Human hippocampal replay during rest prioritizes weakly learned information and predicts memory performance

Abstract

The hippocampus replays experiences during quiet rest periods, and this replay benefits subsequent memory. A critical open question is how memories are prioritized for this replay. We used functional magnetic resonance imaging (fMRI) pattern analysis to track item-level replay in the hippocampus during an awake rest period after participants studied 15 objects and completed a memory test. Objects that were remembered less well were replayed more during the subsequent rest period, suggesting a prioritization process in which weaker memories—memories most vulnerable to forgetting—are selected for replay. In a second session 12 hours later, more replay of an object during a rest period predicted better subsequent memory for that object. Replay predicted memory improvement across sessions only for participants who slept during that interval. Our results provide evidence that replay in the human hippocampus prioritizes weakly learned information, predicts subsequent memory performance, and relates to memory improvement across a delay with sleep.

Awake reactivation and suppression after brief task exposure depend on task novelty

“…Even without such external modulator, it seems that the brain has its own selection mechanism. Recent study showed that the brain prioritizes weakly learned information and predicts later performance (Schapiro, McDevitt, Rogers, Mednick, & Norman, 2018). Together with this line of studies, the current study adds the evidence that the reactivation favors novel and salient information.…”

Multiple memories can be simultaneously reactivated during sleep as effectively as a single memory

“…Sequential learning-related spiking activity was shown to "replay" during sleep, and this phenomenon has since been connected to the off-line consolidation process 6 . In Humans, recent studies using multivariate pattern classification analysis in fMRI have also shown evidence for reactivation of cortical and hippocampal memory-related patterns during sleep and awake rest 7,8,9,10 .An important milestone in the study of sleep-related reactivation has been the development of targeted memory reactivation (TMR), a paradigm designed to reactivate specific memories by unobtrusively presenting learning-related cues during sleep 11 . TMR has been shown to improve various forms of learning, including spatial 12, 13 , skill 14, 15 and vocabulary 16 learning.…”

“…Sequential learning-related spiking activity was shown to "replay" during sleep, and this phenomenon has since been connected to the off-line consolidation process 6 . In Humans, recent studies using multivariate pattern classification analysis in fMRI have also shown evidence for reactivation of cortical and hippocampal memory-related patterns during sleep and awake rest 7,8,9,10 .…”

“…The reactivated item may be selected randomly with each presentation of a cue or there could be some systematic bias towards reactivating a specific item (e.g., weakly activated memories might more likely be reactivated 8,22 ). An extension of this hypothesis postulates that a small subset (i.e., more than one -but not all items) is reactivated and benefit.…”

Learning of distant state predictions by the orbitofrontal cortex in humans

“…Previous research in humans has found that hippocampal activity during reward learning co-varies with the activation of associated items in the visual cortex 12 and that hippocampal activity patterns represent retrieved information about currently cued target locations 50 . Recent papers have reported reactivation of hippocampal activity patterns during rest periods following learning 51,52 and that hippocampal activity co-varies with the reactivation of visual stimuli 53 . Interestingly, in recent work using MEG, an imaging method with much faster temporal resolution, Kurth-Nelson et al 54 reported that fast sequences of activity reflected potential trajectories in a non-spatial environment.…”