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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.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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InfluentialSelf-citationInsomnia as predictor versus outcome of PTSD and depression among Iraq combat veterans
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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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Sleep spindles preferentially consolidate weakly encoded memories
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“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.
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“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
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How do I remember? Let me count the ways
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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 93
“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 104
“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 91
“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 92
“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
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
Benedict, C., Scheller, J., Rose‐John, S., Jan Born, A., & Marshall, L. (2009) · The FASEB Journal · doi:10.1096/fj.08-122853 · Cited by 88
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
“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
“…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
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 87
Feld, G. B., & Jan Born, A. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0490-9 · Cited by 84
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
Offline memory consolidation during waking rest
Wamsley, E. J. (2022) · Nature Reviews Psychology · doi:10.1038/s44159-022-00072-w · Cited by 84
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
“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 88
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
Nocturnal Mnemonics: Sleep and Hippocampal Memory Processing
Saletin, J., & Walker, M. P. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00059 · Cited by 84
“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
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
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 87
“…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
Giraudier, M., Ventura‐Bort, C., & Weymar, M. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.01276 · Cited by 78
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 80
“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 89
“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
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
“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
“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 72
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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