Dual-mode dynamics in hippocampal populations enable rapid and precise spatial coding

Hippocampal spatial representations emerge within minutes of first exposure to novel environments, challenging models based solely on gradual synaptic plasticity. Here, we show that CA1 spatial coding is organized according to a dual-mode architecture comprising a pre-organized backbone and an experience-dependent component. Backbone cells expressing immediately emerging place fields form a stable spatial scaffold and dominate positional decoding from the first traversal, whereas experience-dependent cells bearing gradually emerging fields are progressively incorporated to refine spatial representations. Analyses of ensemble activity further reveal that offline dynamics prospectively organize future spatial coding. In backbone cells, latent tuning aligns with their future place fields prior to task engagement, while in experience-dependent cells this alignment strengthens before overt place-field expression. Together, these findings identify a dual-mode organization of hippocampal populations in which offline dynamics pre-organize network activity to enable rapid and precise spatial coding in novel environments.