An enduring role for hippocampal pattern completion in addition to an emergent non-hippocampal contribution to holistic episodic retrieval after a 24-hour delay

Abstract

Episodic memory retrieval is associated with the holistic neocortical reinstatement of all event information; an effect driven by hippocampal pattern completion. However, whether holistic reinstatement occurs, and whether hippocampal pattern completion continues to drive reinstatement, after a period of consolidation is unclear. Theories of systems consolidation predict either a time-variant or -invariant role of the hippocampus in the holistic retrieval of episodic events. Here, we assessed whether episodic events continue to be reinstated holistically and whether hippocampal pattern completion continues to facilitate holistic reinstatement following a period of consolidation. Female and male human participants learnt ‘events’ that were composed of multiple overlapping pairs of event elements (e.g., person-location, object-location, location-person). Importantly, encoding occurred either immediately before or 24-hours before retrieval. Using fMRI during the retrieval of events, we show evidence for holistic reinstatement, as well as a correlation between reinstatement and hippocampal pattern completion, regardless of whether retrieval occurred immediately or 24-hours after encoding. Thus, hippocampal pattern completion continues to contribute to holistic reinstatement after a delay. However, our results also revealed that some holistic reinstatement can occur without evidence for a corresponding signature of hippocampal pattern completion after a delay (but not immediately after encoding). We therefore show that hippocampal pattern completion, in addition to a non-hippocampal process, has a role in holistic reinstatement following a period of consolidation. Our results point to a consolidation process where the hippocampus and neocortex may work in an additive, rather than compensatory, manner to support episodic memory retrieval.Significance StatementThe hippocampus plays a critical role in the recollection of episodic events. However, its role in episodic memory retrieval over time is still debated with theories of systems consolidation predicting both a time-limited and time-invariant role. We used fMRI and an experimental assay of holistic episodic memory retrieval to assess hippocampal pattern completion and its relationship to neocortical reinstatement across delay. We provide evidence that hippocampal pattern completion is associated with neocortical reinstatement following delay, but that some reinstatement can occur without a corresponding signature of hippocampal pattern completion. Our results suggest that hippocampal pattern completion, in addition to an emergent non-hippocampal process, may play an additive role in the recollection of episodic memories following a period of consolidation.