Long-term memories are linked to cortical representations of perceived events, but it is unclear which types of representations can later be recollected. Using magnetoencephalography-based decoding, we examined which brain activity patterns elicited during encoding are later replayed during recollection in the human brain. The results show that the recollection of images depicting faces and scenes is associated with a replay of neural representations that are formed at very early (180 ms) stages of encoding. This replay occurs quite rapidly, ϳ500 ms after the onset of a cue that prompts recollection and correlates with source memory accuracy. Therefore, long-term memories are rapidly replayed during recollection and involve representations that were formed at very early stages of encoding. These findings indicate that very early representational information can be preserved in the memory engram and can be faithfully and rapidly reinstated during recollection. These novel insights into the nature of the memory engram provide constraints for mechanistic models of long-term memory function.

Two primary functions attributed to the hippocampus and prefrontal cortex (PFC) network are retaining the temporal and spatial associations of events and detecting deviant events. It is unclear, however, how these two functions converge into one mechanism. Here, we tested whether increased activity with perceiving salient events is a deviant detection signal or contains information about the event associations by reflecting the magnitude of deviance (i.e., event saliency). We also tested how the deviant detection signal is affected by the degree of anticipation. We studied regional neural activity when people watched a movie that had varying saliency of a novel or an anticipated flow of salient events. Using intracranial electroencephalography from 10 patients, we observed that high-frequency activity (50–150 Hz) in the hippocampus, dorsolateral PFC, and medial OFC tracked event saliency. We also observed that medial OFC activity was stronger when the salient events were anticipated than when they were novel. These results suggest that dorsolateral PFC and medial OFC, as well as the hippocampus, signify the saliency magnitude of events, reflecting the hierarchical structure of event associations.

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