Characterizing the temporal dynamics and maturation of brain activity during sleep: an EEG microstate study in preterm and full-term infants

Abstract

By interfering with the normal sequence of mechanisms serving the brain maturation, premature birth and related stress can alter perinatal experiences, with potential long-term consequences on a child's neurodevelopment. The early characterization of brain functioning and maturational changes is thus of critical interest in premature infants who are at high risk of atypical outcomes and could benefit from early diagnosis and dedicated interventions. Using high-density electroencephalography (HD-EEG), we recorded resting-state brain activity in extreme and very preterm infants at the equivalent age of pregnancy term (n=43), and longitudinally 2-months later (n=33), compared with full-term born infants (n=14). We characterized the maturation of brain activity by using microstate analysis (a method to quantify the spatiotemporal dynamics of the spontaneous transient network activity) while controlling for vigilance states. The comparison of premature and full-term infants first showed slower dynamics as well as altered spatio-temporal properties of resting-state activity in preterm infants. Maturation of functional networks between term-equivalent age and 2 months later in preterms was translated by the emergence of richer dynamics, manifested in part by faster temporal activity (shorter duration of microstates) as well as an evolution in the spatial organization of the dominant microstates. The inter-individual differences in the temporal dynamics of brain activity at term-equivalent age were further impacted by gestational age at birth and sex (with slower microstate dynamics in infants with lower birth age and in boys) but not by other considered risk factors. This study highlights the potential of the microstate approach to reveal maturational properties of the emerging resting-state network activity in premature infants.