Sleep Spindles and Their Significance for Declarative Memory Consolidation
Abstract
Study objectives Functional significance of stage 2 sleep spindle activity for declarative memory consolidation. Design Randomized, within-subject, multicenter. Setting Weekly sleep laboratory visits, actigraphy, and sleep diary (4 weeks). Participants Twenty-four healthy subjects (12 men) aged between 20 and 30 years. Interventions Declarative memory task or nonlearning control task before sleep. Measurement and results This study measured spindle activity during stage 2 sleep following a (declarative) word-pair association task as compared to a control task. Participants performed a cued recall in the evening after learning (160 word pairs) as well as in the subsequent morning after 8 hours of undisturbed sleep with full polysomnography. Overnight change in the number of recalled words, but not absolute memory performance, correlated significantly with increased spindle activity during the experimental night (r24 = .63, P Conclusion A growing body of evidence supports the active role of sleep for information reprocessing. Whereas past research focused mainly on the distinct rapid eye movement and slow-wave sleep, these results indicate that increased sleep stage 2 spindle activity is related to an increase in recall performance and, thus, may reflect memory consolidation.
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Indicators of sleep spindle expression consistently correlated with the amount of overnight retention of declarative memories.
“Furthermore, indicators of sleep spindle expression consistently correlated with the amount of overnight retention of declarative memories (86,213,214,235,446,562,822,1016,1024,1037,1044,1057).”
From About Sleep's Role in Memory (2013) · cites this paper as [1037]
Cites
The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research
Buysse, D. J., Reynolds, C. F., Monk, T. H., Berman, S. R., & Kupfer, D. J. (1989) · Psychiatry Research · doi:10.1016/0165-1781(89)90047-4 · Cited by 35,234 · see citing works
A self-rating depression scale
ZUNG, W. W. K. (1965) · Archives of General Psychiatry · doi:10.1001/archpsyc.1965.01720310065008 · Cited by 9,813 · see citing works
Effects of early and late nocturnal sleep on declarative and procedural memory
Plihal, W., & Born, J. (1997) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1997.9.4.534 · Cited by 1,026 · see citing works
Sleep-dependent learning: A nap is as good as a night
Mednick, S., Nakayama, K., & Stickgold, R. (2003) · Nature Neuroscience · doi:10.1038/nn1078 · Cited by 594 · see citing works
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Diekelmann, S., & Born, J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2762 · Cited by 3,760 · see citing works
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
Sleep-dependent memory consolidation
Stickgold, R. (2005) · Nature · doi:10.1038/nature04286 · Cited by 1,857 · see citing works
The hyperarousal model of insomnia: A review of the concept and its evidence
Riemann, D., Spiegelhalder, K., Feige, B., Voderholzer, U., Berger, M., Perlis, M., & Nissen, C. (2010) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2009.04.002 · Cited by 1,789 · see citing works
Sleep spindles: mechanisms and functions
Fernandez, L. M. J., & Lüthi, A. (2020) · Physiological Reviews · doi:10.1152/physrev.00042.2018 · Cited by 716 · see citing works
Mölle, M., Bergmann, T. O., Marshall, L., & Born, J. (2011) · Sleep · doi:10.5665/sleep.1290 · Cited by 557 · see citing works
The whats and whens of sleep-dependent memory consolidation
Diekelmann, S., Wilhelm, I., & Born, J. (2009) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2008.08.002 · Cited by 566 · see citing works
Wamsley, E. J., Tucker, M. A., Shinn, A. K., Ono, K. E., McKinley, S. K., Ely, A. V., Goff, D. C., Stickgold, R., & Manoach, D. S. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.08.008 · Cited by 492 · see citing works
Sleep Spindles in Humans: Insights from Intracranial EEG and Unit Recordings
Andrillon, T., Nir, Y., Staba, R. J., Ferrarelli, F., Cirelli, C., Tononi, G., & Fried, I. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.2604-11.2011 · Cited by 504 · see citing works
Sleep spindle activity is associated with the integration of new memories and existing knowledge
Tamminen, J., Payne, J. D., Stickgold, R., Wamsley, E. J., & Gaskell, M. G. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3028-10.2010 · Cited by 478 · see citing works
Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans
Clemens, Z., Molle, M., Eross, L., Barsi, P., Halasz, P., & Born, J. (2007) · Brain · doi:10.1093/brain/awm146 · Cited by 398 · see citing works
Sleep selectively enhances memory expected to be of future relevance
Wilhelm, I., Diekelmann, S., Molzow, I., Ayoub, A., Mölle, M., & Born, J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3575-10.2011 · Cited by 397 · see citing works
Learning‐dependent changes in sleep spindles and Stage 2 sleep
FOGEL, S. M., & SMITH, C. T. (2006) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2006.00522.x · Cited by 344 · see citing works
Mölle, M., Eschenko, O., Gais, S., Sara, S. J., & Born, J. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06654.x · Cited by 322 · see citing works
Functional Neuroimaging Insights into the Physiology of Human Sleep.
Dang-Vu, T. T., Schabus, M., Desseilles, M., Sterpenich, V., Bonjean, M., & Maquet, P. (2010) · SLEEP · doi:10.1093/sleep/33.12.1589 · Cited by 284 · see citing works
Sleep and memory in healthy children and adolescents - a critical review
Kopasz, M., Loessl, B., Hornyak, M., Riemann, D., Nissen, C., Piosczyk, H., & Voderholzer, U. (2010) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2009.10.006 · Cited by 277 · see citing works
Sleep spindles in midday naps enhance learning in preschool children
Kurdziel, L., Duclos, K., & Spencer, R. M. C. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1306418110 · Cited by 266 · see citing works
Slow oscillations orchestrating fast oscillations and memory consolidation
Mölle, M., & Born, J. (2011) · Progress in Brain Research · doi:10.1016/b978-0-444-53839-0.00007-7 · Cited by 270 · see citing works
Schabus, M., Hödlmoser, K., Gruber, G., Sauter, C., Anderer, P., Klösch, G., Parapatics, S., Saletu, B., Klimesch, W., & Zeitlhofer, J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04694.x · Cited by 261 · see citing works
Self-citationProcessing of emotional reactivity and emotional memory over sleep
Baran, B., Pace-Schott, E. F., Ericson, C., & Spencer, R. M. C. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.2532-11.2012 · Cited by 254 · see citing works
“Such misperceptions have been observed by others (Carskadon et al., 1976; Silva et al., 2007).”
Dreaming of a learning task is associated with enhanced sleep-dependent memory consolidation
Wamsley, E. J., Tucker, M., Payne, J. D., Benavides, J. A., & Stickgold, R. (2010) · Current Biology · doi:10.1016/j.cub.2010.03.027 · Cited by 255 · see citing works
FOGEL, S., SMITH, C., & COTE, K. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.02.037 · Cited by 246 · see citing works
Bergmann, T. O., Mölle, M., Diedrichs, J., Born, J., & Siebner, H. R. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.036 · Cited by 228 · see citing works
Learning to modulate one’s own brain activity: The effect of spontaneous mental strategies
Kober, S. E., Witte, M., Ninaus, M., Neuper, C., & Wood, G. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00695 · Cited by 225 · see citing works
Eschenko, O., Magri, C., Panzeri, S., & Sara, S. J. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr121 · Cited by 194 · see citing works
Clemens, Z., Fabó, D., & Halász, P. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.04.035 · Cited by 179 · see citing works
Is there a link between sleep changes and memory in Alzheimer's disease?
Rauchs, G., Schabus, M., Parapatics, S., Bertran, F., Clochon, P., Hot, P., Denise, P., Desgranges, B., Eustache, F., Gruber, G., et al. (2008) · NeuroReport · doi:10.1097/wnr.0b013e32830867c4 · Cited by 179 · see citing works
Self-citationInterindividual sleep spindle differences and their relation to learning-related enhancements
Schabus, M., Hoedlmoser, K., Pecherstorfer, T., Anderer, P., Gruber, G., Parapatics, S., Sauter, C., Kloesch, G., Klimesch, W., Saletu, B., et al. (2008) · Brain Research · doi:10.1016/j.brainres.2007.10.106 · Cited by 174 · see citing works
Self-citationDecoding material-specific memory reprocessing during sleep in humans
Schönauer, M., Alizadeh, S., Jamalabadi, H., Abraham, A., Pawlizki, A., & Gais, S. (2017) · Nature Communications · doi:10.1038/ncomms15404 · Cited by 139 · see citing works
Slow oscillation-spindle coupling predicts enhanced memory formation from childhood to adolescence
Hahn, M. A., Heib, D., Schabus, M., Hoedlmoser, K., & Helfrich, R. F. (2020) · eLife · doi:10.7554/elife.53730 · Cited by 140 · see citing works
Self-citationKaestner, E. J., Wixted, J. T., & Mednick, S. C. (2013) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00433 · Cited by 149 · see citing works
Targeted memory reactivation during sleep depends on prior learning
Creery, J. D., Oudiette, D., Antony, J. W., & Paller, K. A. (2015) · SLEEP · doi:10.5665/sleep.4670 · Cited by 150 · see citing works
The Role of Sleep in Directed Forgetting and Remembering of Human Memories
Saletin, J. M., Goldstein, A. N., & Walker, M. P. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr034 · Cited by 151 · see citing works
Future Research Directions in Sleep and ADHD: Report of a Consensus Working Group
Owens, J., Gruber, R., Brown, T., Corkum, P., Cortese, S., O’Brien, L., Stein, M., & Weiss, M. (2013) · Journal of Attention Disorders · doi:10.1177/1087054712457992 · Cited by 143 · see citing works
Sleep-Dependent Facilitation of Episodic Memory Details
van der Helm, E., Gujar, N., Nishida, M., & Walker, M. P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027421 · Cited by 138 · see citing works
Memory consolidation as an adaptive process
Cowan, E. T., Schapiro, A. C., Dunsmoor, J. E., & Murty, V. P. (2021) · Psychonomic Bulletin & Review · doi:10.3758/s13423-021-01978-x · Cited by 133 · see citing works
NREM2 and sleep spindles are instrumental to the consolidation of motor sequence memories
Laventure, S., Fogel, S., Lungu, O., Albouy, G., Sévigny-Dupont, P., Vien, C., Sayour, C., Carrier, J., Benali, H., & Doyon, J. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002429 · Cited by 132 · see citing works
Wamsley, E. J., Perry, K., Djonlagic, I., Reaven, L. B., & Stickgold, R. (2010) · Sleep · doi:10.1093/sleep/33.1.59 · Cited by 124 · see citing works
Memory, sleep, and dreaming: experiencing consolidation
Wamsley, E. J., & Stickgold, R. (2011) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2010.12.008 · Cited by 115 · see citing works
Daytime napping: Effects on human direct associative and relational memory
Lau, H., Tucker, M. A., & Fishbein, W. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.02.003 · Cited by 115 · see citing works
Prehn-Kristensen, A., Göder, R., Fischer, J., Wilhelm, I., Seeck-Hirschner, M., Aldenhoff, J., & Baving, L. (2011) · Sleep Medicine · doi:10.1016/j.sleep.2010.10.010 · Cited by 114 · see citing works
Sleep function: current questions and new approaches
Vassalli, A., & Dijk, D. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06767.x · Cited by 110 · see citing works
Cowan, E., Liu, A., Henin, S., Kothare, S., Devinsky, O., & Davachi, L. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.1946-19.2020 · Cited by 97 · see citing works
Sleep spindles as facilitators of memory formation and learning
Ulrich, D. (2016) · Neural Plasticity · doi:10.1155/2016/1796715 · Cited by 94 · see citing works
A mechanism for learning with sleep spindles
Peyrache, A., & Seibt, J. (2020) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2019.0230 · Cited by 89 · see citing works
Structural brain correlates of human sleep oscillations
Saletin, J. M., van der Helm, E., & Walker, M. P. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.06.021 · Cited by 93 · see citing works
Ayoub, A., Aumann, D., Hörschelmann, A., Kouchekmanesch, A., Paul, P., Born, J., & Marshall, L. (2013) · Sleep · doi:10.5665/sleep.2722 · Cited by 91 · see citing works
Wamsley, E. J., Tucker, M. A., Payne, J. D., & Stickgold, R. (2010) · Learning & Memory · doi:10.1101/lm.1828310 · Cited by 89 · see citing works
Sleep stage II contributes to the consolidation of declarative memories
Ruch, S., Markes, O., Duss, S. B., Oppliger, D., Reber, T. P., Koenig, T., Mathis, J., Roth, C., & Henke, K. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.06.008 · Cited by 88 · see citing works
The sleeping infant brain anticipates development
Friedrich, M., Wilhelm, I., Mölle, M., Born, J., & Friederici, A. D. (2017) · Current Biology · doi:10.1016/j.cub.2017.06.070 · Cited by 77 · see citing works
Overnight 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
A local signature of LTP‐ and LTD‐like plasticity in human NREM sleep
Bergmann, T. O., Mölle, M., Marshall, L., Kaya‐Yildiz, L., Born, J., & Roman Siebner, H. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06178.x · Cited by 67 · see citing works
Sleep Spindle Activity Is Correlated With Reading Abilities in Developmental Dyslexia
Bruni, O., Ferri, R., Novelli, L., Terribili, M., Troianiello, M., Finotti, E., Leuzzi, V., & Curatolo, P. (2009) · Sleep · doi:10.1093/sleep/32.10.1333 · Cited by 66 · see citing works
Hokett, E., Arunmozhi, A., Campbell, J., Verhaeghen, P., & Duarte, A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.05.010 · Cited by 60 · see citing works
Höhn, C., Schmid, S. R., Plamberger, C. P., Bothe, K., Angerer, M., Gruber, G., Pletzer, B., & Hoedlmoser, K. (2021) · Clocks & Sleep · doi:10.3390/clockssleep3010005 · Cited by 61 · see citing works
“This was followed by two encoding blocks of a declarative learning task (adapted from Schabus and colleagues [85]).”
BackgroundMethodSelf-citationSleep spindles track cortical learning patterns for memory consolidation
Petzka, M., Chatburn, A., Charest, I., Balanos, G. M., & Staresina, B. P. (2022) · Current Biology · doi:10.1016/j.cub.2022.04.045 · Cited by 63 · see citing works
Spindle activity orchestrates plasticity during development and sleep
Lindemann, C., Ahlbeck, J., Bitzenhofer, S. H., & Hanganu-Opatz, I. L. (2016) · Neural Plasticity · doi:10.1155/2016/5787423 · Cited by 59 · see citing works
Sleep in humans stabilizes pattern separation performance
Hanert, A., Weber, F. D., Pedersen, A., Born, J., & Bartsch, T. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.1189-17.2017 · Cited by 52 · see citing works
Cortical reactivations during sleep spindles following declarative learning
Jegou, A., Schabus, M., Gosseries, O., Dahmen, B., Albouy, G., Desseilles, M., Sterpenich, V., Phillips, C., Maquet, P., Grova, C., et al. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.03.051 · Cited by 54 · see citing works
Self-citationHow to become an expert: a new perspective on the role of sleep in the mastery of procedural skills
Fogel, S. M., Ray, L. B., Binnie, L., & Owen, A. M. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.10.004 · Cited by 55 · see citing works
Developmental changes in sleep spindle characteristics and sigma power across early childhood
McClain, I. J., Lustenberger, C., Achermann, P., Lassonde, J. M., Kurth, S., & LeBourgeois, M. K. (2016) · Neural Plasticity · doi:10.1155/2016/3670951 · Cited by 52 · see citing works
Friedrich, M., Mölle, M., Friederici, A. D., & Born, J. (2020) · Nature Communications · doi:10.1038/s41467-020-14850-8 · Cited by 49 · see citing works
The Significance of Sigma Neurofeedback Training on Sleep Spindles and Aspects of Declarative Memory
Berner, I., Schabus, M., Wienerroither, T., & Klimesch, W. (2006) · Applied Psychophysiology and Biofeedback · doi:10.1007/s10484-006-9013-7 · Cited by 49 · see citing works
Self-citationMental Sleep Activity and Disturbing Dreams in the Lifespan
Scarpelli, S., Bartolacci, C., D’Atri, A., Gorgoni, M., & De Gennaro, L. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16193658 · Cited by 41 · see citing works
“Spindle activity is involved in long-term memory consolidation [30,31] and cognitive abilities [32].”
Friedrich, M., Mölle, M., Friederici, A. D., & Born, J. (2019) · Developmental Science · doi:10.1111/desc.12743 · Cited by 38 · see citing works
Eckert, M. J., McNaughton, B. L., & Tatsuno, M. (2020) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2019.0655 · Cited by 34 · see citing works
Spindle-dependent memory consolidation in healthy adults: a meta-analysis
Kumral, D., Matzerath, A., Leonhart, R., & Schönauer, M. (2023) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2023.108661 · Cited by 32 · see citing works
Sleep restriction can attenuate prioritization benefits on declarative memory consolidation
Lo, J. C., Bennion, K. A., & Chee, M. W. L. (2016) · Journal of Sleep Research · doi:10.1111/jsr.12424 · Cited by 29 · see citing works
Mikoteit, T., Brand, S., Beck, J., Perren, S., von Wyl, A., von Klitzing, K., Holsboer-Trachsler, E., & Hatzinger, M. (2012) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2011.562241 · Cited by 21 · see citing works
Rauchs, G., Harand, C., Bertran, F., Desgranges, B., & Eustache, F. (2010) · Revue Neurologique · doi:10.1016/j.neurol.2010.03.021 · Cited by 19 · see citing works
Llewellyn, S. (2016) · Consciousness and Cognition · doi:10.1016/j.concog.2016.09.018 · Cited by 17 · see citing works
Memory for nonadjacent dependencies in the first year of life and its relation to sleep
Friedrich, M., Mölle, M., Born, J., & Friederici, A. D. (2022) · Nature Communications · doi:10.1038/s41467-022-35558-x · Cited by 12 · see citing works
Sleep and individual differences in intellectual abilities
Smith, D., Fang, Z., Thompson, K., & Fogel, S. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.02.011 · Cited by 8 · see citing works
- Authors
- Schabus, M., Gruber, G., Parapatics, S., Sauter, C., Klösch, G., Anderer, P., Klimesch, W., Saletu, B., & Zeitlhofer, J.
- Affiliations
- University of Salzburg (AT)
- Medical University of Vienna (AT)
- Corresponding author
- Schabus, Manuel
- Venue
- Sleep
- Publisher
- Oxford University Press (OUP)
- Published
- 2004-12
- Volume
- 27
- Issue
- 8
- Pages
- 1479-1485
- ISSN
- 0161-8105 (ISSN-L)
- 1550-9109
- OpenAlex
- W2151528679
- Cited by
- 560
- References
- 4
- Citations by year
- 2026: 14 · 2025: 18 · 2024: 21 · 2023: 20 · 2022: 21 · 2021: 26 · 2020: 37 · 2019: 40 · 2018: 28 · 2017: 40 · 2016: 40 · 2015: 31 · 2014: 36 · 2013: 38 · 2012: 31
- FWCI
- 4.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- SLEEP (publishedVersion)
- PubMed (publishedVersion)
- Funders
- European Commission
- Austrian Science Fund
- 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 spindles, stage 2 sleep, declarative memory consolidation, word pair association, cued recall, memory reprocessing, sleep-dependent memory, polysomnography
- MeSH terms
- Adult, Algorithms, Cues, Electrodes, Female, Humans, Male, Mastoid, Memory, Sleep, REM, Polysomnography, Intention
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