Coordinated representational reinstatement in the human hippocampus and lateral temporal cortex during episodic memory retrieval

Abstract

Theoretical models of episodic memory have proposed that retrieval depends on interactions between the hippocampus and neocortex, where hippocampal reinstatement of item-context associations drives neocortical reinstatement of item information. Here, we simultaneously recorded intracranial EEG from hippocampus and lateral temporal cortex (LTC) of epilepsy patients who performed a virtual reality spatial navigation task. We extracted stimulus-specific representations of both item and item-context associations from the time-frequency patterns of activity in hippocampus and LTC. Our results revealed a double dissociation of representational reinstatement across time and space: an early reinstatement of item-context associations in hippocampus preceded a later reinstatement of item information in LTC. Importantly, reinstatement levels in hippocampus and LTC were correlated across trials, and the quality of LTC reinstatement was predicted by the magnitude of phase synchronization between hippocampus and LTC. These findings confirm that episodic memory retrieval in humans relies on coordinated representational interactions within a hippocampal-neocortical network.

Electrophysiological signatures of memory reactivation in humans

“…The authors interpreted this result as reflecting hippocampal pattern completion processes. Estefan et al [55] recorded from the hippocampus and the lateral temporal cortex and could show that item-specific reinstatement in the lateral temporal cortex was preceded by the reactivation of item-context associations in the hippocampus, which could be described as pattern completion. They also show increased levels of cortico-hippocampal communication alongside the reinstatement periods, which is in line with the idea that the hippocampus triggers cortical reinstatement during memory reactivation.…”

Event conjunction: How the hippocampus integrates episodic memories across event boundaries

“…Our framework would predict that this effect arises regardless of whether the event is later remembered, as the maintenance of the theta‐gamma code is essential to comprehending the ongoing event. The original theta‐gamma code should be detectable during the unfolding of the second event . Our framework posits that the original event is rapidly reactivated (Michelmann, Staresina, Bowman, & Hanslmayr, ; Pacheco Estefan et al, ; Yaffe, Shaikhouni, Arai, Inati, & Zaghloul, ) and reconstructed within the hippocampus when a related event begins. Therefore, we speculate that the original theta‐gamma code should be detected during the second event.…”

A mechanism for hippocampal memory recall based on excitatory-inhibitory fluctuations in neocortex

“…This reciprocal anatomical connectivity equips the hippocampus with the necessary architecture to coordinate activity with neocortex, thus providing a 'memory index', or summary sketch, for information stored across distributed cortical circuits [7][8][9] . Consistent with this view, during memory recall hippocampal reinstatement predicts subsequent neocortical reinstatement 10 .…”