Sleep preferentially enhances memory for emotional components of scenes
Open accessAbstract
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.
“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]
The Discussion (page unavailable) proposes an active role for sleep in consolidating emotional memories and reports better memory for negative objects after sleep than after wakefulness. It does not report whether sleep reduces the emotional response associated with those memories, so it does not support the affective-depotentiation part of the claim. (LLM, conf=0.84)
Experimental — accuracy not yet measuredSleep enhances memory consolidation, particularly for emotional relative to neutral materials.
“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
Sleep has been shown to modulate the processing of emotional memory.
“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]
Some studies demonstrated that sleep preferentially consolidates emotional over neutral memories.
“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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“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) Recent functional magnetic resonance imaging studies show that participants who slept after encoding emotionally aversive pictures showed reduced amygdala activi…”
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“2011), or retention of previously encoded emotional pictures or texts (Wagner et al. 2001; Payne et al. 2008; Nishida et al. 2009).”
BackgroundSakaki, M., Niki, K., & Mather, M. (2011) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-011-0062-x · Cited by 124 · see citing works
Dreaming 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
Sleep Supports Selective Retention of Associative Memories Based on Relevance for Future Utilization
van Dongen, E. V., Thielen, J.-W., Takashima, A., Barth, M., & Fernández, G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043426 · Cited by 110 · see citing works
“be selectively facilitated by sleep [11].”
BackgroundThe Nature and Functions of Dreaming
Hartmann, E. L. (2010) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199751778.001.0001 · Cited by 109 · see citing works
Virginie Sterpenich, A., Schmidt, C., Albouy, G., Matarazzo, L., Vanhaudenhuyse, A., Boveroux, P., Degueldre, C., Leclercq, Y., Balteau, E., Collette, F., et al. (2014) · SLEEP · doi:10.5665/sleep.3762 · Cited by 110 · see citing works
Napping promotes inter-session habituation to emotional stimuli
Pace-Schott, E. F., Shepherd, E., Spencer, R. M. C., Marcello, M., Tucker, M., Propper, R. E., & Stickgold, R. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.10.006 · Cited by 109 · see citing works
“For example, sleep enhances a trade-off in visual memory insofar as memory for emotional (but not neutral) objects is preferentially remembered (Payne et al., 2008) and sleep promotes generalization of extinction of conditioned fear (PaceSchott et al., 2009).”
BackgroundSelf-citationNewbury, C. R., Crowley, R., Rastle, K., & Tamminen, J. (2021) · Psychological Bulletin · doi:10.1037/bul0000348 · Cited by 113 · see citing works
“…appear to suggest that sleep benefits recognitionmemory for emotional stimuli but not for neutral stimuli (Alger et al., 2018; Hu et al., 2006; Payne et al., 2008, 2015; see Kim & Payne, 2020 for a review) suggesting that sleep’s impact on recognition memory may be modulated by emotionality.”
BackgroundRemembering to Execute a Goal: Sleep on It!
Scullin, M. K., & McDaniel, M. A. (2010) · Psychological Science · doi:10.1177/0956797610373373 · Cited by 106 · see citing works
Replay in Deep Learning: Current Approaches and Missing Biological Elements
Hayes, T. L., Krishnan, G. P., Bazhenov, M., Siegelmann, H. T., Sejnowski, T. J., & Kanan, C. (2021) · Neural Computation · doi:10.1162/neco_a_01433 · Cited by 106 · see citing works
“Consolidation of the hippocampus independent short-term memory, such as emotional and procedural memory, is also enhanced by sleep (McGaugh, 2000; Hu, Stylos-Allan, & Walker, 2006; Payne, Stickgold, Swan-berg, & Kensinger, 2008; Wagner et al., 2001).”
Lehmann, M., Schreiner, T., Seifritz, E., & Rasch, B. (2016) · Scientific Reports · doi:10.1038/srep39229 · Cited by 99 · see citing works
Evidence for the preferential incorporation of emotional waking-life experiences into dreams.
Malinowski, J., & Horton, C. L. (2014) · Dreaming · doi:10.1037/a0036017 · Cited by 101 · see citing works
“Additionally, it has been shown that sleep ‘unbinds’ the emotional elements of memories for selective consolidation (Payne et al., 2008), again demonstrating how emotions seem to guide the process of determining which memories are chosen for encoding during sleep.”
Post-learning hippocampal replay selectively reinforces spatial memory for highly rewarded locations
Michon, F., Sun, J.-J., Kim, C. Y., Ciliberti, D., & Kloosterman, F. (2019) · Current Biology · doi:10.1016/j.cub.2019.03.048 · Cited by 86 · see citing works
“Experiences that are salient or relevant to an organism are generally better remembered over time [1, 2].”
BackgroundSleep and emotional memory processing
van der Helm, E., & Walker, M. P. (2011) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2010.12.010 · Cited by 102 · see citing works
Retroactive and graded prioritization of memory by reward
Braun, E. K., Wimmer, G. E., & Shohamy, D. (2018) · Nature Communications · doi:10.1038/s41467-018-07280-0 · Cited by 101 · see citing works
Spontaneous repetitive thoughts can be adaptive: Postscript on “mind wandering”.
Baars, B. J. (2010) · Psychological Bulletin · doi:10.1037/a0018726 · Cited by 99 · see citing works
Asymmetric effects of emotion on mnemonic interference
Leal, S. L., Tighe, S. K., & Yassa, M. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.02.013 · Cited by 93 · see citing works
Poor Sleep Quality Predicts Deficient Emotion Information Processing over Time in Early Adolescence
Soffer‐Dudek, N., Sadeh, A., Dahl, R. E., & Rosenblat-Stein, S. (2011) · SLEEP · doi:10.5665/sleep.1386 · Cited by 96 · see citing works
Memory for details with self-referencing
Serbun, S. J., Shih, J. Y., & Gutchess, A. H. (2011) · Memory · doi:10.1080/09658211.2011.626429 · Cited by 94 · see citing works
“To examine general memory we used the equation from Payne et al. (2008), which accounts for the fact that ‘‘similar’’ and ‘‘same’’ responses are mutually exclusive.”
Cunningham, T. J., Crowell, C. R., Alger, S. E., Kensinger, E. A., Villano, M. A., Mattingly, S. M., & Payne, J. D. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.06.002 · Cited by 94 · see citing works
“…stages were scored according to the criteria described by Rechtschaffen and Kales (1968) and discussion of stages use their nomenclature (i.e. REM sleep, SWS) in order to be consistent with most studies of sleep and memory consolidation (e.g. Payne et al., 2008, 2012; Diekelmann & Born, 2010).”
BackgroundMethodResultInfluentialSelf-citationContribution of norepinephrine to emotional memory consolidation during sleep
Groch, S., Wilhelm, I., Diekelmann, S., Sayk, F., Gais, S., & Born, J. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.03.006 · Cited by 93 · see citing works
“Nevertheless, considering previous work that demonstrated a particular importance of REM sleep for the consolidation of emotional aspects in a memory (Wagner et al., 2001, 2002; Payne et al., 2008; Nishida et al., 2009) it cannot be excluded that clonidine affected memory consolidation by modulating REM sleep.”
BackgroundPreferential Consolidation of Emotional Memory During Sleep: A Meta-Analysis
Lipinska, G., Stuart, B. L., Thomas, K. G. F., Baldwin, D. S., & Bolinger, E. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.01014 · Cited by 93 · see citing works
“A number of seminal studies (e.g., Wagner et al., 2001; Hu et al., 2006; Payne et al., 2008) suggest that emotional memory is enhanced by sleep.”
BackgroundInfluentialEffects of emotional valence and arousal upon memory trade-offs with aging.
Waring, J., & Kensinger, E. (2009) · Psychology and Aging · doi:10.1037/a0015526 · Cited by 100 · see citing works
“For example, the difference score for positive high-arousal items would be equivalent to the recognition rate for positive high-arousal items minus the recognition rate for neutral items (see Leclerc & Kensinger, 2008, and Payne et al., 2008, for use of these types of difference scores).”
BackgroundInfluentialSelf-citationOlfactory Aversive Conditioning during Sleep Reduces Cigarette-Smoking Behavior
Arzi, A., Holtzman, Y., Samnon, P., Eshel, N., Harel, E., & Sobel, N. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2291-14.2014 · Cited by 88 · see citing works
How do I remember? Let me count the ways
Stickgold, R. (2009) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2009.05.004 · Cited by 90 · see citing works
Self-citationDoes abnormal sleep impair memory consolidation in schizophrenia?
Manoach, D. S. (2009) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.021.2009 · Cited by 91 · see citing works
“Sleep and memory in schizophrenia either neutral or aversive objects placed on neutral backgrounds, subsequent recognition of the aversive objects, relative to their backgrounds, was enhanced after sleep compared to wake (Payne et al., 2008).”
Malinowski, J., & Horton, C. L. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01132 · Cited by 93 · see citing works
“Sleep also ‘unbinds’ waking-life stimuli, selectively consolidating emotional rather than neutral aspects of it, both over the course of a night and during a nap (Payne et al., 2008, 2015).”
BackgroundClosed-Loop Acoustic Stimulation Enhances Sleep Oscillations But Not Memory Performance
Henin, S. E., Borges, H., Shankar, A., Sarac, C., Melloni, L., Friedman, D. J., Flinker, A., Parra, L. C., Buzsáki, G., Devinsky, O., et al. (2019) · eNeuro · doi:10.1523/eneuro.0306-19.2019 · Cited by 88 · see citing works
“Emotional memories may be more strongly remembered after sleep compared with neutral memories (Wagner et al., 2006; Payne et al., 2008; Nishida et al., 2009; Javadi et al., 2011; Payne and Kensinger, 2011; Baran et al., 2012), although other studies did not find these effects (Sterpenich et al.,…”
Sleep and Cortisol Interact to Support Memory Consolidation
Bennion, K. A., Steinmetz, K. R. M., Kensinger, E. A., & Payne, J. D. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht255 · Cited by 88 · see citing works
“This finding suggests that sleep unbinds scenes, consolidating only the most emotionally salient aspect of the experience (Payne et al. 2008; Payne and Kensinger 2010).”
BackgroundSelf-citationSchäfer, S. K., Wirth, B. E., Staginnus, M., Becker, N., Michael, T., & Sopp, M. R. (2020) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2020.101280 · Cited by 85 · see citing works
Quality of sleep among university students: effects of nighttime computer and television use
Duarte, G. G. D. M., & Reimão, R. (2010) · Arquivos de Neuro-Psiquiatria · doi:10.1590/s0004-282x2010000500009 · Cited by 83 · see citing works
Benedict, C., Scheller, J., Rose‐John, S., Jan Born, A., & Marshall, L. (2009) · The FASEB Journal · doi:10.1096/fj.08-122853 · Cited by 84 · see citing works
Spontaneous thought as an unconstrained memory process
Mildner, J. N., & Tamir, D. I. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.09.001 · Cited by 83 · see citing works
“Memory replay during waking and sleep often features content that is emotional [140], rewarded [141], or that is known to be important for the future [142,143].”
BackgroundAge-related differences in sleep-based memory consolidation: a meta-analysis
Gui, W.-J., Li, H.-J., Guo, Y.-H., Peng, P., Lei, X., & Yu, J. (2017) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2017.02.001 · Cited by 78 · see citing works
“…other tasks, such as object/face locations, personal event memories, and emotional scenes (Aly and Moscovitch, 2010; Cherdieu et al., 2014; Jones et al., 2016; Payne et al., 2008; Rasch et al., 2007; Scullin and Bliwise, 2015; Scullin and McDaniel, 2010; Talamini et al., 2008; Wagner et al., 2001).”
Deak, M. C., & Stickgold, R. (2010) · WIREs Cognitive Science · doi:10.1002/wcs.52 · Cited by 81 · see citing works
Self-citationConsolidative mechanisms of emotional processing in REM sleep and PTSD
Murkar, A., & Koninck, J. D. (2018) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2018.03.001 · Cited by 82 · see citing works
Feld, G. B., & Jan Born, A. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0490-9 · Cited by 79 · see citing works
Groch, S., Zinke, K., Wilhelm, I., & Born, J. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.08.013 · Cited by 76 · see citing works
Offline memory consolidation during waking rest
Wamsley, E. J. (2022) · Nature Reviews Psychology · doi:10.1038/s44159-022-00072-w · Cited by 76 · see citing works
The impact of overnight consolidation upon memory for emotional and neutral encoding contexts
Lewis, P. A., Cairney, S., Manning, L., & Critchley, H. D. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.05.009 · Cited by 79 · see citing works
“To quantify the impact an off-line delay upon memory performance, we created a measure of forgetting which was calculated for each participant as forgetting = immediate performance − delayed performance (Payne et al., 2008).”
BackgroundMethodCorbin, J. C., Reyna, V. F., Weldon, R. B., & Brainerd, C. J. (2015) · Journal of Applied Research in Memory and Cognition · doi:10.1016/j.jarmac.2015.09.001 · Cited by 81 · see citing works
Assessing the dream-lag effect for rem and nrem stage 2 dreams
Blagrove, M., Fouquet, N. C., Henley-Einion, J. A., Pace-Schott, E. F., Davies, A. C., Neuschaffer, J. L., & Turnbull, O. H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026708 · Cited by 75 · see citing works
Nocturnal Mnemonics: Sleep and Hippocampal Memory Processing
Saletin, J., & Walker, M. P. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00059 · Cited by 76 · see citing works
“emotionality (Hu et al., 2006; Wagner et al., 2006, 2007; Payne et al., 2008; Nishida et al., 2009; Walker and van der Helm, 2009; Payne and Kensinger, 2011), reward potential (Fischer and Born, 2009; Wilhelm et al.”
BackgroundPsychological Effect of an Analogue Traumatic Event Reduced by Sleep Deprivation
Porcheret, K., Holmes, E. A., Goodwin, G. M., Foster, R. G., & Wulff, K. (2015) · Sleep · doi:10.5665/sleep.4802 · Cited by 74 · see citing works
The sleep benefit in episodic memory: An integrative review and a meta-analysis.
Berres, S., & Erdfelder, E. (2021) · Psychological Bulletin · doi:10.1037/bul0000350 · Cited by 74 · see citing works
Sleep smart—optimizing sleep for declarative learning and memory
Feld, G. B., & Diekelmann, S. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.00622 · Cited by 74 · see citing works
“…to renormalize synapses (Hill and Tononi, 2005; Esser et al., 2007; Sullivan and de Sa, 2008), and potentiating synapses by extended learning (Huber et al., 2004a; Schmidt et al., 2006) or by transcranial magnetic stimulation (Huber et al., 2007, 2008) induces local increases of slow wave activity.”
BackgroundSopp, M. R., Michael, T., Weeß, H.-G., & Mecklinger, A. (2017) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-017-0542-8 · Cited by 68 · see citing works
Giraudier, M., Ventura‐Bort, C., & Weymar, M. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.01276 · Cited by 71 · see citing works
Sleeping Worries Away or Worrying Away Sleep? Physiological Evidence on Sleep-Emotion Interactions
Talamini, L. M., Bringmann, L. F., de Boer, M., & Hofman, W. F. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062480 · Cited by 74 · see citing works
“Moreover, sleep has been shown to benefit memory performance [25,26,27], and more specifically emotional memory performance [28,29,30,31], in several ways.”
BackgroundMemory sources of dreams: the incorporation of autobiographical rather than episodic experiences
Malinowski, J., & Horton, C. L. (2014) · Journal of Sleep Research · doi:10.1111/jsr.12134 · Cited by 73 · see citing works
“Payne et al. (2008) have demonstrated that emotional waking-life memories are consolidated selectively over neutral ones, and two studies have demonstrated that emotional waking-life experiences are incorporated preferentially into dreams (Malinowski and Horton, in review; Schredl, 2006).”
BackgroundOvernight Sleep Enhances Hippocampus-Dependent Aspects of Spatial Memory.
Nguyen, N. D., Tucker, M. A., Stickgold, R., & Wamsley, E. J. (2013) · SLEEP · doi:10.5665/sleep.2808 · Cited by 72 · see citing works
Self-citationBäuml, K.-H. T., Holterman, C., & Abel, M. (2014) · Journal of Experimental Psychology: Learning, Memory, and Cognition · doi:10.1037/xlm0000025 · Cited by 71 · see citing works
“For instance, emotional memories have been found to show more sleep benefits than neutral memories do (Payne et al., 2008), and memories considered relevant for the future show more sleep benefits than supposedly irrelevant material does (Wilhelm et al., 2011).”
BackgroundMethodHorton, C. L., & Malinowski, J. E. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.00874 · Cited by 68 · see citing works
“Indeed it has been suggested that bizarreness arises out of the joining together of disparate elements (often from waking life; e.g., Revonsuo and Tarkko, 2002; Levin and Nielsen, 2007), which is also indicative of hyperassociativity.”
BackgroundInfluentialThe nonspecific thalamus: A place in a wedding bed for making memories last?
de Vasconcelos, A. P., & Cassel, J. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.021 · Cited by 68 · see citing works
- 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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