Anterior hippocampal integration tracks the developmental emergence of flexible navigation through changing environments

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 humans. In a large resting-state fMRI sample (N = 382; ages 5-34 years; 174 females, 208 males), temporal autocorrelation increased with age in anterior, but not posterior, hippocampus. This anterior-specific pattern was replicated in an independent task-based fMRI sample (N = 83; aged 6-12 years and adults; 41 females, 42 males), 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 objects. 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 navigation trajectories. 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.