory analysis with functional magnetic resonance imaging data to address these questions. Chinese-English unbalanced bilinguals read narratives for comprehension in Chinese (L1) and in English (L2). Compared with L2, reading in L1 evoked greater brain activation and recruited a more globally efficient but less clustered network organization. Regions with both increased network efficiency and enhanced brain activation in L1 reading were mostly located in the fronto-temporal reading-related network (RN), whereas regions with decreased global network efficiency, increased clustering, and more deactivation in L2 reading were identified in the default mode network (DMN). Moreover, functional network efficiency was closely associated with local brain activation, and such associations were also modulated by reading efficiency in the two languages. Our results demonstrate that an economical and integrative brain network topology is associated with efficient reading, and further reveal a dynamic association between network efficiency and local activation for both RN and DMN. These findings underscore the importance of considering interregional connectivity when interpreting local BOLD signal changes in bilingual reading.