ASSOCIATIVE MEMORY SHAPES HIPPOCAMPAL LATENT DYNAMICS TO BIAS FLEXIBLE ENCODING OF NEW COGNITIVE MAPS

Early theories of hippocampal function were centered on a putative split between space and memory. Today, cognitive maps and associative memories are better understood as two descriptions of the same underlying relational coding system in the hippocampus, implemented by overlapping neuronal populations with graded specialization rather than segregated networks. If this is the case, however, a critical question remains unresolved: how do these two functions dynamically interact across experience? Specifically, how does the encoding and consolidation of an associative memory reshape the formation and stabilization of a novel cognitive map, and how does it interact with previously established ones? Using calcium imaging in freely behaving mice, we find that spatial representations and associative memory engrams are encoded within overlapping neuronal populations in hippocampal CA3. Fear learning, as a form of associative engram formation within this shared circuitry, biases the representational progression of new cognitive maps, promoting early map precision while reducing experience-dependent reorganization over time. This effect is mediated by changes in the latent dynamics of CA3 population activity, and promotes flexible remapping across subsequent re-exposures to the same context, which is expressed as reduced alignment of manifold trajectories across days. Together, these results reveal that associative memory formation can dynamically enhance the plasticity of hippocampal networks during the encoding and stabilization of new spatial representations, and demonstrate that cognitive maps and associative memories are implemented within a shared hippocampal representational system where they interact through state-dependent modulation of learning dynamics rather than competition for neuronal resources.