The world through a child’s eyes. The hippocampus builds personalized spatial maps that integrate prominent features in the environment and self-generated information such as body position, elapsed time, and distance traveled. Previous studies showed that representations centered on the external world emerge around the third postnatal week in rodents. But when do self-centered representations of the environment appear? In this study, the authors show that the coding of elapsed time, followed by the coding of distance traveled, emerges about a week later. This surprisingly late maturation occurs despite the fact that juveniles are already highly active at this age. The findings suggest that the brain’s representation of personal experience develops on a very different timetable from its representation of the external world.

Authors: Leprince, Filippi, Mantez, Dard, Dichio, Majnik, Cretella, Bocchio, Picardo, Monasson, Platel & Cossart

Scientific abstract: The hippocampus generates cognitive maps through two distinct mechanisms: external representations anchored to environmental landmarks and internal sequences integrating self-referenced information. In adult CA1, these functions segregate radially, with deep cells processing external cues and superficial cells handling internal representations. This anatomical organization suggests that developmental processes constrain the formation of these functionally distinct circuits. However, the developmental timeline for the emergence of these two types of hippocampal representations remains unknown. Using longitudinal two-photon calcium imaging in head-fixed mice during the fourth postnatal week, we investigated when internal vs. external hippocampal representations emerge. We recorded from deep and superficial CA1 layers while mice ran on treadmills that were bare or enriched with tactile cues, addressing the challenge of tracking cells across sessions. Internal sequences emerged during the mid-fourth postnatal week, following the development of cue-based representations. These sequences initially encoded elapsed time before evolving to integrate run distance, arising after rest cell assemblies, as spatial coding and functional connectivity networks stabilized. These findings identify the fourth postnatal week as a critical developmental period marking the establishment of a balanced integration between external landmark-based and internal self-referenced spatial representations. This transition period may constitute a vulnerable developmental window during which disruptions could predispose to disorders characterized by altered cognitive maps.

Published in Current Biology, 2026