The human hippocampus retroactively binds experiences across time

Abstract

Creating memories requires linking events across seconds and minutes, but canonical mechanisms of associative plasticity operate over much shorter timescales. This poses a fundamental problem: how can the brain bind information that arrives at different times? Computational model and animal studies implicate the hippocampus in associating events across time, but when the hippocampus becomes engaged and how it interacts with representations of preceding events are unknown. Here we show, using intracranial recordings in humans forming image-word associations across a ~2-s temporal gap, that hippocampal high-frequency activity predicts later memory when the second event arrives, but not during the initial image or intervening delay. At this moment, neurons tuned to the preceding image reinstate stimulus-specific firing despite its sensory absence. Across trials, hippocampal high-frequency activity was selectively coupled to this reinstatement during successful encoding and increased before spiking of image-tuned neurons. These findings reveal a retroactive mode of hippocampal binding, whereby representations of preceding events are recruited when new information arrives. This mechanism provides a neural solution for binding experiences across the temporal discontinuities that characterize everyday life.