Idiosyncratic navigation determines mouse CA1 representational structure in a multicompartment environment

Organisms from mice to humans rely on cognitive maps instantiated by the hippocampal formation to flexibly and efficiently navigate the world. Traditional theories of cognitive mapping posit that these representations encode geometric relationships among their contents, while recent alternative theories propose that they encode the predictive relationships among their contents that the navigator experiences. Here, we leverage longitudinal miniscope calcium imaging of CA1 in mice navigating a multicompartment environment to adjudicate between predictions of these theories. We find that different mice instantiate different representational structures across identical compartments. Within mouse, compartments with more similar navigational patterns on a particular spatiotemporal scale are represented more similarly, accounting for these individual differences. Finally, we demonstrate that manipulating navigational patterns on this scale induces a corresponding change in CA1 representational structure. Together, these results demonstrate that idiosyncratic navigation is a key determinant of hippocampal representational structure, consistent with predictive theories of cognitive mapping.