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Sleep-Dependent Facilitation of Episodic Memory Details

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van der Helm, Els, Gujar, Ninad, Nishida, Masaki, Walker, Matthew P.·2011·PLoS ONE
DOI 10.1371/journal.pone.0027421PMC PMC3219667
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Abstract

While a role for sleep in declarative memory processing is established, the qualitative nature of this consolidation benefit, and the physiological mechanisms mediating it, remain debated. Here, we investigate the impact of sleep physiology on characteristics of episodic memory using an item- (memory elements) and context- (contextual details associated with those elements) learning paradigm; the latter being especially dependent on the hippocampus. Following back-to-back encoding of two word lists, each associated with a different context, participants were assigned to either a Nap-group, who obtained a 120-min nap, or a No Nap-group. Six hours post-encoding, participants performed a recognition test involving item-memory and context-memory judgments. In contrast to item-memory, which demonstrated no between-group differences, a significant benefit in context-memory developed in the Nap-group, the extent of which correlated both with the amount of stage-2 NREM sleep and frontal fast sleep-spindles. Furthermore, a difference was observed on the basis of word-list order, with the sleep benefit and associated physiological correlations being selective for the second word-list, learned last (most proximal to sleep). These findings suggest that sleep may preferentially benefit contextual (hippocampal-dependent) aspects of memory, supported by sleep-spindle oscillations, and that the temporal order of initial learning differentially determines subsequent offline consolidation.

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Figure 1 Experimental design. Participants studied two lists of 50 words, one after the other. The two lists were each associated with a different set of contextual cues, making each list distinct. Subjects were then randomly assigned to the Nap- or No Nap-group, with participants in the Nap-group obtaining a 120 min sleep opportunity, while the No Nap-group performed standard daily activities. After 6 hours of offline consolidation time, both groups returned for a memory recognition test, where the 100 old items were presented together with a 100 intermixed foils (new items).
Figure 1 Experimental design. Participants studied two lists of 50 words, one after the other. The two lists were each associated with a different set of contextual cues, making each list distinct. Subjects were then randomly assigned to the Nap- or No Nap-group, with participants in the Nap-group obtaining a 120 min sleep opportunity, while the No Nap-group performed standard daily activities. After 6 hours of offline consolidation time, both groups returned for a memory recognition test, where the 100 old items were presented together with a 100 intermixed foils (new items).CC BY · PubMed Central
Figure 2 Memory performance and sleep association. A) Item-memory performance and B) context-memory performance for the No Nap- (clear bar) and Nap-group (filled bar). C) Within the Nap-group (filled bar in 2B) the extent of context-memory retention significantly correlated with total time spent in stage-2 sleep. Error bar represents s.e.m. * P<0.05 n.s. = non-significant.
Figure 2 Memory performance and sleep association. A) Item-memory performance and B) context-memory performance for the No Nap- (clear bar) and Nap-group (filled bar). C) Within the Nap-group (filled bar in 2B) the extent of context-memory retention significantly correlated with total time spent in stage-2 sleep. Error bar represents s.e.m. * P<0.05 n.s. = non-significant.CC BY · PubMed Central
Figure 3 The association in the Nap-group between context-memory retention and fast sleep spindles across the four electrode derivations (left top corner box label), with corresponding r- and P-values provided.
Figure 3 The association in the Nap-group between context-memory retention and fast sleep spindles across the four electrode derivations (left top corner box label), with corresponding r- and P-values provided.CC BY · PubMed Central
Figure 4 Context memory and sleep association. A) Context-memory performance in the No Nap- (clear bar) and Nap-group (filled bar) for List1, and B) for List2, C) Within the Nap-group, the association between the amount of Stage-2 NREM sleep and the extent of List1 context-memory retention, and similarly D) the corresponding association for List2 retention. Error bar represents s.e.m. *P = 0.028, n.s. = non-significant.
Figure 4 Context memory and sleep association. A) Context-memory performance in the No Nap- (clear bar) and Nap-group (filled bar) for List1, and B) for List2, C) Within the Nap-group, the association between the amount of Stage-2 NREM sleep and the extent of List1 context-memory retention, and similarly D) the corresponding association for List2 retention. Error bar represents s.e.m. *P = 0.028, n.s. = non-significant.CC BY · PubMed Central
Figure 5 The association in the Nap-group between context-memory retention for List2 and fast sleep spindles across the four electrode derivations (left top corner box label), with corresponding r- and P-values provided.
Figure 5 The association in the Nap-group between context-memory retention for List2 and fast sleep spindles across the four electrode derivations (left top corner box label), with corresponding r- and P-values provided.CC BY · PubMed Central

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Cites

Show all 83 references

Research works printed but not linked: 3

  1. [6]Walker MP Stickgold R 2010 Overnight alchemy: sleep-dependent memory evolution. Nat Rev Neurosci 11 218; author reply 218 20168316 PMC2891532
  2. [64]Nishida M Walker M 2007 Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS ONE 2 e341 17406665 PMC1828623
  3. [72]Clemens Z Fabo D Halasz P 2006 Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles. Neurosci Lett 403 52 56 16714084

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Metadata

Authors
van der Helm, E., Gujar, N., Nishida, M., & Walker, M. P.
Affiliations
  • University of California, Berkeley (US)
  • Tokyo Medical and Dental University (JP)
Corresponding author
Walker, Matthew P.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2011-11-17
Volume
6
Issue
11
Pages
e27421
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0027421
PMC
PMC3219667
OpenAlex
W2150174546
Cited by
138
References
83
Citations by year
2025: 5 · 2024: 7 · 2023: 5 · 2022: 8 · 2021: 12 · 2020: 9 · 2019: 11 · 2018: 8 · 2017: 12 · 2016: 7 · 2015: 11 · 2014: 15 · 2013: 18 · 2012: 8
FWCI
6.65
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • Figshare (submittedVersion, cc-by)
Funders
  • National Institutes of Health
  • National Institute on Aging (R01AG031164)
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
sleep-dependent memory consolidation, episodic memory, contextual memory, item memory, hippocampus, NREM sleep, sleep spindles, frontal lobe, recognition memory, declarative memory
MeSH terms
Adolescent, Adult, Female, Hippocampus, Humans, Learning, Male, Sleep, Wakefulness, Young Adult, Memory, Episodic

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