Distinct developmental changes in linear and nonlinear neural interactions across infancy and adulthood

Abstract

The development of functional brain connectivity during early life depends on social experience and is best understood in the context of interactions with a caregiver. It is still an open question to what extent distinct modes of functional connectivity dominate in different stages of human brain development, and whether cognitive tasks can differentially modulate them. Using electroencephalography (EEG), we investigated the development of linear and nonlinear functional brain connectivity in infants and adults while they socially interacted. Using simultaneous EEG recordings in parent-infant dyads performing two different experiments (N = 160; 80 adults and 80 infants), we computed functional connectivity capturing distinct dynamics: a linear measure capturing phase synchronization (weighted phase lag index; WPLI), and a nonlinear measure capturing information sharing (weighted symbolic mutual information; WSMI). In both tasks, adults showed higher WSMI than infants, whereas infants showed higher WPLI than adults. Moreover, infant age predicted only task-related connectivity values computed with the nonlinear measure and not with its linear counterpart, suggesting that the information-theoretic measure was more sensitive to developmental changes in task-relevant neural processing. These findings suggest that over development, a shift in dominance from linear to nonlinear modes of brain communication may be essential for supporting emerging higher cognitive abilities, such as precursors to executive function (here, attention shifting) and social decision-making. Further, this work highlights the importance of using nonlinear measures in addition to traditional linear ones, which collectively permit a more robust capture of maturational changes.