Theta-band brain synchronization supports the immediate and post-sleep dynamics of memory recall in children
Memory engrams emerge from dynamic, coordinated interactions among synchronized functional brain networks. Yet, how these networks are selectively reactivated upon cued recall and gradually (re)organized over time, especially through sleep, remains poorly understood. Using magnetoencephalography (MEG), sleep electroencephalography (EEG) and behavioral measures, we investigated the spatiotemporal neural dynamics of cued recall memory during immediate and post-sleep (i.e., 90-minute post-learning nap) recall sessions in school-aged children. Results showed that immediate recall engaged a temporally ordered sequence of theta-band phase synchronization across two transiently synchronized networks: an early (150-350 ms) network involving the ventral visual pathway and left medial temporal lobe (MTL), followed by a later (550-750 ms) network encompassing the bilateral MTL and widespread neocortical associative regions. Post-sleep recall was associated, relative to wakefulness, with strengthened theta-band phase synchronization between the left MTL and widespread bilateral neocortical regions in a similar late window (450-650 ms). Post-sleep theta-band synchronization and memory gains in performance positively correlated with slow oscillation-spindle coupling during the post-learning nap. Altogether, these findings highlight oscillatory and spatiotemporal dynamics of memory recall networks and suggest that sleep, possibly driven by slow-oscillation-spindle coupling mechanisms, supports the efficient reinstatement of memory traces in the developing brain.