Pattern-Specific Associative Long-Term Potentiation Induced by a Sleep Spindle-Related Spike Train
Open accessAbstract
Spindles are non-rapid eye movement (non-REM) sleep EEG rhythms (7-14 Hz) that occur independently or in association with slow oscillations (0.6-0.8 Hz). Despite their proposed function in learning and memory, their role in synaptic plasticity is essentially unknown. We studied the ability of a neuronal firing pattern underlying spindles in vivo to induce synaptic plasticity in neocortical pyramidal cells in vitro. A spindle stimulation pattern (SSP) was extracted from a slow oscillation upstate that was recorded in a cat anesthetized with ketamine-xylazine, which is known to induce a sleep-like state. To mimic the recurrence of spindles grouped by the slow oscillation, the SSP was repeated every 1.5 s (0.6 Hz). Whole-cell patch-clamp recordings were obtained from layer V pyramidal cells of rat somatosensory cortex with infrared videomicroscopy, and composite EPSPs were evoked within layers II-III. Trains of EPSPs and action potentials simultaneously triggered by the SSP induced an NMDA receptor-dependent short-term potentiation (STP) and an L-type Ca2+ channel-dependent long-term potentiation (LTP). The number of spindle sequences affected the amount of STP-LTP. In contrast, spindle trains of EPSPs alone led to long-term depression. LTP was not consistently induced by a regular firing pattern, a mirrored SSP, or a randomized SSP; however, a synthetic spindle pattern consisting of repetitive spike bursts at 10 Hz reliably induced STP-LTP. Our results show that spindle-associated spike discharges are efficient in modifying excitatory neocortical synapses according to a Hebbian rule. This is in support of a role for sleep spindles in memory consolidation.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Repeated spindle-associated spike discharges efficiently triggered LTP in neocortical synapses in in vitro models.
“Repeated spindle-associated spike discharges efficiently triggered LTP in neocortical synapses in in vitro models (1012, 1197).”
From About Sleep's Role in Memory (2013) · cites this paper as [1012]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Huber, R., Felice Ghilardi, M., Massimini, M., & Tononi, G. (2004) · Nature · doi:10.1038/nature02663 · Cited by 1,854 · see citing works
The sleep slow oscillation as a traveling wave
Massimini, M., Huber, R., Ferrarelli, F., Hill, S., & Tononi, G. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1318-04.2004 · Cited by 1,221 · see citing works
Sleep-Dependent Learning and Memory Consolidation
Walker, M. P., & Stickgold, R. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.031 · Cited by 1,113 · cited 1× · see citing works
“An increasing amount of experimental evidence suggests that sleep is important for learning, memory consolidation, and development (Frank et al., 2001; Hobson and Pace-Schott, 2002; Walker and Stickgold, 2004).”
Destexhe, A., Contreras, D., & Steriade, M. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04595.1999 · Cited by 573 · see citing works
Sleep Enhances Plasticity in the Developing Visual Cortex
Frank, M. G., Issa, N. P., & Stryker, M. P. (2001) · Neuron · doi:10.1016/s0896-6273(01)00279-3 · Cited by 523 · see citing works
The restorative effect of naps on perceptual deterioration
Mednick, S. C., Nakayama, K., Cantero, J. L., Atienza, M., Levin, A. A., Pathak, N., & Stickgold, R. (2002) · Nature Neuroscience · doi:10.1038/nn864 · Cited by 360 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Tononi, G., & Cirelli, C. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.025 · Cited by 2,356 · see citing works
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 · see citing works
Mechanisms of systems memory consolidation during sleep
Klinzing, J. G., Niethard, N., & Born, J. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0467-3 · Cited by 1,176 · 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
The Consolidation and Transformation of Memory
Dudai, Y., Karni, A., & Born, J. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.004 · Cited by 741 · see citing works
Hippocampo-cortical coupling mediates memory consolidation during sleep
Maingret, N., Girardeau, G., Todorova, R., Goutierre, M., & Zugaro, M. (2016) · Nature Neuroscience · doi:10.1038/nn.4304 · Cited by 667 · see citing works
Mather, M., Clewett, D., Sakaki, M., & Harley, C. W. (2016) · Behavioral and Brain Sciences · doi:10.1017/s0140525x15000667 · Cited by 695 · see citing works
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 · see citing works
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644 · see citing works
Latchoumane, C.-F. V., Ngo, H.-V. V., Born, J., & Shin, H.-S. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.025 · Cited by 561 · 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
Old brains come uncoupled in sleep: slow wave-spindle synchrony, brain atrophy, and forgetting
Helfrich, R. F., Mander, B. A., Jagust, W. J., Knight, R. T., & Walker, M. P. (2018) · Neuron · doi:10.1016/j.neuron.2017.11.020 · Cited by 497 · 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 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
Memory consolidation is linked to spindle-mediated information processing during sleep
Cairney, S. A., Guttesen, A. Á. V., El Marj, N., & Staresina, B. P. (2018) · Current Biology · doi:10.1016/j.cub.2018.01.087 · Cited by 289 · 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
Cortical circuit activity underlying sleep slow oscillations and spindles
Niethard, N., Ngo, H.-V. V., Ehrlich, I., & Born, J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1805517115 · Cited by 245 · 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
Fine‐tuned coupling between human parahippocampal ripples and sleep spindles
Clemens, Z., Mölle, M., Erőss, L., Jakus, R., Rásonyi, G., Halász, P., & Born, J. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07505.x · Cited by 214 · see citing works
The Ca <sub>V</sub> 3.3 calcium channel is the major sleep spindle pacemaker in thalamus
Astori, S., Wimmer, R. D., Prosser, H. M., Corti, C., Corsi, M., Liaudet, N., Volterra, A., Franken, P., Adelman, J. P., & Lüthi, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105115108 · Cited by 213 · see citing works
Fast and slow spindle involvement in the consolidation of a new motor sequence
Barakat, M., Doyon, J., Debas, K., Vandewalle, G., Morin, A., Poirier, G., Martin, N., Lafortune, M., Karni, A., Ungerleider, L. G., et al. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.10.019 · Cited by 203 · see citing works
Sleep spindles and learning potential.
Fogel, S. M., Nader, R., Cote, K. A., & Smith, C. T. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.1.1 · Cited by 188 · see citing works
Form and function of sleep spindles across the lifespan
Clawson, B. C., Durkin, J., & Aton, S. J. (2016) · Neural Plasticity · doi:10.1155/2016/6936381 · Cited by 178 · 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
Schreiner, T., Petzka, M., Staudigl, T., & Staresina, B. P. (2021) · Nature Communications · doi:10.1038/s41467-021-23520-2 · Cited by 161 · see citing works
Generalization of word meanings during infant sleep
Friedrich, M., Wilhelm, I., Born, J., & Friederici, A. D. (2015) · Nature Communications · doi:10.1038/ncomms7004 · Cited by 176 · see citing works
Sleep and memory in mammals, birds and invertebrates
Vorster, A. P., & Born, J. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.09.020 · Cited by 169 · see citing works
Interindividual 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
Involvement of spindles in memory consolidation is slow wave sleep-specific
Cox, R., Hofman, W. F., & Talamini, L. M. (2012) · Learning & Memory · doi:10.1101/lm.026252.112 · Cited by 163 · see citing works
“In addition, spindle activity correlates with memory retention over sleep (Clemens et al. 2005, 2006; Van der Helm et al. 2011) and predicts performance in a directed-forgetting paradigm (Saletin et al. 2011), suggesting spindle involvement in memory consolidation processes.”
BackgroundSlow 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
The role of sleep spindles and slow-wave activity in integrating new information in semantic memory
Tamminen, J., Lambon Ralph, M. A., & Lewis, P. A. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.5093-12.2013 · Cited by 152 · see citing works
The Role of Sleep in Memory Consolidation and Brain Plasticity: Dream or Reality?
Frank, M. G., & Benington, J. H. (2006) · The Neuroscientist · doi:10.1177/1073858406293552 · Cited by 143 · 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
Synaptic Mechanisms of Memory Consolidation during Sleep Slow Oscillations
Wei, Y., Krishnan, G. P., & Bazhenov, M. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.3648-15.2016 · Cited by 116 · 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
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
Self-citationA 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
Plasticity during sleep is linked to specific regulation of cortical circuit activity
Niethard, N., Burgalossi, A., & Born, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00065 · Cited by 89 · 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
Sleep and dreaming are for important matters
Perogamvros, L., Dang-Vu, T. T., Desseilles, M., & Schwartz, S. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00474 · Cited by 77 · see citing works
“…spindles during NREM sleep have been reported to be associated with memory (procedural and declarative) consolidation and synaptic plasticity processes (Huber et al., 2004; Rosanova and Ulrich, 2005; Marshall et al., 2006; Bergmann et al., 2008; Diekelmann and Born, 2010; Fogel and Smith, 2011).”
BackgroundFogel, S. M., Smith, C. T., & Beninger, R. J. (2009) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2009.03.002 · Cited by 80 · 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
Sleep 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
The memory function of noradrenergic activity in non-REM sleep
Gais, S., Rasch, B., Dahmen, J. C., Sara, S., & Born, J. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2011.21622 · Cited by 60 · 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
How 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
Niethard, N., Brodt, S., & Born, J. (2021) · The Journal of Neuroscience · doi:10.1523/jneurosci.1957-20.2021 · Cited by 46 · see citing works
Varela, C., & Wilson, M. A. (2020) · eLife · doi:10.7554/elife.48881 · 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
Friedrich, M., Mölle, M., Friederici, A. D., & Born, J. (2019) · Developmental Science · doi:10.1111/desc.12743 · Cited by 38 · 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
Coupling of gamma band activity to sleep spindle oscillations - a combined EEG/MEG study
Weber, F. D., Supp, G. G., Klinzing, J. G., Mölle, M., Engel, A. K., & Born, J. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2020.117452 · Cited by 29 · see citing works
Neural mechanisms of mental schema: a triplet of delta, low beta/spindle and ripple oscillations
Ohki, T., & Takei, Y. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13844 · Cited by 20 · 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
- Authors
- Rosanova, M., & Ulrich, D.
- Affiliations
- University of Bern (CH)
- Corresponding author
- Ulrich, Daniel
- ORCID
- Rosanova, Mario
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2005-10-12
- Volume
- 25
- Issue
- 41
- Pages
- 9398-9405
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6725710
- OpenAlex
- W2003326720
- Cited by
- 413
- References
- 6
- Citations by year
- 2026: 4 · 2025: 13 · 2024: 21 · 2023: 15 · 2022: 20 · 2021: 16 · 2020: 27 · 2019: 42 · 2018: 25 · 2017: 28 · 2016: 32 · 2015: 22 · 2014: 26 · 2013: 28 · 2012: 14
- FWCI
- 3.27
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Canadian Institutes of Health Research
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- sleep spindles, long-term potentiation, short-term potentiation, slow oscillations, synaptic plasticity, NMDA receptor, L-type calcium channels, Hebbian learning, spike trains, memory consolidation, somatosensory cortex, pyramidal neurons, NREM sleep
- MeSH terms
- Action Potentials, Animals, Cats, Male, Sleep, Somatosensory Cortex, Rats, Wistar, Long-Term Potentiation, Rats
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