Sleep promotes lasting changes in selective memory for emotional scenes
Open accessAbstract
Although we know that emotional events enjoy a privileged status in our memories, we still have much to learn about how emotional memories are processed, stored, and how they change over time. Here we show a positive association between REM sleep and the selective consolidation of central, negative aspects of complex scenes. Moreover, we show that the placement of sleep is critical for this selective emotional memory benefit. When testing occurred 24 h post-encoding, subjects who slept soon after learning (24 h Sleep First group) had superior memory for emotional objects compared to subjects whose sleep was delayed for 16 h post-encoding following a full day of wakefulness (24 h Wake First group). However, this increase in memory for emotional objects corresponded with a decrease in memory for the neutral backgrounds on which these objects were placed. Furthermore, memory for emotional objects in the 24 h Sleep First group was comparable to performance after just a 12 h delay containing a night of sleep, suggesting that sleep soon after learning selectively stabilizes emotional memory. These results suggest that the sleeping brain preserves in long-term memory only what is emotionally salient and perhaps most adaptive to remember.
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Sleep 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, Chambers, & Kensinger, 2012
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Regulation of hippocampal dendritic spines following sleep deprivation
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Self-citationDenis, D., Sanders, K. E. G., Kensinger, E., & Payne, J. D. (2022) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2202657119 · Cited by 47 · see citing works
Self-citationRihm, J. S., & Rasch, B. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.04.008 · Cited by 50 · see citing works
Selective effects of sleep on emotional memory: What mechanisms are responsible?
Bennion, K. A., Payne, J. D., & Kensinger, E. A. (2015) · Translational Issues in Psychological Science · doi:10.1037/tps0000019 · Cited by 49 · see citing works
Self-citationThe Role of Sleep in Human Declarative Memory Consolidation
Alger, S. E., Chambers, A. M., Cunningham, T. J., & Payne, J. D. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_341 · Cited by 49 · see citing works
Self-citationThe 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-citationAlger, S. E., & Payne, J. D. (2016) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-016-0460-1 · Cited by 50 · see citing works
Self-citationSleep and intrusive memories immediately after a traumatic event in emergency department patients
Porcheret, K., Iyadurai, L., Bonsall, M. B., Goodwin, G. M., Beer, S., Darwent, M., & Holmes, E. A. (2020) · SLEEP · doi:10.1093/sleep/zsaa033 · Cited by 45 · see citing works
Current research and emerging directions in emotion-cognition interactions
Dolcos, F., Wang, L., & Mather, M. (2014) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2014.00083 · Cited by 45 · see citing works
Role of sleep for encoding of emotional memory
Kaida, K., Niki, K., & Jan Born, A. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.04.002 · Cited by 45 · see citing works
Targeted memory reactivation in REM but not SWS selectively reduces arousal responses
Hutchison, I. C., Pezzoli, S., Tsimpanouli, M.-E., Abdellahi, M. E. A., Pobric, G., Hulleman, J., & Lewis, P. A. (2021) · Communications Biology · doi:10.1038/s42003-021-01854-3 · Cited by 43 · see citing works
Daily Life Experiences in Dreams and Sleep-Dependent Memory Consolidation
Eichenlaub, J.-B., Cash, S. S., & Blagrove, M. (2017) · Studies in Neuroscience, Psychology and Behavioral Economics · doi:10.1007/978-3-319-45066-7_10 · Cited by 42 · see citing works
Relearn Faster and Retain Longer
Mazza, S., Gerbier, É., Gustin, M., Kasikci, Z., Koenig, O., Toppino, T. C., & Magnin, M. (2016) · Psychological Science · doi:10.1177/0956797616659930 · Cited by 44 · see citing works
Kim, S. Y., Kark, S. M., Daley, R. T., Alger, S. E., Reboucas, D. A., Kensinger, E. A., & Payne, J. D. (2019) · Hippocampus · doi:10.1002/hipo.23138 · Cited by 42 · see citing works
Self-citationBennion, K. A., Payne, J. D., & Kensinger, E. (2016) · Behavioral Neuroscience · doi:10.1037/bne0000142 · Cited by 41 · see citing works
Self-citationSleep spindles provide indirect support to the consolidation of emotional encoding contexts
Cairney, S. A., Durrant, S. J., Jackson, R. L., & Lewis, P. A. (2014) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2014.09.016 · Cited by 39 · see citing works
Morning REM Sleep Naps Facilitate Broad Access to Emotional Semantic Networks
Carr, M., & Nielsen, T. (2015) · SLEEP · doi:10.5665/sleep.4504 · Cited by 39 · see citing works
Laugh yourself to sleep: memory consolidation for humorous information
Chambers, A. M., & Payne, J. D. (2013) · Experimental Brain Research · doi:10.1007/s00221-013-3779-7 · Cited by 38 · see citing works
Self-citationHarrington, M. O., Johnson, J. M., Croom, H., Pennington, K., & Durrant, S. J. (2018) · Cortex; a journal devoted to the study of the nervous system and behavior · doi:10.1016/j.cortex.2017.12.004 · Cited by 30 · see citing works
The digital divide and its impact on the development of Mediterranean countries
Pérez-Castro, M. Á., Maslouhi, M. M., & Alonso, M. Á. M. (2020) · Technology in Society · doi:10.1016/j.techsoc.2020.101452 · Cited by 36 · see citing works
Cunningham, T. J., Stickgold, R., & Kensinger, E. A. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.910317 · Cited by 34 · see citing works
Self-citationCecchini, M. G., Iannoni, M. E., Aceto, P., Baroni, E., Vito, C. D., & Lai, C. (2017) · Infant Behavior and Development · doi:10.1016/j.infbeh.2017.06.004 · Cited by 33 · see citing works
Porcheret, K., der Kloet, D. V. H., Goodwin, G. M., Foster, F., Wulff, K., & Holmes, E. A. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0403-z · Cited by 31 · see citing works
The Amygdala and Prioritization of Declarative Memories
Manns, J. R., & Bass, D. I. (2016) · Current Directions in Psychological Science · doi:10.1177/0963721416654456 · Cited by 31 · see citing works
Harrington, 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 · see citing works
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 31 · see citing works
Self-citationCunningham, T. J., Chambers, A. M., & Payne, J. D. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.00862 · Cited by 32 · see citing works
Self-citationTest 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 · see citing works
Both slow wave and rapid eye movement sleep contribute to emotional memory consolidation
Yüksel, Ç., Denis, D., Coleman, J., Ren, B., Oh, A., Cox, R., Morgan, A., Sato, E., & Stickgold, R. (2025) · Communications Biology · doi:10.1038/s42003-025-07868-5 · Cited by 43 · see citing works
Consolidation of Prospective Memory: Effects of Sleep on Completed and Reinstated Intentions
Barner, C., Seibold, M., Born, J., & Diekelmann, S. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.02025 · Cited by 29 · see citing works
Sleep’s contribution to memory formation
Lutz, N. D., Harkotte, M., & Jan Born, A. (2025) · Physiological Reviews · doi:10.1152/physrev.00054.2024 · Cited by 40 · see citing works
Kensinger, E., & Kark, S. M. (2018) · doi:10.1002/9781119170174.epcn101
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 · see citing works
Nightmares and Nightmare Function
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Hokett, E., & Duarte, A. (2019) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2019.00176 · Cited by 24 · see citing works
The Effect of Obstructive Sleep Apnea on Sleep-dependent Emotional Memory Consolidation
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Noradrenergic Mechanisms of Arousal’s Bidirectional Effects on Episodic Memory
Clewett, D. V., Sakaki, M., Nielsen, S., Petzinger, G., & Mather, M. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.10.017 · Cited by 20 · see citing works
Sharp Wave-Ripples in Human Amygdala and Their Coordination with Hippocampus during NREM Sleep
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Evidence of an active role of dreaming in emotional memory processing shows that we dream to forget
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Hippocampal Contributions to Declarative Memory Consolidation During Sleep
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Higher post-encoding cortisol benefits the selective consolidation of emotional aspects of memory
Cunningham, T. J., Mattingly, S. M., Tlatenchi, A., Wirth, M. M., Alger, S. E., Kensinger, E. A., & Payne, J. D. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107411 · Cited by 22 · see citing works
Self-citationDo different salience cues compete for dominance in memory over a daytime nap?
Alger, S. E., Chen, S., & Payne, J. D. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.06.005 · Cited by 23 · see citing works
Self-citationDenis, D., Kim, S. Y., Kark, S. M., Daley, R. T., Kensinger, E. A., & Payne, J. D. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15132 · Cited by 23 · see citing works
Self-citationNegative reinforcement impairs overnight memory consolidationPreprint
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Pereira, S. I. R., Tsimpanouli, M.-E., Hutchison, I. C., Schneider, J., Anderson, I. M., McFarquhar, M., Elliott, R., & Lewis, P. A. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119120 · Cited by 21 · see citing works
Residual effects of emotion are reflected in enhanced visual activity after sleep
Bennion, K. A., Payne, J. D., & Kensinger, E. A. (2016) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-016-0479-3 · Cited by 21 · see citing works
Self-citationSuppression-induced forgetting diminishes following a delay of either sleep or wake
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Future-relevant memories are not selectively strengthened during sleep
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Sleep selectively stabilizes contextual aspects of negative memories
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The ‘affect tagging and consolidation’ (ATaC) model of depression vulnerability
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Asymmetrical Effects of Sleep and Emotions in Daily Life
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Time, Not Sleep, Unbinds Contexts from Item Memory
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Overnight sleep benefits both neutral and negative direct associative and relational memory
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REM refines and rescues memory representations: a new theory
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Age-related positivity effect in emotional memory consolidation from middle age to late adulthood
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Self-citationRecall and recognition of discourse memory across sleep and wake
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Individual alpha frequency modulates sleep-related emotional memory consolidation
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Zhang, K., Lian, N., Ding, R., Guo, C., Dong, X., Li, Y., Wei, S., Jiao, Q., Yu, Y., & Shen, H. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.589176 · Cited by 17 · see citing works
- Authors
- Payne, J. D., Chambers, A. M., & Kensinger, E. A.
- Affiliations
- University of Notre Dame (US)
- Boston College (US)
- Corresponding author
- Payne, Jessica D.
- Venue
- Frontiers in Integrative Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2012
- Volume
- 6
- Pages
- 108-108
- ISSN
- 1662-5145 (ISSN-L)
- PMC
- PMC3503264
- OpenAlex
- W2111745829
- Cited by
- 183
- References
- 67
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 13 · 2023: 14 · 2022: 10 · 2021: 11 · 2020: 14 · 2019: 15 · 2018: 16 · 2017: 18 · 2016: 12 · 2015: 20 · 2014: 24 · 2013: 5
- FWCI
- 8.03
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Integrative Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Science Foundation (0963581)
- National Institutes of Health (MH48,832)
- National Institute of Mental Health (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
- REM sleep, emotional memory, memory consolidation, selective memory, emotional scenes, sleep timing, long-term memory, emotional salience, negative emotional stimuli
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