Abstract
Consolidation stabilizes memory traces after initial encoding. Rodent studies suggest that memory consolidation depends on replay of stimulus-specific activity patterns during fast hippocampal “ripple” oscillations. Here, we measured replay in intracranial electroencephalography recordings in human epilepsy patients, and related replay to ripples. Stimulus-specific activity was identified using representational similarity analysis and then tracked during waking rest and sleep after encoding. Stimulus-specific gamma (30–90 Hz) activity during early (100–500 ms) and late (500–1200 ms) encoding is spontaneously reactivated during waking state and sleep, independent of later memory. Ripples during nREM sleep, but not during waking state, trigger replay of activity from the late time window specifically for remembered items. Ripple-triggered replay of activity from the early time window during nREM sleep is enhanced for forgotten items. These results provide the first electrophysiological evidence for replay related to memory consolidation in humans, and point to a prominent role of nREM ripple-triggered replay in consolidation processes.
Highlights
Consolidation stabilizes memory traces after initial encoding
Areas of the medial temporal lobe including the hippocampus[10] and parahippocampal gyrus[12] showed increased blood oxygen level dependent (BOLD) responses in functional magnetic resonance imaging when the cues were presented during sleep, consistent with reactivation of previously acquired memory traces
Our results show that stimulus-specific information is spontaneously replayed during both waking state and non-rapid eye movement (nREM) sleep, but these general replay levels do not predict later memory
Summary
Consolidation stabilizes memory traces after initial encoding. Rodent studies suggest that memory consolidation depends on replay of stimulus-specific activity patterns during fast hippocampal “ripple” oscillations. Ripples during nREM sleep, but not during waking state, trigger replay of activity from the late time window for remembered items. Replay was observed during both waking state and sleep, in apparent conflict with behavioral data showing that sleep—in particular, non-rapid eye movement (nREM) sleep—benefits memory consolidation[18,19,20,21,22] These studies provided first evidence for replay in humans and showed that the amount of replay was related to subsequent memory performance[14,15,23]. By contrast, rippletriggered replay of activity from late encoding stages (500–1200 ms after stimulus onset) occurs for items that are later remembered, and only during nREM sleep These findings suggest a mechanistic explanation for the beneficial role of sleep for memory consolidation
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