Cited by 66Sleep and Wakefulness ResearchMemory and Neural MechanismsMemory Processes and Influences

Targeted memory reactivation during sleep elicits neural signals related to learning content

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Wang, Boyu, Antony, James W., Lurie, Sarah, Brooks, Paula P., Paller, Ken A., Norman, Kenneth A.·2019·The Journal of Neuroscience

Published version of a preprint

Abstract

Retrieval of learning-related neural activity patterns is thought to drive memory stabilization. However, finding reliable, noninvasive, content-specific indicators of memory retrieval remains a central challenge. Here, we attempted to decode the content of retrieved memories in the EEG during sleep. During encoding, male and female human subjects learned to associate spatial locations of visual objects with left- or right-hand movements, and each object was accompanied by an inherently related sound. During subsequent slow-wave sleep within an afternoon nap, we presented half of the sound cues that were associated (during wake) with left- and right-hand movements before bringing subjects back for a final postnap test. We trained a classifier on sleep EEG data (focusing on lateralized EEG features that discriminated left- vs right-sided trials during wake) to predict learning content when we cued the memories during sleep. Discrimination performance was significantly above chance and predicted subsequent memory, supporting the idea that retrieval leads to memory stabilization. Moreover, these lateralized signals increased with postcue sleep spindle power, demonstrating that retrieval has a strong relationship with spindles. These results show that lateralized activity related to individual memories can be decoded from sleep EEG, providing an effective indicator of offline retrieval. SIGNIFICANCE STATEMENT Memories are thought to be retrieved during sleep, leading to their long-term stabilization. However, there has been relatively little work in humans linking neural measures of retrieval of individual memories during sleep to subsequent memory performance. This work leverages the prominent electrophysiological signal triggered by lateralized movements to robustly demonstrate the retrieval of specific cued memories during sleep. Moreover, these signals predict subsequent memory and are correlated with sleep spindles, neural oscillations that have previously been implicated in memory stabilization. Together, these findings link memory retrieval to stabilization and provide a powerful tool for investigating memory in a wide range of learning contexts and human populations.

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Crossref · 10.1523/jneurosci.2798-18.2019

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Authors
Wang, B., Antony, J. W., Lurie, S., Brooks, P. P., Paller, K. A., & Norman, K. A.
Affiliations
  • Princeton University (US)
  • Northwestern University (US)
Venue
The Journal of Neuroscience
Published
2019-06-24
Volume
39
Issue
34
Pages
6728-6736
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2953473680
Cited by
66
References
35
Citations by year
2026: 2 · 2025: 13 · 2024: 10 · 2023: 10 · 2022: 13 · 2021: 5 · 2020: 8 · 2019: 5
FWCI
4.51
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Science Foundation (1461088, 1533511)
  • National Institute on Aging (R01AG017139)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords
targeted memory reactivation, sleep, memory retrieval, memory stabilization, sleep spindles, slow-wave sleep, EEG decoding, associative learning, memory prediction, neural oscillations
MeSH terms
Memory Consolidation, Adolescent, Adult, Cues, Electroencephalography, Female, Humans, Functional Laterality, Learning, Male, Memory, Movement, Mental Recall, Sleep, Young Adult

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