The ontogeny of hippocampal spatial memory is supported by postnatal Cajal-Retzius cells

Abstract

The functional capabilities of the adult hippocampus depend on specialized circuits that are established during development. Cajal-Retzius (CR) cells persist in the hippocampus long after their disappearance from the neocortex and contribute to the postnatal maturation of hippocampal circuits, but how this developmental role shapes adult hippocampal function remains unknown. Here, we selectively ablated CR cells from the postnatal hippocampus and examined the consequences for spatial learning, navigation, and CA1 spatial representations. CR-cell ablated animals learned reward locations and adapted to changing task conditions, but learned more slowly and made more errors. Reinforcement-learning models suggest that these behavioral differences reflect less stable internal representations guiding behavior. Consistent with this, CA1 spatial representations remained present but were more unstable and showed reduced differentiation of reward locations, particularly when task conditions changed. Our findings identify postnatal CR cells as key developmental contributors to the stability of hippocampal spatial representations and the adaptive behavior they support.