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

Abstract

Flexible memory depends on cognitive maps that integrate spatial relationships and guide behavior as environments change. The anterior hippocampus is well positioned to support integration across broad spatiotemporal scales, but its late maturation may constrain development of flexible, map-based navigation. Here, we tested whether hippocampal temporal autocorrelation, an index of neural activity stability over time, tracks the development of spatial integration. In a large resting-state fMRI sample (N = 382; ages 5-34 years), temporal autocorrelation increased with age in anterior, but not posterior, hippocampus. This anterior-specific pattern was replicated in an independent task-based fMRI sample of children, adolescents, and adults (N = 85; aged 6-12 years and adults), wherein we linked hippocampal autocorrelation to dissociable components of spatial behavior. The navigation task separated memory for object locations from the ability to update and generalize knowledge across rotations of the distal reference frame and to new object sets. Although all age groups learned object locations, only older participants showed evidence that prior spatial structure supported performance as the environment changed across runs. Critically, hippocampal autocorrelation related to behavior only when spatial knowledge was used across runs, rather than improved through within-run feedback, with the clearest profile emerging in adults. In adults, anterior and posterior autocorrelation jointly predicted precise object-location memory, whereas anterior autocorrelation uniquely predicted efficient trajectories from novel starting positions. These findings identify anterior hippocampal temporal autocorrelation as a later-maturing computation that supports the transition from local spatial learning in childhood to flexible navigation through changing environments in adulthood. Significance StatementFinding our way through the world requires more than remembering where things are. We also need to use what we have learned to take new routes, adjust when familiar places change, and apply old knowledge to new situations. These abilities improve from childhood to adulthood, but the brain changes that support this transition remain unclear. We show that a signal in anterior hippocampus, a brain region important for linking experiences, becomes more stable over development. Using a navigation task that separated remembering object locations from flexibly using a map, we found that this signal was most strongly tied to adults ability to navigate efficiently through changing environments. These findings reveal a hippocampal mechanism that supports flexible navigation as children mature.