Hippocampal and cortical oscillations support the encoding of event memories during movie watching

Abstract

Remembering temporally-extended experiences requires integrating information over time into coherent event representations that can be stored and later retrieved. Oscillatory dynamics may provide a flexible mechanism to support these operations by coordinating communication across regions and organizing neural activity in time. Yet most evidence for the oscillatory basis of episodic encoding comes from discrete-stimulus paradigms, leaving unclear whether these mechanisms can help organize memory during continuous experience. Using iEEG recorded while participants watched a 50-min film, we measured how power, synchrony and phase alignment support memory formation at the beginning, middle, and end of the events. At event onset, remembered events showed reduced gamma power with increased hippocampal-frontal synchrony, indicating that successful events begin with transient long-range coordination rather than heightened local processing. Within an event, memory was predicted by the direction of change, with recalled events showing increases in temporal gamma power and hippocampal-temporal gamma synchrony, consistent with the progressive binding of incoming information into a developing event representation. At the end of an event, memory was supported by an increase in hippocampal theta power and phase resetting. Temporal gamma power was likewise elevated and hippocampal-temporal gamma synchrony increased, suggesting that information bound locally over the course of the event might be transmitted to the hippocampus as the event closes. Frontal beta power decreased at the same moment, consistent with disruption of the outgoing event model. Naturalistic memory formation therefore does not rest on a sustained encoding state, but on the appropriate temporal coordination and stability of oscillatory states across brain regions and event phases, in which stable oscillatory states support ongoing representation while transient, boundary-driven reorganization of hippocampal-cortical networks switches the system between consolidating the completed event and encoding the next.