Fast-timescale hippocampal processes bridge between slowly unfurling neocortical states during memory search

Prior behavioral work showed that event structure plays a key role in our ability to mentally search through memories of continuous naturalistic experience. We hypothesized that, neurally, this mem- ory search process involves a division of labor between slowly un- furling neocortical states representing event knowledge and fast hippocampal-neocortical communication that supports retrieval of new information at transitions between events. To test this, we tracked slow neural state-patterns in a sample of ten patients under- going intracranial electroencephalography as they viewed a movie and then searched their memories in a structured naturalistic in- terview. As patients answered questions (“after X, when does Y happen next?”), state-patterns from movie-viewing were reinstated in neocortex; during memory-search, states unfurled in a forward di- rection. Moments of state-transition were marked by low-frequency power decreases in cortex and preceded by power decreases in hip- pocampus that correlated with reinstatement. Connectivity-analysis revealed information-flow from hippocampus to cortex underpinning state-transitions. Together, these results support our hypothesis that fast hippocampal processes bridge between slow neocortical states during memory search.