Involvement of spindles in memory consolidation is slow wave sleep-specific
Open accessAbstract
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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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 [235]
The Abstract reports a strong positive correlation between spindle density during slow-wave sleep and declarative-memory retention. But the study measured retention across a nap, not overnight, and found no significant correlation for spindle density during light sleep or for spindle-frequency power. It therefore does not support the claim that indicators of spindle expression consistently correlated with overnight retention. (LLM, conf=0.88)
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Cites
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BackgroundSlow Wave Sleep Induced by GABA Agonist Tiagabine Fails to Benefit Memory Consolidation
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“The latter view is fed by several studies implicating SWS in the ‘replay’ and consolidation of memory representations [24,54,55].”
BackgroundSelf-citationSpindle Oscillations in Sleep Disorders: A Systematic Review
Weiner, O. M., & Dang‐Vu, T. T. (2016) · Neural Plasticity · doi:10.1155/2016/7328725 · Cited by 74 · see citing works
“Similarly, Cox and colleagues [31] demonstrated that greater spindle density specifically during slow-wave sleep was positively correlated with declarative memory performance.”
BackgroundTravelling spindles create necessary conditions for spike-timing-dependent plasticity in humans
Dickey, C. W., Sargsyan, A., Madsen, J. R., Eskandar, E. N., Cash, S. S., & Halgren, E. (2021) · Nature Communications · doi:10.1038/s41467-021-21298-x · Cited by 70 · see citing works
Large-scale structure and individual fingerprints of locally coupled sleep oscillations
Cox, R., Mylonas, D., Manoach, D. S., & Stickgold, R. (2018) · SLEEP · doi:10.1093/sleep/zsy175 · Cited by 67 · see citing works
Self-citationA deep learning approach for real-time detection of sleep spindles
Kulkarni, P. M., Xiao, Z., Robinson, E. J., Jami, A. S., Zhang, J., Zhou, H., Henin, S. E., Liu, A. A., Osorio, R. S., Wang, J., et al. (2019) · Journal of Neural Engineering · doi:10.1088/1741-2552/ab0933 · Cited by 66 · see citing works
The Contribution of Thalamocortical Core and Matrix Pathways to Sleep Spindles
Piantoni, G., Halgren, E., & Cash, S. S. (2016) · Neural Plasticity · doi:10.1155/2016/3024342 · Cited by 64 · see citing works
Closed-loop auditory stimulation of sleep slow oscillations: Basic principles and best practices
Esfahani, M. J., Farboud, S., Ngo, H.-V. V., Schneider, J., Weber, F. D., Talamini, L. M., & Dresler, M. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105379 · Cited by 65 · see citing works
“This further emphasizes the important relationship between SOs and sleep spindles (Cox et al., 2012; Ngo et al., 2013; Ruch et al., 2012; Timofeev et al., 2002).”
Self-citationAdamczyk, M., Genzel, L., Dresler, M., Steiger, A., & Frieß, E. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00624 · Cited by 62 · see citing works
Cortical source localization of sleep-stage specific oscillatory activity
Brancaccio, A., Tabarelli, D., Bigica, M., & Baldauf, D. (2020) · Scientific Reports · doi:10.1038/s41598-020-63933-5 · Cited by 60 · see citing works
Monosynaptic Hippocampal-Prefrontal Projections Contribute to Spatial Memory Consolidation in Mice
Binder, S., Mölle, M., Lippert, M., Bruder, R., Aksamaz, S., Ohl, F. W., Wiegert, J. S., & Marshall, L. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2158-18.2019 · Cited by 55 · see citing works
“Successful memory consolidation has furthermore been linked to enhanced post-learning spindle activity (Gais et al., 2002; Schabus et al., 2004; Clemens et al., 2005; Cox et al., 2012).”
BackgroundDenis, D., Schapiro, A. C., Poskanzer, C., Bursal, V., Charron, L. S., Morgan, A., & Stickgold, R. (2020) · Learning & Memory · doi:10.1101/lm.051383.120 · Cited by 54 · see citing works
“This builds on other evidence showing that sleep spindles facilitate memory consolidation (Schabus et al. 2004; Cox et al. 2012), Furthermore, memory replay in the BA Figure 3.”
BackgroundBrain Rhythms During Sleep and Memory Consolidation: Neurobiological Insights
Marshall, L., Cross, N. E., Binder, S., & Dang‐Vu, T. T. (2019) · Physiology · doi:10.1152/physiol.00004.2019 · Cited by 47 · see citing works
The impact of frequent napping and nap practice on sleep-dependent memory in humans
McDevitt, E. A., Sattari, N. S., Duggan, K. A., Cellini, N., Whitehurst, L. N., Perera, C., Reihanabad, N., Granados, S., Hernandez, L. T., & Mednick, S. C. (2018) · Scientific Reports · doi:10.1038/s41598-018-33209-0 · Cited by 50 · see citing works
The Common Effects of Sleep Deprivation on Human Long-Term Memory and Cognitive Control Processes
Kim, T., Kim, S., Kang, J., Kwon, M., & Lee, S. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.883848 · Cited by 54 · see citing works
Insights into sleep's role for insight: Studies with the number reduction task
Verleger, R., Rose, M. R., Wagner, U., Yordanova, J., & Kolev, V. (2013) · Advances in Cognitive Psychology · doi:10.5709/acp-0143-8 · Cited by 48 · see citing works
Nap sleep preserves associative but not item memory performance.
Studte, S., Bridger, E. K., & Mecklinger, A. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.02.012 · Cited by 39 · see citing works
“This finding is consistent with studies showing that short periods of sleep are sufficient to induce a measurable benefit in declarative memory (Cox et al., 2012; Saletin et al., 2011; Schmidt et al., 2006; Tucker et al., 2006).”
InfluentialGeneralization from episodic memories across time: A route for semantic knowledge acquisition
Sweegers, C. C. G., & Talamini, L. M. (2014) · Cortex · doi:10.1016/j.cortex.2014.07.006 · Cited by 45 · see citing works
Self-citationCosta, M. S., Weigenand, A., Ngo, H.-V. V., Marshall, L., Jan Born, A., Martinetz, T., & Claussen, J. C. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005022 · Cited by 45 · see citing works
Remembering to Forget: A Dual Role for Sleep Oscillations in Memory Consolidation and Forgetting
Langille, J. J. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00071 · Cited by 44 · see citing works
Farthouat, J., Gilson, M., & Peigneux, P. (2017) · Sleep Spindles & Cortical Up States · doi:10.1556/2053.1.2016.002 · Cited by 41 · see citing works
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Malerba, P., Whitehurst, L. N., Simons, S. B., & Mednick, S. C. (2018) · SLEEP · doi:10.1093/sleep/zsy197 · Cited by 39 · see citing works
Age-related differences and sexual dimorphism in canine sleep spindles
Iotchev, I. B., Kis, A., Turcsán, B., de Lara, D. R. T. F., Reicher, V., & Enikö Kubinyi, B. (2019) · Scientific Reports · doi:10.1038/s41598-019-46434-y · Cited by 39 · see citing works
Sex Hormones, Sleep, and Memory: Interrelationships Across the Adult Female Lifespan
Harrington, Y. A., Parisi, J. M., Duan, D., Rojo‐Wissar, D. M., Holingue, C., & Spira, A. P. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.800278 · Cited by 38 · see citing works
Koo, P. C., Mölle, M., & Marshall, L. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13877 · Cited by 37 · see citing works
“More importantly, however, several studies indicate that the phase-dependent concurrence of spindles within the slow oscillation appears to be a closer correlate of consolidation than the power of spindle or slow oscillations per se (Cox et al., 2012; Ngo et al., 2013; Weigenand et al., 2016), and it has recently been…”
BackgroundLong term effects of cueing procedural memory reactivation during NREM sleep
Rakowska, M., Abdellahi, M. E. A., Bagrowska, P., Navarrete, M., & Lewis, P. A. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118573 · Cited by 38 · see citing works
Berkers, R. M. W. J., Ekman, M., van Dongen, E. V., Takashima, A., Barth, M., Paller, K. A., & Fernández, G. (2018) · Scientific Reports · doi:10.1038/s41598-018-35287-6 · Cited by 37 · see citing works
A daytime nap restores hippocampal function and improves declarative learning
Ong, J. L., Lau, T., Lee, X. K., van Rijn, E., & Chee, M. W. L. (2020) · SLEEP · doi:10.1093/sleep/zsaa058 · Cited by 35 · see citing works
“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.”
BackgroundCunningham, T. J., Stickgold, R., & Kensinger, E. A. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.910317 · Cited by 34 · see citing works
Studte, S., Bridger, E. K., & Mecklinger, A. (2017) · Brain and Language · doi:10.1016/j.bandl.2016.03.003 · Cited by 35 · see citing works
“Sleep spindles were detected using an adaption of the algorithm originally provided by Ferrarelli et al., 2007 (see also Cox et al., 2012, Studte at al., 2015).”
Yordanova, J., Kirov, R., Verleger, R., & Kolev, V. (2017) · Scientific Reports · doi:10.1038/s41598-017-15195-x · Cited by 33 · see citing works
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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
Yordanova, J., Kolev, V., Bruns, E., Kirov, R., & Verleger, R. (2017) · SLEEP · doi:10.1093/sleep/zsx151 · Cited by 32 · see citing works
“Also, offline transformation of sequence representations from implicit to explicit was expected to correlate with sleep spindles during SWS.9,27 Finally, if increased awareness was determined by individual or trait-like characteristics,20 some participants might have both more explicit knowledge and more spindles, irr…”
BackgroundREM theta activity predicts re-experiencing symptoms after exposure to a traumatic film
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 33 · see citing works
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 · see citing works
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 30 · see citing works
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 28 · see citing works
“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 · see citing works
Targeted memory reactivation to augment treatment in post-traumatic stress disorder.
der Heijden, A. V. D. V., van der Werf, Y., van den Heuvel, O. A., Talamini, L. M., & van Marle, H. V. (2024) · Current Biology · doi:10.1016/j.cub.2024.07.019 · Cited by 20 · see citing works
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 27 · see citing works
Valencia, M., Artieda, J., Bolam, J. P., & Mena‐Segovia, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067540 · Cited by 26 · see citing works
“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 23 · see citing works
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 · see citing works
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 24 · see citing works
Farthouat, J., Atas, A., Wens, V., Tiège, X. D., & Peigneux, P. (2018) · Scientific Reports · doi:10.1038/s41598-018-30105-5 · Cited by 23 · see citing works
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 · see citing works
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., & Enikö Kubinyi, B. (2020) · Scientific Reports · doi:10.1038/s41598-020-80417-8 · Cited by 23 · see citing works
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 24 · see citing works
“…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 23 · see citing works
“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 · see citing works
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 23 · see citing works
“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 21 · see citing works
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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 22 · see citing works
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 · see citing works
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 21 · see citing works
“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 19 · see citing works
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 · see citing works
“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 · see citing works
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 18 · see citing works
“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 19 · see citing works
- 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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