Dynamic transient brain states in preschoolers mirror parental report of behavior and emotion regulation

Abstract

The temporal dynamics of resting-state networks (RSNs) may represent an intrinsic functional repertoire supporting cognitive control performance across the lifespan (Kupis et al., 2021). However, little is known about brain dynamics during the preschool period, which is a sensitive time window for cognitive control development. The fast timescale of synchronization and switching characterizing cortical network functional organization gives rise to quasi-stable patterns (i.e., brain states) that recur over time. These can be inferred at the whole-brain level using Hidden Markov Models (HMMs), an unsupervised machine learning technique that allows the identification of rapid oscillatory patterns at the macro-scale of cortical networks (Vidaurre et al., 2018). The present study used a HMM technique to investigate dynamic neural reconfigurations and their associations with behavioral (i.e., parental questionnaires) and cognitive (i.e., neuropsychological tests) measures in typically developing preschoolers (4-6 years old). We used high density EEG to better capture the fast reconfiguration patterns of the HMM-derived metrics (i.e., switching rates, entropy rates, transition probabilities and fractional occupancies). Our results revealed that the HMM-derived metrics were reliable indices of individual neural variability and differed between boys and girls. However, only brain state transition patterns toward prefrontal and default-mode brain states, predicted differences on parental-report questionnaire scores. Overall, these findings support the importance of resting-state brain dynamics as functional scaffolds for behavior and cognition. Brain state transitions may be crucial markers of individual differences in cognitive control development in preschoolers. KeypointsO_LIHMM-derived metrics are reliable hallmarks of individual neural variability and show gender-related differences. C_LIO_LIBrain state transition patterns toward prefrontal and default-mode brain states predict differences on parental-report questionnaires scores. C_LIO_LIBrain state transitions may be crucial markers of individual differences in cognitive control development in preschoolers. C_LI