Mechanisms of Memory Retrieval in Slow-Wave Sleep

Abstract

Study ObjectivesMemories are strengthened during sleep. The benefits of sleep for memory can be enhanced by re-exposing the sleeping brain to auditory cues; a technique known as targeted memory reactivation (TMR). Prior studies have not assessed the nature of the retrieval mechanisms underpinning TMR: the matching process between auditory stimuli encountered during sleep and previously encoded memories. We carried out two experiments to address this issue.MethodsIn Experiment 1, participants associated words with verbal and nonverbal auditory stimuli before an overnight interval in which subsets of these stimuli were replayed in slow-wave sleep. We repeated this paradigm in Experiment 2 with the single difference that the gender of the verbal auditory stimuli was switched between learning and sleep.ResultsIn Experiment 1, forgetting of cued (vs. noncued) associations was reduced by TMR with verbal and nonverbal cues to similar extents. In Experiment 2, TMR with identical nonverbal cues reduced forgetting of cued (vs. noncued) associations, replicating Experiment 1. However, TMR with nonidentical verbal cues reduced forgetting of both cued and noncued associations.ConclusionsThese experiments suggest that the memory effects of TMR are influenced by the acoustic overlap between stimuli delivered at training and sleep. Our findings hint at the existence of two processing routes for memory retrieval during sleep. Whereas TMR with acoustically identical cues may reactivate individual associations via simple episodic matching, TMR with nonidentical verbal cues may utilize linguistic decoding mechanisms, resulting in widespread reactivation across a broad category of memories.

Contextual priming of word meanings is stabilized over sleep

“…Furthermore priming based on similarity at a surface level may have a slower, more effortful mechanism than priming that relies on match at an abstract level (e.g., McLennan & Luce, 2005). Our proposal based on the current evidence is that word-meaning priming is supported the same medial temporal lobe circuitry that underpins paired-associate learning, which at least in part may have a more abstract element (Cairney, Sobczak, Lindsay, & Gaskell, 2017), linking the words at a lexical or conceptual level rather than a more superficial level.…”

Memory consolidation is linked to spindle-mediated information processing during sleep

“…Likewise, replaying verbal foreign language cues facilitates the retrieval of cued (vs. non-cued) vocabulary translations 19,20 . These findings are supplemented by a range of behavioural 21,22 , neuropsychological 23 and neuroimaging 24 studies, indicating that TMR can be used to selectively strengthen declarative memories.…”

Memory Consolidation Is Linked to Spindle-Mediated Information Processing during Sleep

“…Previous research has established the role of non-rapid eye movement (NREM) sleep, along with its electrophysiological signatures of slow oscillations (SOs) and spindles, for memory consolidation [ 1 , 2 , 3 , 4 ]. In related work, experimental manipulations have demonstrated that NREM sleep provides a window of opportunity to selectively strengthen particular memory traces via the delivery of auditory cues [ 5 , 6 , 7 , 8 , 9 , 10 ], a procedure known as targeted memory reactivation (TMR). It has remained unclear, however, whether TMR triggers the brain’s endogenous consolidation mechanisms (linked to SOs and/or spindles) and whether those mechanisms in turn mediate effective processing of mnemonic information.…”