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Sleep-dependent memory triage: evolving generalization through selective processing
Open accessAbstract
The brain does not retain all the information it encodes in a day. Much is forgotten, and of those memories retained, their subsequent evolution can follow any of a number of pathways. Emerging data makes clear that sleep is a compelling candidate for performing many of these operations. But how does the sleeping brain know which information to preserve and which to forget? What should sleep do with that information it chooses to keep? For information that is retained, sleep can integrate it into existing memory networks, look for common patterns and distill overarching rules, or simply stabilize and strengthen the memory exactly as it was learned. We suggest such 'memory triage' lies at the heart of a sleep-dependent memory processing system that selects new information, in a discriminatory manner, and assimilates it into the brain's vast armamentarium of evolving knowledge, helping guide each organism through its own, unique life.
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“Across diverse forms memory, sleep following encoding results in improved memory performance after a delay [13, 14].”
From Constructive episodic simulation in dreams (2022) · cites this paper as [14]
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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 [66]
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“On the other hand, sleep enables the extraction of regularities across instances, the loss of contextual information and the retention of gist, as seen in representations in extra-hippocampal regions 89,97 .”
From From cognitive maps to spatial schemas (2023) · cites this paper as [97]
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“…on sleep (Ellenbogen et al., 2006; Jenkins and Dallenbach, 1924; Walker et al., 2002), with greatest importance usually ascribed to non-rapid eye movement (NREM) sleep, and a relatively poorly understood role for rapid eye movement (REM) sleep (Rasch and Born, 2013; Stickgold and Walker, 2013).”
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“Recent work in both humans and animal models has demonstrated the importance of specific brain oscillations, including sleep spindles, in the consolidation of different memory types during sleep (Dudai et al., 2015; Rasch and Born, 2013; Stickgold and Walker, 2013).”
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“This also entails new memories being integrated with old memories so that new and old memories can infl uence one another (Davis & Gaskell, 2009; Davis et al., 2009; Stickgold & Walker, 2013; Walker & Stickgold, 2010).”
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“Previous studies have shown that consolidation involves extracting the commonalities across distinct experiences (Rasch and Born, 2008, 2013; Lewis and Durrant, 2011; Stickgold and Walker, 2013).”
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Emotional Memory Processing during REM Sleep with Implications for Post-Traumatic Stress Disorder
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“…Levin & Nielsen, 2009) whereas others stem from studying offline memory processes during sleep (Llewellyn, 2013a, 2013b; Payne, 2010; Stickgold & Walker, 2013; Walker & van der Helm, 2009; Wamsley & Stickgold, 2010), they provide different answers to the question whether dreams only reflect, or…”
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Melnattur, K. V., Kirszenblat, L., Morgan, E. P., Militchin, V., Sakran, B., English, D., Patel, R., Chan, D., van Swinderen, B., & Shaw, P. J. (2020) · SLEEP · doi:10.1093/sleep/zsaa197 · Cited by 22
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ResultHippocampal Contributions to Declarative Memory Consolidation During Sleep
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“However, in addition to memory, sleep aids the generalization and abstraction of information, which may rely on reactivation (Stickgold and Walker 2013).”
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BackgroundDo different salience cues compete for dominance in memory over a daytime nap?
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“While different causal mechanisms have been discussed to underlie thememory function of sleep [10, 44], the active system consolidation hypothesis proposes that during sleep, memory traces are gradually strengthened and integrated into cortical longterm memory based on repeated and spontaneous hippocampal reactivation…”
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“…is required (e.g., Van der Werf et al., 2009), whereas a vast amount of literature supports the role of sleep in the consolidation of both hippocampal-dependent and hippocampal-independent memories (for recent reviews see Diekelmann & Born, 2010; Rasch & Born, 2013; Stickgold & Walker, 2013).”
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“However, sleep‐dependent memory consolidation in adults does not occur indiscriminately (for a review, see Stickgold & Walker, 2013).”
BackgroundInfluentialThe bio-habitable zone and atmospheric properties for planets of red dwarfs
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Motor imagery practice benefits during arm immobilization
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“encoding recently learned information continues to be processed during offline periods wherein memories are selectively retained or pruned via covert reactivation and consolidation processes (Rasch and Born, 2013; Stickgold and Walker, 2013; Tambini and Davachi, 2019; Hu et al., 2020).”
BackgroundPharmacological Treatment of Sleep Disorders and Its Relationship with Neuroplasticity
Abad, V. C., & Guilleminault, C. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_365 · Cited by 22
Yoshiike, T., Honma, M., Yamada, N., Kim, Y., & Kuriyama, K. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.06.015 · Cited by 21
Cody, S. L., Fazeli, P. L., Crowe, M. G., Kempf, M.-C., Moneyham, L. L., Stavrinos, D., Vance, D. E., & Heaton, K. L. (2019) · Applied Neuropsychology Adult · doi:10.1080/23279095.2018.1534736 · Cited by 20
“…homeostasis hypothesis, sleep plays a functional role in synaptic plasticity or strengthening of neuronal connections and promotes growth of new neurons in the hippocampus, particularly the dentate gyrus which involves the formation of memories (Stickgold & Walker, 2013; Tononi & Cirelli, 2014).”
BackgroundGist extraction and sleep in 12-month-old infants
Konrad, C., Herbert, J. S., Schneider, S., & Seehagen, S. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.08.021 · Cited by 20
“Thus, sleep might help infants to extract rules from relations (Stickgold & Walker, 2013).”
Active forgetting and neuropsychiatric diseases
Berry, J. A., Guhle, D. C., & Davis, R. L. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02521-9 · Cited by 21
Sleep sharpens sensory stimulus coding in human visual cortex after fear conditioning
Virginie Sterpenich, A., Piguet, C., Desseilles, M., Ceravolo, L., Gschwind, M., Ville, D. V. D., Vuilleumier, P. O., & Schwartz, S. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.06.003 · Cited by 19
“…new evidence for a role of sleep in both quantitative and qualitative changes of memory representations (Diekelmann and Born, 2010; Maquet, 2001; Stickgold and Walker, 2013), here driven by emotional significance, arising in category-specific sensory cortices, and characterized by…”
BackgroundInfluentialHonma, M., Plass, J., Brang, D., Florczak, S. M., Grabowecky, M., & Paller, K. A. (2016) · Neuroscience of Consciousness · doi:10.1093/nc/niw020 · Cited by 21
“…consolidation can facilitate both the selection of important information for storage (Fischer and Born, 2009; Wilhelm et al. , 2011) and the integration of novel information into existing neural representations (e.g., Tamminen et al. , 2010; Lewis and Durrant, 2011; Stickgold and Walker, 2013).”
Long-term effects of directed forgetting
Hupbach, A. (2017) · Memory · doi:10.1080/09658211.2017.1358748 · Cited by 22
“…in line with findings showing that information that was tagged as relevant during or shortly after encoding is preferentially consolidated in comparison to information that was tagged as irrelevant (Diekelmann & Born, 2010; Dudai, Karni, & Born, 2015; Gruber et al., 2016; Stickgold & Walker, 2013).”
BackgroundResultInfluentialSleep selectively stabilizes contextual aspects of negative memories
Cox, R., van Bronkhorst, M. L. V., Bayda, M., Gomillion, H., Cho, E., Parr, E., Manickas-Hill, O. P., Schapiro, A. C., & Stickgold, R. (2018) · Scientific Reports · doi:10.1038/s41598-018-35999-9 · Cited by 22
Self-citationActive transitive inference: When learner control facilitates integrative encoding
Markant, D. B. (2020) · Cognition · doi:10.1016/j.cognition.2020.104188 · Cited by 19
Sleep quality and outcome of exposure therapy in adults with social anxiety disorder
Dutcher, C. D., Dowd, S. M., Zalta, A. K., Taylor, D. J., Rosenfield, D., Perrone, A., Otto, M. W., Pollack, M. H., Hofmann, S. G., & Smits, J. A. J. (2021) · Depression and Anxiety · doi:10.1002/da.23167 · Cited by 19
“Sleep promotes cognitive flexibility in problem‐ solving, aids integration of new information, and helps stimulate memory associations (Stickgold & Walker, 2013).”
BackgroundEngineering decisions: Information, knowledge and understanding
Brown, C. B., & Elms, D. G. (2014) · Structural Safety · doi:10.1016/j.strusafe.2014.09.001 · Cited by 19
“Research shows that one function of sleep is to choose between what should be remembered and what should be discarded and forgotten [27].”
BackgroundEichenlaub, J., van Rijn, E., Phelan, M., Ryder, L., Gaskell, M. G., Lewis, P. A., P. Walker, M., & Blagrove, M. (2019) · Journal of Sleep Research · doi:10.1111/jsr.12697 · Cited by 18
“A process of triage for sleep-dependent memory consolidation has been proposed (Stickgold & Walker, 2013) in which there is a differential processing of memories based on factors such as salience, emotional involvement and future relevance.”
BackgroundSelf-citationThe function of REM and NREM sleep on memory distortion and consolidation
Kaida, K., Mori, I., Kihara, K., & Kaida, N. (2023) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2023.107811 · Cited by 22
Impaired off-line motor skills consolidation in young primary insomniacs
Cellini, N., de Zambotti, M., Covassin, N., Sarlo, M., & Stegagno, L. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.06.006 · Cited by 18
Sleep‐dependent memory consolidation is related to perceived value of learned material
van Rijn, E., Lucignoli, C., Izura, C., & Blagrove, M. (2017) · Journal of Sleep Research · doi:10.1111/jsr.12457 · Cited by 18
Chatburn, A., Lushington, K., & Kohler, M. J. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107384 · Cited by 16
Sleep-dependent prospective memory consolidation is impaired with aging
Leong, R. L. F., Lo, J. C.-Y., & Chee, M. W. L. (2021) · SLEEP · doi:10.1093/sleep/zsab069 · Cited by 18
“While sleep unequivocally benefits the consolidation of declarative [1–3] and procedural memory [4–6] in young adults, an increasing number of studies have begun to show that in older adults, this sleep effect is significantly reduced or absent [7–9].”
BackgroundSleep disturbance and memory dysfunction in early multiple sclerosis
Sumowski, J. F., Horng, S. H., Brandstadter, R., Krieger, S. C., Leavitt, V. M., Sand, I. K., Fabian, M. T., Klineova, S., Graney, R., Riley, C., et al. (2021) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.51262 · Cited by 18
“Homeostatic synaptic downscaling during sleep supports the encoding of new information after waking,(17,18) Sleepdependent memory processing also involves discriminate selection of prior wake experiences which are assimilated into existing knowledge (traditionally termed “consolidation”).(15) Given that sleep disturba…”
BackgroundThe Neuroscience of Sleep and Dreams
McNamara, P. (2019) · Cambridge University Press eBooks · doi:10.1017/9781316817094 · Cited by 21
Viczko, J., Sergeeva, V., Ray, L. B., Owen, A. M., & Fogel, S. M. (2018) · Learning & Memory · doi:10.1101/lm.044719.116 · Cited by 20
“One of themost important functions of sleep is to support learning and memory (for reviews, see Maquet 2001; Smith 2001; Doyon et al. 2009b; Fogel and Smith 2011; Rasch and Born 2013; Stickgold and Walker 2013; Stickgold 2013; Tononi and Cirelli 2014).”
BackgroundSleep strengthens integration of spatial memory systemsPreprint
Noack, H., Doeller, C. F., & Jan Born, A. (2021) · Learning & Memory · doi:10.1101/lm.053249.120 · Cited by 19
“…et al. 1999; Doeller et al. 2008; Rich and Shapiro 2009), that is, a region that is not only involved in the abstraction of schemalike spatial representations (Tse et al. 2011; van Buuren et al. 2014) but, also shows neuronal reactivation during sleep (Euston et al. 2007; Peyrache et al. 2009).”
BackgroundLlewellyn, S. (2016) · Consciousness and Cognition · doi:10.1016/j.concog.2016.09.018 · Cited by 17
“Several studies suggest that sleep mentation or its neural substrates impact on subsequent thought and action during wake (Diekelmann & Born, 2010; Stickgold & Walker, 2013; Verleger, Rose, Wagner, Yordanova, & Kolev, 2013), for impact to occur during wake there must be retention from the sleep…”
BackgroundOvernight sleep benefits both neutral and negative direct associative and relational memory
Huguet, M., Payne, J. D., Kim, S. Y., & Alger, S. E. (2019) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-019-00746-8 · Cited by 17
Labile sleep promotes awareness of abstract knowledge in a serial reaction time task.
Kirov, R., Kolev, V., Verleger, R., & Yordanova, J. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01354 · Cited by 17
Age-related positivity effect in emotional memory consolidation from middle age to late adulthood
Niu, X., Utayde, M. F., Sanders, K. E. G., Denis, D., Kensinger, E. A., & Payne, J. D. (2024) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2024.1342589 · Cited by 22
Honma, M., Yoshiike, T., Ikeda, H., Kim, Y., & Kuriyama, K. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085734 · Cited by 17
“Sleep-dependent memory processing guides memory enhancements by selecting the most relevant information from its own autobiographical history and optimally integrates it into memory networks [40].”
BackgroundMalkov, A., Shevkova, L., Latyshkova, A., & Kitchigina, V. F. (2022) · Experimental Neurology · doi:10.1016/j.expneurol.2022.114110 · Cited by 18
Metadata
- Authors
- Stickgold, R., & Walker, M. P.
- Affiliations
- Beth Israel Deaconess Medical Center (US)
- University of California, Berkeley (US)
- Corresponding author
- Stickgold, Robert
- Walker, Matthew P
- Venue
- Nature Neuroscience
- Published
- 2013-01-28
- Volume
- 16
- Issue
- 2
- Pages
- 139-145
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC5826623
- OpenAlex
- W2036537336
- Cited by
- 755
- References
- 77
- Citations by year
- 2026: 29 · 2025: 44 · 2024: 45 · 2023: 113 · 2022: 39 · 2021: 50 · 2020: 58 · 2019: 71 · 2018: 58 · 2017: 60 · 2016: 40 · 2015: 62 · 2014: 58 · 2013: 26
- FWCI
- 5.31
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute on Aging (R01AG031164, AG031164)
- National Institute of Mental Health (MH-48832, R01MH093537, MH093537, R01MH048832, MH92638, R01MH092638)
- National Institute on Drug Abuse (DA031939, R21DA031939)
- 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, forgetting, memory generalization, memory integration, memory stabilization, feature binding, evolution of memory
- MeSH terms
- Animals, Discrimination, Psychological, Humans, Learning, Memory, Psychological Theory, Sleep
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