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Involvement of spindles in memory consolidation is slow wave sleep-specific
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Both sleep spindles and slow oscillations have been implicated in sleep-dependent memory consolidation. Whereas spindles occur during both light and deep sleep, slow oscillations are restricted to deep sleep, raising the possibility of greater consolidation-related spindle involvement during deep sleep. We assessed declarative memory retention over an interval containing a nap and determined spindle density for light and deep sleep separately. In deep sleep, spindle density was considerably higher and showed a strong and robust positive correlation with retention. This relation was absent for light sleep, suggesting that the potentiating effects of spindles are tied to their co-occurrence with slow oscillations.
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“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 [235]
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Cites
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“…this association was more pronounced during deep sleep than during light sleep, the pertaining correlation coefficients were contrasted directly (Meng et al. 1992), revealing a significantly stronger link between memory retention and spindle density during SWS than during stage 2 sleep (Z ¼…”
BackgroundBoosting slow oscillations during sleep potentiates memory
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ResultThe Hippocampo-Neocortical Dialogue
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“As such, the temporal coupling of hippocampal ripples, sleep spindles, and slow oscillations might reflect a hippocampo-cortical di- alogue underlying system-level memory consolidation during sleep (Buzsáki 1996; Born et al. 2006).”
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“Our observed spindle densities are roughly similar to values obtained with other detection algorithms in both EEG (Gais et al. 2002; Mölle et al. 2011) and intracortical (Peter-Derex et al. 2012) studies, suggesting that our finding is not an artifact stemming from the spindle algorithm used.”
BackgroundResultInfluentialGrouping of spindle activity during slow oscillations in human non-rapid eye movement sleep
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“Importantly, slow oscillations have a naturally occurring grouping influence on spindles (Mölle et al. 2002; Clemens et al. 2007), and such focusing of spindle rhythms into the active slow oscillation up-state increases after a learning episode (Mölle et al. 2009).”
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“It should be mentioned that we do not claim that sleep spindles during light sleep are completely unrelated to memory processing, as various studies have demonstrated otherwise (e.g., Gais et al. 2002; Schabus et al. 2008; Tamaki et al. 2008).”
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“As such, the temporal coupling of hippocampal ripples, sleep spindles, and slow oscillations might reflect a hippocampo-cortical di- alogue underlying system-level memory consolidation during sleep (Buzsáki 1996; Born et al. 2006).”
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“As spindle power averaged across SWS of the entire stimulation period did not differ between conditions (Figure S1), these observations indicate that in-phase stimulation chiefly enhanced the synchronization of spindles to the SO and corroborates findings showing that the synchrony with the SO cycle rather than the am…”
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“While fast spindle amount and density have been more consistently shown to be associated with better memory consolidation processes [31, 53], we also found a negative relationship between spindle peak frequency and an increase in learning performance that was unexpected.”
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Sopp, M. R., Brueckner, A. H., Schäfer, S. K., Lass‐Hennemann, J., & Michael, T. (2018) · Sleep Medicine · doi:10.1016/j.sleep.2018.10.030 · Cited by 35
Nap sleep spindle correlates of intelligence
Ujma, P. P., Bódizs, R., Gombos, F., Stintzing, J., Konrad, B. N., Genzel, L., Steiger, A., & Dresler, M. (2015) · Scientific Reports · doi:10.1038/srep17159 · Cited by 30
Phase-based coordination of hippocampal and neocortical oscillations during human sleep
Cox, R., Rüber, T., Staresina, B. P., & Fell, J. (2020) · Communications Biology · doi:10.1038/s42003-020-0913-5 · Cited by 36
Self-citationCharacterization of K-Complexes and Slow Wave Activity in a Neural Mass Model
Weigenand, A., Costa, M. S., Ngo, H.-V. V., Claussen, J. C., & Martinetz, T. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003923 · Cited by 32
“Especially its hallmarks, cortical slow oscillations (SO), are hypothesized to be a key mechanism for the transfer of memory into the neocortical longterm storage [3,4].”
BackgroundThe role of daytime napping in declarative memory performance: a systematic review
Farhadian, N., Khazaie, H., Nami, M., & Khazaie, S. (2021) · Sleep Medicine · doi:10.1016/j.sleep.2021.05.019 · Cited by 28
Targeted memory reactivation to augment treatment in post-traumatic stress disorder
van der Heijden, A. C., van der Werf, Y. D., van den Heuvel, O. A., Talamini, L. M., & van Marle, H. J. F. (2024) · Current Biology · doi:10.1016/j.cub.2024.07.019 · Cited by 30
Self-citationMemory-relevant nap sleep physiology in healthy and pathological aging
Ladenbauer, J., Ladenbauer, J., Külzow, N., & Flöel, A. (2021) · SLEEP · doi:10.1093/sleep/zsab002 · Cited by 28
Valencia, M., Artieda, J., Bolam, J. P., & Mena‐Segovia, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067540 · Cited by 27
“Recent evidence shows that both spindles and gamma play an important part in the functional role of the slow oscillations and have been associated with plasticity and learning processes [12,15].”
BackgroundSleep spindle dynamics suggest over-consolidation in post-traumatic stress disorder
van der Heijden, A. C., Hofman, W. F., de Boer, M., Nijdam, M. J., van Marle, H. J. F., Jongedijk, R. A., Olff, M., & Talamini, L. M. (2022) · SLEEP · doi:10.1093/sleep/zsac139 · Cited by 24
Self-citationOpposite effect of motivated forgetting on sleep spindles during stage 2 and slow wave sleep
Dehnavi, F., Moghimi, S., Haghighi, S. S., Safaie, M., & Ghorbani, M. (2019) · SLEEP · doi:10.1093/sleep/zsz085 · Cited by 24
Is the role of sleep in memory consolidation overrated?
Dastgheib, M., Kulanayagam, A., & Dringenberg, H. C. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104799 · Cited by 27
Farthouat, J., Atas, A., Wens, V., Tiège, X. D., & Peigneux, P. (2018) · Scientific Reports · doi:10.1038/s41598-018-30105-5 · Cited by 23
Incubation, not sleep, aids problem-solving
Brodt, S., Pöhlchen, D., Täumer, E., Gais, S., & Schönauer, M. (2018) · Sleep · doi:10.1093/sleep/zsy155 · Cited by 23
Averaging sleep spindle occurrence in dogs predicts learning performance better than single measures
Iotchev, I. B., Reicher, V., Kovács, E., Kovács, T., Kis, A., Gácsi, M., & Kubinyi, E. (2020) · Scientific Reports · doi:10.1038/s41598-020-80417-8 · Cited by 23
Weiner, O. M., O’Byrne, J., Cross, N. E., Giraud, J., Tarelli, L., Yue, V., Homer, L., Walker, K., Carbone, R., & Dang‐Vu, T. T. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.15980 · Cited by 29
“…and proxy-measures of sigma ( σ ) power, have been shown to promote sleep stability (Dang-Vu et al., 2010; see also Fernandez & Lüthi, 2020) and memory (Clemens et al., 2005; Cox et al., 2012; Mölle et al., 2011; see also Kumral et al., 2022 for a recent meta-analysis of spindles and memory).”
BackgroundHippocampal Contributions to Declarative Memory Consolidation During Sleep
Antony, J. W., & Paller, K. A. (2017) · Springer eBooks · doi:10.1007/978-3-319-50406-3_9 · Cited by 27
“2007) and spindles (de Gennaro and Ferrara 2003) occur more frequently during lighter NREM stages, though this could be due to analysis issues with respect to identifying spindles by eye when they are superimposed on predominant slow oscillations (Cox et al. 2012).”
BackgroundAutonomic/central coupling benefits working memory in healthy young adults
Chen, P., Whitehurst, L. N., Naji, M., & Mednick, S. C. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107267 · Cited by 26
Denis, 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 25
“It is notable that no associations between SWS activity and memory were found in the control group, given other research showing SWS- related benefits for both neutral and emotional episodic memory in non- stressed participants (Ackermann & Rasch, 2014; Cox et al., 2012; Denis, Mylonas, et al., 2020; Groch et al., 201…”
ResultSemantic congruence reverses effects of sleep restriction on associative encoding
Alberca-Reina, E., Cantero, J. L., & Atienza, M. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.01.012 · Cited by 22
Takeuchi, S., Murai, R., Shimazu, H., Isomura, Y., Mima, T., & Tsujimoto, T. (2016) · SLEEP · doi:10.5665/sleep.6100 · Cited by 22
Lateralised sleep spindles relate to false memory generation
Shaw, J. J., & Padraic Monaghan, B. (2017) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2017.11.002 · Cited by 24
Altered sleep spindles and slow waves during space shuttle missions
Koller, D. P., Kasanin, V., Flynn‐Evans, E. E., Sullivan, J. P., Dijk, D., Czeisler, C. A., & Barger, L. K. (2021) · npj Microgravity · doi:10.1038/s41526-021-00177-1 · Cited by 19
Sleep loss disrupts the neural signature of successful learning
Guttesen, A. Á. V., Gaskell, M. G., Madden, E. V., Appleby, G., Cross, Z. R., & Cairney, S. A. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac159 · Cited by 24
“Our pre-registered upper bound was 120 Hz, but because our sampling rate was 200 Hz the upper bound was above the Nyquist frequency and had to be lowered.”
InfluentialSleep: The Tip of the Iceberg in the Bidirectional Link Between Alzheimer's Disease and Epilepsy
Szabo, A. B., Cretin, B., Gérard, F., Curot, J., Barbeau, E. J., Pariente, J., Dahan, L., & Valton, L. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.836292 · Cited by 21
Shared and unique features of mammalian sleep spindles – insights from new and old animal models
Iotchev, I. B., & Enikö Kubinyi, B. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12688 · Cited by 18
“In light of this, human findings showing that the precise stage of NREM sleep was relevant to associations between spindle occurrence and recall performance (Cox et al., 2012) present a specific argument for studies of our closest phylogenetic relatives.”
BackgroundParker, J. L., Melaku, Y. A., D'Rozario, A. L., Wittert, G., Martin, S., CATCHESIDE, P. G., Lechat, B., Teare, A. J., Adams, R., Appleton, S., et al. (2021) · SLEEP · doi:10.1093/sleep/zsab282 · Cited by 19
Time, Not Sleep, Unbinds Contexts from Item Memory
Cox, R., Tijdens, R. R., Meeter, M., Sweegers, C. C. G., & Talamini, L. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088307 · Cited by 22
“oscillations [24–26].”
Self-citationSleep Promotes Phonological Learning in Children Across Language and Autism Spectra
Knowland, V. C. P., Fletcher, F. E., Henderson, L. M., Walker, S., Norbury, C., & Gaskell, M. G. (2019) · Journal of Speech Language and Hearing Research · doi:10.1044/2019_jslhr-s-19-0098 · Cited by 23
Metadata
- Authors
- Cox, R., Hofman, W. F., & Talamini, L. M.
- Affiliations
- University of Amsterdam (NL)
- ORCID
- Cox, Roy
- Venue
- Learning & Memory
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2012-06-14
- Volume
- 19
- Issue
- 7
- Pages
- 264-267
- ISSN
- 1072-0502 (ISSN-L)
- 1549-5485
- OpenAlex
- W2125579095
- Cited by
- 163
- References
- 31
- Citations by year
- 2026: 10 · 2025: 6 · 2024: 6 · 2023: 10 · 2022: 14 · 2021: 15 · 2020: 20 · 2019: 18 · 2018: 11 · 2017: 11 · 2016: 10 · 2015: 11 · 2014: 12 · 2013: 9
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Learning & Memory (publishedVersion)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- UvA-DARE (University of Amsterdam) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (452-08-013)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- sleep spindles, slow oscillations, memory consolidation, sleep-dependent memory consolidation, slow-wave sleep, light sleep, spindle density
- MeSH terms
- Adolescent, Adult, Electroencephalography, Female, Humans, Male, Neuropsychological Tests, Surveys and Questionnaires, Retention, Psychology, Sleep, Sleep Deprivation, Sleep Stages, Time Factors, Linear Models, Polysomnography, Young Adult, Brain Waves
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