Dentate gyrus population activity during immobility drives formation of precise memories

All vertebrates are capable of generating dissimilar patterns of neuronal activity from similar sensory-driven input patterns, a phenomenon called pattern separation. It is unclear, however, how these separated patterns are transformed into lasting memories that retain the initial discrimination. Using dual-color in-vivo two-photon Ca2+ imaging, we show that the dentate gyrus, a region implicated in pattern separation, generates in immobile mice sparse, synchronized activity patterns driven by entorhinal cortex activity. These population events are structured and modified by changes in the environment; they incorporate place- and speed cells and are similar to population patterns evoked during self-motion. Inhibiting only granule cells in immobile mice impairs formation of pattern-separated memories. These patterns, thus, support the creation of precise memories by replaying the population codes of the current environment on a short time scale.