The DOI matches its Crossref record; 71 of the 71 references it cites were found in a registry or an index.
The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats
Abstract
The mechanisms underlying off-line consolidation of memory during sleep are elusive. Learning of hippocampus-dependent tasks increases neocortical slow oscillation synchrony, and thalamocortical spindle and hippocampal ripple activity during subsequent non-rapid eye movement sleep. Slow oscillations representing an oscillation between global neocortical states of increased (up-state) and decreased (down-state) neuronal firing temporally group thalamic spindle and hippocampal ripple activity, which both occur preferentially during slow oscillation up-states. Here we examined whether slow oscillations also group learning-induced increases in spindle and ripple activity, thereby providing time-frames of facilitated hippocampus-to-neocortical information transfer underlying the conversion of temporary into long-term memories. Learning (word-pairs in humans, odor-reward associations in rats) increased slow oscillation up-states and, in humans, shaped the timing of down-states. Slow oscillations grouped spindle and rat ripple activity into up-states under basal conditions. Prior learning produced in humans an increase in spindle activity focused on slow oscillation up-states. In rats, learning induced a distinct increase in spindle and ripple activity that was not synchronized to up-states. Event-correlation histograms indicated an increase in spindle activity with the occurrence of ripples. This increase was prolonged after learning, suggesting a direct temporal tuning between rip…
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“In humans, intense learning of declarative memories (word pairs) enhanced amplitudes of the slow oscillation up-states as well as coherence in the SWA frequency band during succeeding SWS (829, 831).”
From About Sleep's Role in Memory (2013) · cites this paper as [829]
In the citing paper
“Also, slopes of the down-to-up state of the slow oscillations were steeper after learning.”
From About Sleep's Role in Memory (2013) · cites this paper as [829]
In the citing paper
“At the neocortical level, the slow oscillation in terms of EEG rhythms strongly modulates the amplitude of faster beta and gamma frequencies which is reduced to a minimum during the hyperpolarizing down-phase of the slow oscillation (224,240,828,829).”
From About Sleep's Role in Memory (2013) · cites this paper as [829]
In the citing paper
“In humans, intense learning of vocabulary did not only increase the slope of the down-to-up state transition of the slow oscillation during succeeding non-REM sleep, but concurrently enhanced fast spindle activity, with this increase concentrating on the up-states of the slow oscillation, whereas no changes were observed in hyperpolarizing down-states (826, 829).”
From About Sleep's Role in Memory (2013) · cites this paper as [829]
In the citing paper
“Generation of spindles in the thalamus and generation of SW-Rs in the hippocampus are distinctly suppressed during the down-phase of the slow oscillation, and this is followed by a rebound in spindle and SW-R activity during the succeeding depolarizing up-state (66, 215, 597, 829 -832, 925, 1088).”
From About Sleep's Role in Memory (2013) · cites this paper as [829]
Citations
Cites
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256
Buzsáki, G. (2006) · doi:10.1093/acprof:oso/9780195301069.001.0001 · Cited by 4,873
Sleep function and synaptic homeostasis
Tononi, G., & Cirelli, C. (2006) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2005.05.002 · Cited by 2,151
Sleep-dependent memory consolidation
Stickgold, R. (2005) · Nature · doi:10.1038/nature04286 · Cited by 1,857
Huber, R., Felice Ghilardi, M., Massimini, M., & Tononi, G. (2004) · Nature · doi:10.1038/nature02663 · Cited by 1,854
Boosting slow oscillations during sleep potentiates memory
Marshall, L., Helgadóttir, H., Mölle, M., & Born, J. (2006) · Nature · doi:10.1038/nature05278 · Cited by 1,792
Self-citationTwo-stage model of memory trace formation: A role for “noisy” brain states
Buzsáki, G. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90423-5 · Cited by 1,709
Coordinated memory replay in the visual cortex and hippocampus during sleep
Ji, D., & Wilson, M. A. (2007) · Nature Neuroscience · doi:10.1038/nn1825 · Cited by 1,669
Grouping of brain rhythms in corticothalamic systems
Steriade, M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.029 · Cited by 1,296
Forward and reverse hippocampal place-cell sequences during ripples
Diba, K., & Buzsáki, G. (2007) · Nature Neuroscience · doi:10.1038/nn1961 · Cited by 1,205
Odor cues during slow-wave sleep prompt declarative memory consolidation
Rasch, B., Büchel, C., Gais, S., & Born, J. (2007) · Science · doi:10.1126/science.1138581 · Cited by 1,181
Self-citationCoordinated interactions between hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep
Siapas, A. G., & Wilson, M. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80629-7 · Cited by 1,052
The Hippocampo-Neocortical Dialogue
Buzsáki, G. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.2.81 · Cited by 938
Replay and Time Compression of Recurring Spike Sequences in the Hippocampus
Nádasdy, Z., Hirase, H., Czurkó, A., Csicsvari, J., & Buzsáki, G. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-21-09497.1999 · Cited by 932 · cited 1×
“In the hippocampal circuitry, neuronal replay of recently encoded memories occurs in conjunction with ripples typically forming sharp wave–ripple complexes (Nadasdy et al., 1999; Csicsvari et al., 2000; Diba & Buzsaki, 2007).”
BackgroundCommunication between neocortex and hippocampus during sleep in rodents
Sirota, A., Csicsvari, J., Buhl, D., & Buzsáki, G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437938100 · Cited by 930
Learning-dependent increases in sleep spindle density
Gais, S., Mölle, M., Helms, K., & Born, J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06830.2002 · Cited by 859
Self-citationGoldman‐Rakic, P. S., Selemon, L. D., & Schwartz, M. L. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90166-0 · Cited by 782
Are spatial memories strengthened in the human hippocampus during slow wave sleep?
Peigneux, P., Laureys, S., Fuchs, S., Collette, F., Perrin, F., Reggers, J., Phillips, C., Degueldre, C., Del Fiore, G., Aerts, J., et al. (2004) · Neuron · doi:10.1016/j.neuron.2004.10.007 · Cited by 766
Significance Testing of Difference Potentials
Guthrie, D., & Buchwald, J. S. (1991) · Psychophysiology · doi:10.1111/j.1469-8986.1991.tb00417.x · Cited by 751
Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships
Contreras, D., & Steriade, M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00604.1995 · Cited by 700
The contribution of sleep to hippocampus-dependent memory consolidation
Marshall, L., & Born, J. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.09.001 · Cited by 667
Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation
Steriade, M., Amzica, F., & Contreras, D. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-01-00392.1996 · Cited by 654
The Effects of Coffee and Napping on Nighttime Highway Driving
Philip, P., Taillard, J., Moore, N. D., Delord, S., Valtat, C., Sagaspe, P., & Bioulac, B. H. (2006) · Annals of Internal Medicine · doi:10.7326/0003-4819-144-11-200606060-00004 · Cited by 652
A manual of Standardized Terminology
Rechtschaffen, A. (1968) · Medical Entomology and Zoology · Cited by 632
Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep
Mölle, M., Marshall, L., Gais, S., & Born, J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10941.2002 · Cited by 617
Self-citationFast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep
Euston, D. R., Tatsuno, M., & McNaughton, B. L. (2007) · Science · doi:10.1126/science.1148979 · Cited by 586
Memory consolidation during sleep: a neurophysiological perspective
Buzsáki, G. (1998) · Journal of Sleep Research · doi:10.1046/j.1365-2869.7.s1.3.x · Cited by 578
Destexhe, A., Contreras, D., & Steriade, M. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04595.1999 · Cited by 573
Sleep Spindles and Their Significance for Declarative Memory Consolidation
Schabus, M., Gruber, G., Parapatics, S., Sauter, C., Klösch, G., Anderer, P., Klimesch, W., Saletu, B., & Zeitlhofer, J. (2004) · Sleep · doi:10.1093/sleep/27.7.1479 · Cited by 560
Takashima, A., Petersson, K. M., Rutters, F., Tendolkar, I., Jensen, O., Zwarts, M. J., McNaughton, B. L., & Fernández, G. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507774103 · Cited by 557
Born, J., Rasch, B., & Gais, S. (2006) · The Neuroscientist · doi:10.1177/1073858406292647 · Cited by 557
Self-citationEnsemble Patterns of Hippocampal CA3-CA1 Neurons during Sharp Wave–Associated Population Events
Csicsvari, J., Hirase, H., Mamiya, A., & Buzsáki, G. (2000) · Neuron · doi:10.1016/s0896-6273(00)00135-5 · Cited by 523
Isomura, Y., Sirota, A., Özen, S., Montgomery, S., Mizuseki, K., Henze, D. A., & Buzsáki, G. (2006) · Neuron · doi:10.1016/j.neuron.2006.10.023 · Cited by 500
Why do we sleep?11Published on the World Wide Web on 7 November 2000.
Sejnowski, T. J., & Destexhe, A. (2000) · Brain Research · doi:10.1016/s0006-8993(00)03007-9 · Cited by 489
Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer
Jensen, O. B., & Lisman, J. E. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.12.001 · Cited by 467
Model of Thalamocortical Slow-Wave Sleep Oscillations and Transitions to Activated States
Bazhenov, M., Timofeev, I., Steriade, M., & B, T. J. S. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-19-08691.2002 · Cited by 461
Coordinated Reactivation of Distributed Memory Traces in Primate Neocortex
Hoffman, K. L., & McNaughton, B. L. (2002) · Science · doi:10.1126/science.1073538 · Cited by 420
Pattern-Specific Associative Long-Term Potentiation Induced by a Sleep Spindle-Related Spike Train
Rosanova, M., & Ulrich, D. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2149-05.2005 · Cited by 413
Sleep transforms the cerebral trace of declarative memories
Gais, S., Albouy, G., Boly, M., Dang-Vu, T. T., Darsaud, A., Desseilles, M., Rauchs, G., Schabus, M., Sterpenich, V., Vandewalle, G., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705454104 · Cited by 412
Self-citationOvernight verbal memory retention correlates with the number of sleep spindles
Clemens, Z., Fabó, D., & Halász, P. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.01.011 · Cited by 405
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
Self-citationAre corticothalamic ‘up’ states fragments of wakefulness?
Destexhe, A., Hughes, S. W., Rudolph, M., & Crunelli, V. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.04.006 · Cited by 355
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
Hippocampal Sharp Wave-Ripples Linked to Slow Oscillations in Rat Slow-Wave Sleep
Mölle, M., Yeshenko, O., Marshall, L., Sara, S. J., & Born, J. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00014.2006 · Cited by 337
Self-citationCoherent oscillations and short-term plasticity in corticothalamic networks
Steriade, M. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01407-1 · Cited by 321
Hippocampal sharp wave bursts coincide with neocortical “up-state” transitions
Battaglia, F. P., Sutherland, G. R., & McNaughton, B. L. (2004) · Learning & Memory · doi:10.1101/lm.73504 · Cited by 310 · cited 2×
“…of ripples, like that of spindles, is grouped by the slow oscillation, with there being minimum ripple activity during the hyperpolarization down-state in rats, mice, and humans (Sirota et al., 2003; Battaglia et al., 2004; Isomura et al., 2006; Mölle et al., 2006; Clemens et al., 2007).”
BackgroundVolgushev, M., Chauvette, S., Mukovski, M., & Timofeev, I. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0279-06.2006 · Cited by 289
Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning
Eschenko, O., Ramadan, W., Mölle, M., Born, J., & Sara, S. J. (2008) · Learning & Memory · doi:10.1101/lm.726008 · Cited by 277
Self-citationRibeiro, S., Gervasoni, D., Soares, E. S., Zhou, Y., Lin, S.-C., Pantoja, J., Lavine, M., & Nicolelis, M. A. L. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020024 · Cited by 272
Interaction between neocortical and hippocampal networks via slow oscillations
Sirota, A., & Buzsáki, G. (2005) · Thalamus and Related Systems · doi:10.1017/s1472928807000258 · Cited by 270
Elevated Sleep Spindle Density after Learning or after Retrieval in Rats
Eschenko, O., Mölle, M., Jan Born, A., & Sara, S. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3175-06.2006 · Cited by 268
Self-citationSchabus, 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
Molecular recognition and olfactory processing in the mammalian olfactory system
Mori, K., & Yoshihara, Y. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(94)00058-p · Cited by 247
Cellular Mechanisms of the Slow (<1 Hz) Oscillation in Thalamocortical Neurons In Vitro
Hughes, S. W., Cope, D. W., Blethyn, K. L., & Crunelli, V. (2002) · Neuron · doi:10.1016/s0896-6273(02)00623-2 · Cited by 243
Maintaining memories by reactivation
Rasch, B., & Born, J. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.11.007 · Cited by 240
Wolansky, T., Clement, E., Peters, S. R., Palczak, M. A., & Dickson, C. T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5594-05.2006 · Cited by 236
Encoding Difficulty Promotes Postlearning Changes in Sleep Spindle Activity during Napping
Schmidt, C., Peigneux, P., Muto, V., Schenkel, M., Knoblauch, V., Münch, M. Y., de Quervain, D. J. ‐., Wirz‐Justice, A., & Cajochen, C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2464-06.2006 · Cited by 230
Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations
Mölle, M., Marshall, L., Gais, S., & Born, J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402820101 · Cited by 222
Self-citationBidirectional Control of Quantal Size by Synaptic Activity in the Hippocampus
Oliet, S. H. R., Malenka, R. C., & Nicoll, R. A. (1996) · Science · doi:10.1126/science.271.5253.1294 · Cited by 209 · cited 2×
“during the down-phase is selectively enhanced at synapses previously activated during learning (Eliot et al., 1994; Oliet et al., 1996; Bao et al., 1998; Hoffman & McNaughton, 2002), this could explain an”
BackgroundNeuronal metabolism governs cortical network response state
Cunningham, M. O., Pervouchine, D. D., Racca, C., Kopell, N., Davies, C. H., Jones, R. S. G., Traub, R. D., & Whittington, M. A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600604103 · Cited by 177
Contreras, D., Alain Destexhe, A., & Steriade, M. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.1.335 · Cited by 153
Tronel, S., & Sara, S. J. (2002) · Learning & Memory · doi:10.1101/lm.47802 · Cited by 147
Self-citationHumans as an Animal Model for Systems-Level Organization of Olfaction
Zelano, C., & Sobel, N. (2005) · Neuron · doi:10.1016/j.neuron.2005.10.009 · Cited by 120
EEG theta synchronization conjoined with alpha desynchronization indicate intentional encoding
Mölle, M., Marshall, L., Fehm, H. L., & Born, J. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01921.x · Cited by 114
Self-citationBao, J., Kandel, E. R., & Hawkins, R. D. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00458.1998 · Cited by 109
Eliot, L., Kandel, E., & Hawkins, R. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-05-03280.1994 · Cited by 76
Tronel, S., & Sara, S. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05472.2003 · Cited by 71
Self-citationWerk, C. M., Harbour, V. L., & Chapman, C. A. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.12.020 · Cited by 60
Memory reactivation and consolidation during sleep: from cellular mechanisms to human performance
Pennartz, C. M. A., Uylings, H. B. M., Barnes, C. A., & McNaughton, B. L. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)38076-2 · Cited by 59
EEG Power Densities (0.5–20 Hz) in Different Sleep–Wake Stages in Rats
Bjorvatn, B., Fagerland, S., & Ursin, R. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00460-5 · Cited by 59
Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways.
Lavenex (2000) · Pure Amsterdam UMC · doi:10.1002/1098-1063(2000)10:4 · Cited by 1
Cited by
Sorted by citations
Diekelmann, S., & Born, J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2762 · Cited by 3,760
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783
Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759
Control of sleep and wakefulness
Brown, R. E., Basheer, R., McKenna, J. T., Strecker, R. E., & McCarley, R. W. (2012) · Physiological Reviews · doi:10.1152/physrev.00032.2011 · Cited by 1,477
Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms
Buzsáki, G., Logothetis, N., & Singer, W. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.002 · Cited by 886
Metadata
- Authors
- Mölle, M., Eschenko, O., Gais, S., Sara, S. J., & Born, J.
- Affiliations
- University of Lübeck (DE)
- Centre National de la Recherche Scientifique (FR)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2009-03
- Volume
- 29
- Issue
- 5
- Pages
- 1071-1081
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2163770201
- Cited by
- 322
- References
- 71
- Citations by year
- 2026: 12 · 2025: 16 · 2024: 18 · 2023: 17 · 2022: 17 · 2021: 13 · 2020: 24 · 2019: 46 · 2018: 18 · 2017: 20 · 2016: 19 · 2015: 16 · 2014: 17 · 2013: 22 · 2012: 16
- FWCI
- 7.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- 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 slow oscillations, sleep spindles, hippocampal ripples, memory consolidation, hippocampus-dependent learning, word pair learning, NREM sleep
- MeSH terms
- Adult, Animals, Association Learning, Cerebral Cortex, Electroencephalography, Evoked Potentials, Female, Humans, Male, Neuropsychological Tests, Odorants, Periodicity, Reward, Sleep, Spectrum Analysis, Statistics as Topic, Rats, Sprague-Dawley, Rats, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review