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

• Published in: Nature communications Vol. 9; no. 1; pp. 3920 - 11
• Main Authors: Schapiro, Anna C., McDevitt, Elizabeth A., Rogers, Timothy T., Mednick, Sara C., Norman, Kenneth A.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 25.09.2018; Nature Publishing Group; Nature Portfolio
• Subjects: 59/36; 631/378/1385/2644; 631/378/1595/1554; 631/378/1595/2638; 631/378/2649; Adult; Cognitive ability; Female; Functional magnetic resonance imaging; Hippocampus; Hippocampus - physiology; Humanities and Social Sciences; Humans; Learning; Learning - physiology; Magnetic resonance imaging; Magnetic Resonance Imaging - methods; Male; Memory; Memory - physiology; multidisciplinary; Pattern analysis; Performance prediction; Rest; Rest - physiology; Satellites; Scanners; Science; Science (multidisciplinary); Sleep; Sleep - physiology; Wakefulness - physiology; Young Adult
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-018-06213-1

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. The hippocampus is known to 'replay' experiences and memories during rest periods, but it is unclear how particular memories are prioritized for replay. Here, the authors show that information that is remembered less well is replayed more often, suggesting that weaker memories are selected for replay.