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Sleep Preferentially Enhances Memory for Emotional Components of Scenes
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Central aspects of emotional experiences are often well remembered at the expense of background details. Previous studies of such memory trade-offs have focused on memory after brief delays, but little is known about how these components of emotional memories change over time. We investigated the evolution of memory for negative scenes across 30 min, 12 daytime hours spent awake, and 12 nighttime hours including sleep. After 30 min, negative objects were well remembered at the expense of information about their backgrounds. Time spent awake led to forgetting of the entire negative scene, with memories of objects and their backgrounds decaying at similar rates. Sleep, in contrast, led to a preservation of memories of negative objects, but not their backgrounds, a result suggesting that the two components undergo differential processing during sleep. Memory for a negative scene develops differentially across time delays containing sleep and wake, with sleep selectively consolidating those aspects of memory that are of greatest value to the organism.
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“Our results are in line with studies and theoretical accounts proposing a role of sleep in the affective depotentiation of emotional memories.9,14,13,18,37”
From Effects of Sleep after Experimental Trauma on Intrusive Emotional Memories. (2016) · cites this paper as [14]
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“Sleep is thought to enhance memory consolidation, particularly for emotional relative to neutral materials (Nishida, Pearsall, Buckner, & Walker, 2009; Payne, Chambers, & Kensinger, 2012; Payne, Stickgold, Swanberg, & Kensinger, 2008; Wagner, Gais, & Born, 2001).”
From Intrusive memories of trauma: A target for research bridging cognitive science and its clinical application (2019) · cites this paper as Payne, Stickgold, Swanberg, & Kensinger, 2008
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“Sleep has been shown to modulate the processing of emotional memory.[66][67][68]”
From Cognitive Performance, Sleepiness, and Mood in Partially Sleep Deprived Adolescents: The Need for Sleep Study (2016) · cites this paper as [67]
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“Some studies indeed demonstrated that sleep preferentially consolidates emotional over neutral memories (574,602,861,896,898,1276); however, others failed to reveal such effects (60,168,732,1147,1148).”
From About Sleep's Role in Memory (2013) · cites this paper as [898]
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Self-citationEmotional bias of sleep-dependent processing shifts from negative to positive with aging
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“Several studies found that memory enhancements for negative relative to neutral materials are exaggerated after longer delays (≥24 h) compared to shorter delays (≤30 min), suggesting a role for timedependent consolidation processes (Sharot and Yonelinas 2008), including those that occur during sleep (Payne et al. 2008…”
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BackgroundSelf-citationSleep reduces the testing effect—But not after corrective feedback and prolonged retention interval.
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“…in contrast, in the 12-h sleep condition, participants studied and practiced the paired associates at 9 p.m., and took the final test at 9 a.m., after one night of nocturnal sleep (for similar designs, see Abel & Bäuml, 2013; Bäuml et al., 2014; Payne et al., 2008; Scullin & McDaniel, 2010).”
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“For instance, sleeprelated benefits have been found to depend on the future relevance of memories (e.g., Wilhelm et al., 2011), or their emotional tone (e.g., Payne et al., 2008).”
Sleep unbinds memories from their emotional context
Deliens, G., Gilson, M., Schmitz, R., & Peigneux, P. (2012) · Cortex · doi:10.1016/j.cortex.2012.11.014 · Cited by 33
“Finally, Payne et al. (2008) investigated whether sleep enhances memory for the emotional experience as a whole, or acts separately on different emotional memory constituents by enhancing only the affective component.”
REM theta activity predicts re-experiencing symptoms after exposure to a traumatic film
Sopp, M. R., Brueckner, A. H., Schäfer, S. K., Lass‐Hennemann, J., & Michael, T. (2018) · Sleep Medicine · doi:10.1016/j.sleep.2018.10.030 · Cited by 35
McBean, A. L., & Schlosnagle, L. (2015) · Journal of Sleep Research · doi:10.1111/jsr.12329 · Cited by 32
“A link between retrospective memory, or remembering events in the past, and sleep has been established previously among healthy adult populations (Payne et al., 2008; Rasch et al., 2007).”
BackgroundHarrington, M. O., Nedberge, K. M. W., & Durrant, S. J. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.04.013 · Cited by 31
Sleep's benefits to emotional processing emerge in the long term
Bolinger, E., Cunningham, T. J., Payne, J. D., Bowman, M. A., Bulca, E., Jan Born, A., & Zinke, K. (2019) · Cortex · doi:10.1016/j.cortex.2019.07.008 · Cited by 33
Self-citationCunningham, T. J., Chambers, A. M., & Payne, J. D. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.00862 · Cited by 33
“…preserves memory for emotional vs. neutral information compared to an equivalent period of wakefulness, benefitting memory for negative narratives, negative images, and humorous cartoons (Wagner et al., 2001; Hu et al., 2006; Payne et al., 2008; Nishida et al., 2009; Chambers and Payne, 2014a).”
BackgroundMethodResultInfluentialSelf-citationHow Emotional Arousal Enhances Episodic Memory
Baraly, K. T. A., Hot, P., Davidson, P. S. R., & Talmi, D. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21051-1 · Cited by 32
“It is interesting to note that sleep plays a similar role as emotional arousal on memory: it selectively preserves emotional gist information and deteriorates non-emotional peripheral details (Payne et al., 2008; see Section 4.1).”
BackgroundInfluentialLipinska, G., & Thomas, K. G. F. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.01766 · Cited by 34
Test Expectation Enhances Memory Consolidation across Both Sleep and Wake.
Wamsley, E. J., Hamilton, K., Graveline, Y., Manceor, S., & Parr, E. (2016) · PLoS ONE · doi:10.1371/journal.pone.0165141 · Cited by 29
Comparing the Effects of Sleep and Rest on Memory Consolidation
Tucker, M. A., Humiston, G. B., Summer, T., & Wamsley, E. J. (2020) · Nature and Science of Sleep · doi:10.2147/nss.s223917 · Cited by 33
Intrusive memories: A mechanistic signature for emotional memory persistence
Herz, N., Bar‐Haim, Y., Holmes, E. A., & Censor, N. (2020) · Behaviour Research and Therapy · doi:10.1016/j.brat.2020.103752 · Cited by 33
To Sleep, to Strive, or Both: How Best to Optimize Memory
Tucker, M. A., Tang, S. X., Uzoh, A., Morgan, A., & Stickgold, R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021737 · Cited by 29
“This is interesting in light of other studies that have shown a preferential benefit of sleep for information with strong emotional valence [16,17], which is known to produce heightened activity in the amygdala during encoding [18], and which leads to strengthening of relevant network connectivity following sleep, for…”
Self-citationRetrieval 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
“is a standard way to assess the impact of sleep (Plihal and Born 1997, 1999; Payne et al. 2008).”
BackgroundNeurophysiological Basis of Sleep’s Function on Memory and Cognition
Spencer, R. M. C. (2013) · ISRN Physiology · doi:10.1155/2013/619319 · Cited by 30
“Sleep has been shown to consolidate and, in some cases, preferentially enhance memory for negative emotional images relative to neutral images [129-132].”
Sleep can reduce proactive interference
Abel, M., & Bäuml, K. T. (2013) · Memory · doi:10.1080/09658211.2013.785570 · Cited by 28
The expression of trace conditioning during non-REM sleep and its relation to subjective experience
Wamsley, E. J., & Antrobus, J. S. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.02.012 · Cited by 28
Heib, D. P. J., Hoedlmoser, K., Anderer, P., Gruber, G., Zeitlhofer, J., & Schabus, M. (2015) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00804 · Cited by 34
“Recent studies suggest that sleep is not beneficial for all memories but rather selects specific memories for consolidation (van Dongen et al., 2012; Rauchs et al., 2011; Saletin et al., 2011; Wilhelm et al., 2011; Fischer & Born, 2009; Payne et al., 2008).”
BackgroundA more generalized fear response after a daytime nap
Davidson, P., Carlsson, I., Jönsson, P., & Johansson, M. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.03.005 · Cited by 27
Kurz, E., Conzelmann, A., Barth, G. M., Hepp, L. L., Schenk, D. K., Renner, T. J., Jan Born, A., & Zinke, K. (2019) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13048 · Cited by 29
Offline consolidation of procedural skill learning is enhanced by negative emotional content
Javadi, A. H., Walsh, V., & Lewis, P. A. (2011) · Experimental Brain Research · doi:10.1007/s00221-010-2497-7 · Cited by 26
Gil-Lievana, E., Ramírez-Mejía, G., Urrego-Morales, O., Luis-Islas, J., Gutiérrez, R., & Bermúdez‐Rattoni, F. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.823220 · Cited by 28
Exploring the (lack of) facilitative effect of emoji for word processing
Kaye, L. K., Rocabado, F., Rodríguez‐Cuadrado, S., Jones, B. R., Malone, S. A., Wall, H. J., & Duñabeitia, J. A. (2022) · Computers in Human Behavior · doi:10.1016/j.chb.2022.107563 · Cited by 26
Sleep and dreaming in the light of reactive and predictive homeostasis
Simor, P., Peigneux, P., & Bódizs, R. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105104 · Cited by 34
Sleep and Affective Brain Regulation
van der Helm, E., & Walker, M. P. (2012) · Social and Personality Psychology Compass · doi:10.1111/j.1751-9004.2012.00464.x · Cited by 27
Prehn‐Kristensen, A., Molzow, I., Förster, A., Siebenhühner, N., Gesch, M., Wiesner, C. D., & Baving, L. (2017) · Biological Psychology · doi:10.1016/j.biopsycho.2016.12.017 · Cited by 31
Impact of sex steroids and reproductive stage on sleep-dependent memory consolidation in women
Baker, F. C., Sattari, N. S., de Zambotti, M., Goldstone, A., Alaynick, W. A., & Mednick, S. C. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.03.017 · Cited by 28
Schapiro, A. C., McDevitt, E. A., Rogers, T. T., Mednick, S. C., & Norman, K. A. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/173021 · Cited by 26
The Effect of Obstructive Sleep Apnea on Sleep-dependent Emotional Memory Consolidation
Cunningham, T. J., Kishore, D., Guo, M., Igue, M., Malhotra, A., Stickgold, R., & Djonlagic, I. E. (2022) · Annals of the American Thoracic Society · doi:10.1513/annalsats.202204-315oc · Cited by 24
Self-citationEmotional Memory Processing during REM Sleep with Implications for Post-Traumatic Stress Disorder
Rho, Y.-A., Sherfey, J. S., & Vijayan, S. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1020-22.2022 · Cited by 30
Noradrenergic mechanisms of arousal’s bidirectional effects on episodic memory
Clewett, D., Sakaki, M., Nielsen, S. E., Petzinger, G. M., & Mather, M. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.10.017 · Cited by 26
“Likewise, the mnemonic advantage of emotional over neutral stimuli also appears to increase over longer retention intervals (Sharot & Yonelinas, 2008), which may be driven by offline consolidation processes that occur during sleep (Payne et al., 2012; Payne et al., 2008).”
Metadata
- Authors
- Payne, J. D., Stickgold, R., Swanberg, K., & Kensinger, E. A.
- Affiliations
- Beth Israel Deaconess Medical Center (US)
- Harvard University (US)
- Boston College (US)
- Corresponding author
- Payne, Jessica D.
- Kensinger, Elizabeth A.
- Venue
- Psychological Science
- Publisher
- SAGE Publications
- Published
- 2008-08
- Volume
- 19
- Issue
- 8
- Pages
- 781-788
- ISSN
- 0956-7976 (ISSN-L)
- 1467-9280
- PMC
- PMC5846336
- OpenAlex
- W2163520994
- Cited by
- 440
- References
- 30
- Citations by year
- 2026: 11 · 2025: 21 · 2024: 22 · 2023: 25 · 2022: 21 · 2021: 22 · 2020: 23 · 2019: 28 · 2018: 32 · 2017: 30 · 2016: 21 · 2015: 33 · 2014: 30 · 2013: 24 · 2012: 26
- FWCI
- 12.10
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Psychological Science (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH048832)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- sleep-dependent memory consolidation, emotional memory, scene memory, memory decay, forgetting, time delay effects
- MeSH terms
- Arousal, Attention, Circadian Rhythm, Emotions, Humans, Pattern Recognition, Visual, Retention, Psychology, Sleep, Wakefulness
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