Memory for Semantically Related and Unrelated Declarative Information: The Benefit of Sleep, the Cost of Wake
Open accessAbstract
Numerous studies have examined sleep's influence on a range of hippocampus-dependent declarative memory tasks, from text learning to spatial navigation. In this study, we examined the impact of sleep, wake, and time-of-day influences on the processing of declarative information with strong semantic links (semantically related word pairs) and information requiring the formation of novel associations (unrelated word pairs). Participants encoded a set of related or unrelated word pairs at either 9 am or 9 pm, and were then tested after an interval of 30 min, 12 hr, or 24 hr. The time of day at which subjects were trained had no effect on training performance or initial memory of either word pair type. At 12 hr retest, memory overall was superior following a night of sleep compared to a day of wakefulness. However, this performance difference was a result of a pronounced deterioration in memory for unrelated word pairs across wake; there was no sleep-wake difference for related word pairs. At 24 hr retest, with all subjects having received both a full night of sleep and a full day of wakefulness, we found that memory was superior when sleep occurred shortly after learning rather than following a full day of wakefulness. Lastly, we present evidence that the rate of deterioration across wakefulness was significantly diminished when a night of sleep preceded the wake period compared to when no sleep preceded wake, suggesting that sleep served to stabilize the memories against the deleterious effects of subsequent wakefulness. Overall, our results demonstrate that 1) the impact of 12 hr of waking interference on memory retention is strongly determined by word-pair type, 2) sleep is most beneficial to memory 24 hr later if it occurs shortly after learning, and 3) sleep does in fact stabilize declarative memories, diminishing the negative impact of subsequent wakefulness.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Recall of word pairs after 24 h was better when sleep occurred immediately after learning than after a day of wakefulness.
“Furthermore, recall of word pairs after 24 h was better when sleep occurred immediately after learning than after a day of wakefulness (899).”
From About Sleep's Role in Memory (2013) · cites this paper as [899]
A time dependency of the effects of sleep on memory formation is indicated by studies showing stronger effects for sleep occurring shortly after learning than for sleep at a later time.
“A time dependency of the effects of sleep on memory formation is indicated by studies showing stronger effects for sleep occurring shortly after learning than for sleep at a later time (80,343,431,899,1172).”
From About Sleep's Role in Memory (2013) · cites this paper as [899]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Effects of early and late nocturnal sleep on declarative and procedural memory
Plihal, W., & Born, J. (1997) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1997.9.4.534 · Cited by 1,026 · see citing works
The contribution of sleep to hippocampus-dependent memory consolidation
Marshall, L., & Born, J. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.09.001 · Cited by 667 · see citing works
Wagner, U., Gais, S., & Born, J. (2001) · Learning & Memory · doi:10.1101/lm.36801 · Cited by 605 · cited 1× · see citing works
“Similar patterns of selective consolidation following sleep have been observed in several other domains of declarative memory, including emotional memory [19,20,21,22], semantic memory [23], and direct encoding [24,25,26].”
BackgroundSleep after learning aids memory recall
Gais, S., Lucas, B., & Born, J. (2006) · Learning & Memory · doi:10.1101/lm.132106 · Cited by 457 · see citing works
Sleep preferentially enhances memory for emotional components of scenes
Payne, J. D., Stickgold, R., Swanberg, K., & Kensinger, E. A. (2008) · Psychological Science · doi:10.1111/j.1467-9280.2008.02157.x · Cited by 440 · cited 1× · see citing works
“Similar patterns of selective consolidation following sleep have been observed in several other domains of declarative memory, including emotional memory [19,20,21,22], semantic memory [23], and direct encoding [24,25,26].”
BackgroundSelf-citationBackhaus, J., Hoeckesfeld, R., Born, J., Hohagen, F., & Junghanns, K. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.08.010 · Cited by 168 · see citing works
The Role of Sleep in Directed Forgetting and Remembering of Human Memories
Saletin, J. M., Goldstein, A. N., & Walker, M. P. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr034 · Cited by 151 · see citing works
Self-citationRauchs, G., Feyers, D., Landeau, B., Bastin, C., Luxen, A., Maquet, P., & Collette, F. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3972-10.2011 · Cited by 121 · see citing works
Sleep’s role in the processing of unwanted memories: Sleep and processing of unwanted memories
FISCHER, S., DIEKELMANN, S., & BORN, J. (2011) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2010.00881.x · Cited by 50 · see citing works
Flagged first, then by citations
Research works printed but not linked: 21
- [2]Jenkins JG Dallenbach KM 1924 Oblivescence during sleep and waking. American Journal of Psychology 35 605 612
- [5]Wixted JT 2004 The psychology and neuroscience of forgetting. Annu Rev Psychol 55 235 269 14744216
- [6]Mednick SC Cai DJ Shuman T Anagnostaras S Wixted JT 2011 An opportunistic theory of cellular and systems consolidation. Trends Neurosci 34 504 514 21742389 PMC3183157
- [7]Benson K Feinberg I 1975 Sleep and memory: retention 8 and 24 hours after initial learning. Psychophysiology 12 192 195 1135353
- [8]Benson K Feinberg I 1977 The beneficaial effect of sleep in an extended Jenkins and Dallenbach paradigm. Psychophysiology 14 375 384 882617
- [10]Talamini LM Nieuwenhuis IL Takashima A Jensen O 2008 Sleep directly following learning benefits consolidation of spatial associative memory. Learn Mem 15 233 237 18391183
- [11]Van Der Werf YD Van Der Helm E Schoonheim MM Ridderikhoff A Van Someren EJ 2009 Learning by observation requires an early sleep window. Proc Natl Acad Sci U S A 106 18926 18930 19884499 PMC2776450
- [13]Smith CT 2001 Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med Rev 5 491 506 12531156
- [14]Stickgold R 2004 Dissecting sleep-dependent learning and memory consolidation. Comment on Schabus M et al. Sleep spindles and their significance for declarative memory consolidation. Sleep 2004;27(8):1479–85. Sleep 27 1443 1445 15683132
- [16]Tucker MA Hirota Y Wamsley EJ Lau H Chaklader A 2006 A daytime nap containing solely non-REM sleep enhances declarative but not procedural memory. Neurobiol Learn Mem 86 241 247 16647282
- [17]Hoddes E Zarcone V Smythe H Phillips R Dement WC 1973 Quantification of sleepiness: a new approach. Psychophysiology 10 431 436 4719486
- [18]Gais S Born J 2004 Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc Natl Acad Sci U S A 101 2140 2144 14766981 PMC357065
- [19]Hu P Stylos-Allan M Walker MP 2006 Sleep facilitates consolidation of emotional declarative memory. Psychol Sci 17 891 898 17100790
- [22]Payne JD Kensinger EA 2010 Sleep leads to changes in the emotional memory trace: evidence from FMRI. J Cogn Neurosci 23 1285 1297 20521852
- [23]Payne JD Schacter DL Propper RE Huang LW Wamsley EJ 2009 The role of sleep in false memory formation. Neurobiol Learn Mem 92 327 334 19348959 PMC2789473
- [27]Schmidt C Peigneux P Muto V Schenkel M Knoblauch V 2006 Encoding difficulty promotes postlearning changes in sleep spindle activity during napping. J Neurosci 26 8976 8982 16943553 PMC6675334
- [29]Gais S Molle M Helms K Born J 2002 Learning-dependent increases in sleep spindle density. J Neurosci 22 6830 6834 12151563 PMC6758170
- [30]Schabus M Gruber G Parapatics S Sauter C Klosch G 2004 Sleep spindles and their significance for declarative memory consolidation. Sleep 27 1479 1485 15683137
- [31]Diekelmann S Born J 2010 The memory function of sleep. Nat Rev Neurosci 11 114 126 20046194
- [32]Ellenbogen JM Payne JD Stickgold R 2006 The role of sleep in declarative memory consolidation: passive, permissive, active or none? Curr Opin Neurobiol 16 716 722 17085038
- [33]Walker MP 2010 Sleep, memory and emotion. Prog Brain Res 185 49 68 21075233
Cited by
Sorted by citations
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
Sleep promotes lasting changes in selective memory for emotional scenes
Payne, J. D., Chambers, A. M., & Kensinger, E. A. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2012.00108 · Cited by 183 · see citing works
Self-citationNapping and the selective consolidation of negative aspects of scenes
Payne, J. D., Kensinger, E. A., Wamsley, E. J., Spreng, R. N., Alger, S. E., Gibler, K., Schacter, D. L., & Stickgold, R. (2015) · Emotion · doi:10.1037/a0038683 · Cited by 130 · see citing works
Self-citationDreaming and offline memory consolidation
Wamsley, E. J. (2014) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-013-0433-5 · Cited by 111 · see citing works
Self-citationCairney, S. A., Lindsay, S., Sobczak, J. M., Paller, K. A., & Gaskell, M. G. (2016) · SLEEP · doi:10.5665/sleep.5772 · Cited by 93 · see citing works
Evidence for two distinct sleep-related long-term memory consolidation processes
Schönauer, M., Grätsch, M., & Gais, S. (2015) · Cortex · doi:10.1016/j.cortex.2014.08.005 · Cited by 73 · see citing works
The impact of sleep on true and false memory across long delays
Pardilla-Delgado, E., & Payne, J. D. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.11.016 · Cited by 48 · see citing works
Self-citationLong-term memory. sleep, and the spacing effect
Bell, M. C., Kawadri, N., Simone, P. M., & Wiseheart, M. (2014) · Memory · doi:10.1080/09658211.2013.778294 · Cited by 47 · see citing works
A meta-analysis of the relation between dream content and memory consolidation
Hudachek, L., & Wamsley, E. J. (2023) · SLEEP · doi:10.1093/sleep/zsad111 · Cited by 46 · see citing works
Self-citationSlow wave sleep in naps supports episodic memories in early childhood
Lokhandwala, S., & Spencer, R. M. C. (2021) · Developmental Science · doi:10.1111/desc.13035 · Cited by 41 · see citing works
Sleep deprivation induces fragmented memory loss.
Ashton, J. E., Harrington, M. O., Langthorne, D., Ngo, H.-V. V., & Cairney, S. A. (2020) · Learning & Memory · doi:10.1101/lm.050757.119 · Cited by 36 · see citing works
The role of sleep for episodic memory consolidation: stabilizing or rescuing?
Zhang, J., Whitehurst, L. N., & Mednick, S. C. (2022) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2022.107621 · Cited by 34 · see citing works
Retrieval and sleep both counteract the forgetting of spatial information.
Antony, J. W., & Paller, K. A. (2018) · Learning & Memory · doi:10.1101/lm.046268.117 · Cited by 25 · see citing works
Sleep bolsters schematically incongruent memories
Ashton, J. E., Staresina, B. P., & Cairney, S. A. (2022) · PLoS ONE · doi:10.1371/journal.pone.0269439 · Cited by 18 · see citing works
Mak, M. H. C., Ball, L. V., O'Hagan, A., Walsh, C. R., & Gaskell, M. G. (2025) · Cognition · doi:10.1016/j.cognition.2025.106086 · Cited by 9 · see citing works
- Authors
- Payne, J. D., Tucker, M. A., Ellenbogen, J. M., Wamsley, E. J., Walker, M. P., Schacter, D. L., & Stickgold, R.
- Affiliations
- University of Notre Dame (US)
- Harvard University (US)
- University of California, Berkeley (US)
- Corresponding author
- Payne, Jessica D.
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-03-22
- Volume
- 7
- Issue
- 3
- Pages
- e33079
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3310860
- OpenAlex
- W2167219655
- Cited by
- 181
- References
- 9
- Citations by year
- 2026: 4 · 2025: 13 · 2024: 15 · 2023: 24 · 2022: 8 · 2021: 10 · 2020: 32 · 2019: 14 · 2018: 8 · 2017: 12 · 2016: 10 · 2015: 8 · 2014: 11 · 2013: 9 · 2012: 2
- FWCI
- 4.92
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Institutes of Health (MH48,832)
- National Institute of Mental Health (R01-MH 48832, R01MH048832)
- 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, declarative memory, semantic relatedness, word pair learning, memory retention, wakefulness, time of day, memory stabilization, hippocampus, memory impairment
- MeSH terms
- Adult, Female, Humans, Language, Male, Memory, Sleep
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review