Development of anterior hippocampal integration underlies the protracted emergence of cognitive map formation and generalization

Abstract Flexible memory depends on integrating experiences across time and space into cognitive maps—holistic representations that support flexible navigation and generalization. Although the anterior hippocampus is thought to support integration across broad spatiotemporal scales, it matures relatively late, suggesting that its functional development may be key to mature cognitive mapping. Here, we show that anterior hippocampal integration, indexed by temporal autocorrelation of fMRI activation, undergoes prolonged development and predicts age-related improvements in spatial memory. In a large resting-state sample (N=382; aged 5-34 years), temporal autocorrelation increased with age in anterior but not posterior hippocampus. We replicated this anterior pattern in an independent, task-based sample (N=85; aged 6-12 years and adults). Moreover, we linked hippocampal integration to behavior using a spatial navigation task that required participants to adapt to rotations of a virtual environment across learning runs as well as generalize learned cognitive maps when new objects were introduced. Children exhibited lower anterior autocorrelation and re-learned object positions when the environment changed. In adolescents, increasing anterior hippocampal autocorrelation was accompanied by gradual behavioral improvements in locating objects in the face of environmental change. Adults showed the greatest anterior hippocampal autocorrelation, which uniquely supported accurate spatial memory performance through efficient path navigation in the changing environment. These findings identify spatiotemporal integration in anterior hippocampus as a key mechanism underlying the developmental shift from local representation of individual positions in an environment to formation of flexible cognitive maps that are robust and generalizable in the face of environmental change. Significance Statement A hallmark of cognitive development is the formation of increasingly rich knowledge representations that capture similarities across experiences and guide decision making in new situations. Here, we link such emerging cognitive flexibility to anterior hippocampus development. We show that anterior hippocampus integrates information across broader spatiotemporal scales with age. Furthermore, we show that such increasing anterior hippocampal integration capacity underlies behavioral improvements in spatial memory and navigation. In the face of environmental change, anterior hippocampal integration allows adults to continue to navigate accurately, whereas children and adolescents must relearn the environmental layout each time it changes. These findings indicate that anterior hippocampus development supports a qualitative shift from local, individual memory representation to global, complex knowledge formation into emerging adulthood. Competing Interest Statement The authors have declared no competing interest.