Developmental Emergence of Replay-DMN Coordination Predicts Entorhinal Grid Codes

Abstract

Neural replay, the reactivation of experience-related activity patterns during offline periods, has been implicated in organising memories into cognitive maps. However, how replay processes mature through childhood and adolescence remains unclear. Here we studied 106 participants aged 8-25 who learned a hidden two-dimensional (2D) associative structure and then underwent magnetoencephalography (MEG) during a map-based inference task and post-task rest to detect spontaneous replay. We found that during post-task rest, younger individuals relied primarily on replay alone to represent the 2D relationships, whereas older individuals showed increasingly precise timing alignment between replay events and activity in the default mode network (DMN), particularly when replay occurred at the trough of a DMN theta oscillation. Such replay-DMN coupling predicted the strength of a grid-cell-like code in the entorhinal cortex identified in this cohort with fMRI. Furthermore, resting-state fMRI revealed that DMN functional connectivity strengthened with age, in parallel with reduced reliance on replay and more efficient inference performance. These results reveal a developmental progression in which replay shifts from an isolated process in youth to a coordinated DMN mechanism by adulthood. This transition predicts the maturation of grid-like schema representations, shedding light on how children gradually build internal knowledge structures to support flexible inference.