Emergence of preconfigured and plastic time-compressed sequences in early postnatal development

When and how hippocampal neuronal ensembles first organize to support encoding and consolidation of memory episodes, a critical cognitive function of the brain, are unknown. We recorded electrophysiological activity from large ensembles of hippocampal neurons starting on the first day after eye opening as naïve rats navigated linear environments and slept. We found a gradual age-dependent, navigational experience-independent assembly of preconfigured trajectory-like sequences from persistent, location-depicting ensembles during postnatal week 3. Adult-like compressed binding of adjacent locations into trajectories during navigation and their navigational experience-dependent replay during sleep emerged in concert from spontaneous preconfigured sequences only during early postnatal week 4. Our findings reveal ethologically relevant distinct phases in the development of hippocampal preconfigured and experience-dependent sequential patterns thought to be important for episodic memory formation.