Fine‐tuned coupling between human parahippocampal ripples and sleep spindles
Open accessAbstract
Sleep‐associated memory consolidation is thought to rely on coordinated information transfer between the hippocampus and neocortex brought about during slow wave sleep (SWS) by distinct local field potential oscillations. Specifically, findings in animals have led to the concept that ripples originating from hippocampus combine with spindles to provide a fine‐tuned temporal frame for a persistent transfer of memory‐related information to the neocortex. The present study focused on characterizing the temporal relationship between parahippocampal ripple activity (80–140 Hz) and spindles recorded from frontal, parietal and parahippocampal cortices in 12 epilepsy patients implanted with parahippocampal foramen ovale electrodes. Overall, parietal and parahippocampal spindles showed closer relationships to parahippocampal ripple activity than frontal spindles, with the latter following parietal and parahippocampal spindles at a variable delay of up to 0.5 s. On a timescale of seconds, ripple activity showed a continuous increase before the peak of parietal and parahippocampal spindles, and decreased thereafter. At a fine timescale of milliseconds, parahippocampal ripple activity was tightly phase‐locked to the troughs of these spindles. The demonstration of spindle phase‐locked ripple activity in humans is consistent with the idea of a temporally fine‐tuned hippocampus‐to‐neocortex transfer of information taking place during SWS.
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Fine-grained temporal analyses revealed that the co-occurrence of spindles and ripples leads to the formation of so-called spindle-ripple events where individual ripple events become temporally nested into succeeding troughs of a spindle.
“Moreover, fine-grained temporal analyses revealed that the co-occurrence of spindles and ripples leads to the formation of so-called”
From About Sleep's Role in Memory (2013) · cites this paper as [216]
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Cites
Rechtschaffen, A. (1968) · Medical Entomology and Zoology · Cited by 11,772 · see citing works
Neuronal Oscillations in Cortical Networks
Buzsáki, G., & Draguhn, A. (2004) · Science · doi:10.1126/science.1099745 · Cited by 6,576 · see citing works
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 · see citing works
Buzsáki, G. (2006) · doi:10.1093/acprof:oso/9780195301069.001.0001 · Cited by 4,873 · see citing works
Diekelmann, S., & Born, J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2762 · Cited by 3,760 · see citing works
Self-citationReactivation of hippocampal ensemble memories during sleep
Wilson, M. A., & McNaughton, B. L. (1994) · Science · doi:10.1126/science.8036517 · Cited by 3,118 · see citing works
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 · see citing works
Two-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 · see citing works
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 · see citing works
Grouping of brain rhythms in corticothalamic systems
Steriade, M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.029 · Cited by 1,296 · see citing works
Forward and reverse hippocampal place-cell sequences during ripples
Diba, K., & Buzsáki, G. (2007) · Nature Neuroscience · doi:10.1038/nn1961 · Cited by 1,205 · see citing works
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 · see citing works
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 · see citing works
Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm
Sirota, A., Montgomery, S., Fujisawa, S., Isomura, Y., Zugaro, M., & Buzsáki, G. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.014 · Cited by 1,015 · see citing works
The Hippocampo-Neocortical Dialogue
Buzsáki, G. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.2.81 · Cited by 938 · see citing works
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 · see citing works
Communication 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 · see citing works
Gennaro, L. D., & Ferrara, M. (2003) · Sleep Medicine Reviews · doi:10.1053/smrv.2002.0252 · Cited by 925 · see citing works
Kudrimoti, H. S., Barnes, C. A., & McNaughton, B. L. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-10-04090.1999 · Cited by 753 · see citing works
Bragin, A., Engel, J., Wilson, C. L., Fried, I., & Mathern, G. W. (1999) · Epilepsia · doi:10.1111/j.1528-1157.1999.tb02065.x · Cited by 746 · see citing works
Hippocampal Efferents Reach Widespread Areas of Cerebral Cortex and Amygdala in the Rhesus Monkey
Rosene, D. L., & Hoesen, G. W. V. (1977) · Science · doi:10.1126/science.410102 · Cited by 678 · 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
Staba, R. J., Wilson, C. L., Bragin, A., Fried, I., & Engel, J. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.4.1743 · Cited by 666 · see citing works
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 650 · see citing works
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 · see citing works
Self-citationA direct projection from Ammon's horn to prefrontal cortex in the rat
Swanson, L. W. (1981) · Brain Research · doi:10.1016/0006-8993(81)90192-x · Cited by 533 · see citing works
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 · see citing works
Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep
Schabus, M., Dang-Vu, T. T., Albouy, G., Balteau, E., Boly, M., Carrier, J., Darsaud, A., Degueldre, C., Desseilles, M., Gais, S., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0703084104 · Cited by 488 · see citing works
Steriade, M. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.6.583 · Cited by 429 · see citing works
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 · 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
Self-citationRipples in the medial temporal lobe are relevant for human memory consolidation
Axmacher, N., Elger, C. E., & Fell, J. (2008) · Brain · doi:10.1093/brain/awn103 · Cited by 372 · see citing works
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 · see citing works
Self-citationHigh‐frequency oscillations recorded in human medial temporal lobe during sleep
Staba, R. J., Wilson, C. L., Bragin, A., Jhung, D., Fried, I., & Engel, J. (2004) · Annals of Neurology · doi:10.1002/ana.20164 · Cited by 329 · 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
Self-citationQuantification, smoothing, and confidence limits for single-units' histograms
Abeles, M. (1982) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(82)90002-4 · Cited by 309 · see citing works
State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep
Wierzynski, C. M., Lubenov, E. V., Gu, M., & Siapas, A. G. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.011 · Cited by 289 · see citing works
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 · see citing works
Topographic distribution of sleep spindles in young healthy subjects
ZEITLHOFER, J., GRUBER, G., ANDERER, P., ASENBAUM, S., SCHIMICEK, P., & SALETU, B. (1997) · Journal of Sleep Research · doi:10.1046/j.1365-2869.1997.00046.x · Cited by 222 · see citing works
Wieser, H. G., Elger, C. E., & Stodieck, S. R. G. (1985) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(85)91098-3 · Cited by 207 · see citing works
Paré, D., Steriade, M., Deschênes, M., & Oakson, G. (1987) · Journal of Neurophysiology · doi:10.1152/jn.1987.57.6.1669 · Cited by 114 · see citing works
Spontaneous activity of the perirhinal cortex in behaving cats
Collins, D. R., Lang, E. J., & Paré, D. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00396-0 · Cited by 70 · see citing works
Hippocampus Whispering in Deep Sleep to Prefrontal Cortex—For Good Memories?
Mölle, M., & Born, J. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.002 · Cited by 51 · see citing works
Self-citationSleep Spindles in the Human Hippocampus: Normal or Epileptic Activity?
Montplaisir, J., Leduc, L., Laverdière, M., et al. (1981) · SLEEP · doi:10.1093/sleep/4.4.423 · Cited by 40 · see citing works
Hippocampal sleep spindles revisited: physiologic or epileptic activity?
Malow, B. A., Carney, P. R., Kushwaha, R., & BOWES, R. J. (1999) · Clinical Neurophysiology · doi:10.1016/s1388-2457(99)00008-5 · Cited by 40 · see citing works
Asano, E., Mihaylova, T. G., Juhász, C., Sood, S., & Chugani, H. T. (2007) · Clinical Neurophysiology · doi:10.1016/j.clinph.2007.02.021 · Cited by 34 · see citing works
Nocturnal sleep stereo-electroencephalography and polygraphy in epileptics.
Faber, J., & Vladyka (1984) · PubMed · Cited by 4 · see citing works
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 · see citing works
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Sorted by citations
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
“, at the up-to-down state transition), and thus also tend to follow hippocampal SW-Rs with the same delay (216).”
BackgroundSelf-citationHippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759 · see citing works
Staresina, B. P., Bergmann, T. O., Bonnefond, M., van der Meij, R., Jensen, O., Deuker, L., Elger, C. E., Axmacher, N., & Fell, J. (2015) · Nature Neuroscience · doi:10.1038/nn.4119 · Cited by 831 · 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
System consolidation of memory during sleep
Born, J., & Wilhelm, I. (2012) · Psychological Research · doi:10.1007/s00426-011-0335-6 · Cited by 667 · see citing works
Self-citationLatchoumane, 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
Self-citationSleep 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
Hippocampal ripples and memory consolidation
Girardeau, G., & Zugaro, M. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.02.005 · Cited by 330 · 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
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
Self-citationBergmann, 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
Self-citationLecci, S., Fernandez, L. M. J., Weber, F. D., Cardis, R., Chatton, J.-Y., Born, J., & Lüthi, A. (2017) · Science Advances · doi:10.1126/sciadv.1602026 · Cited by 242 · 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
“This phase locking is combined with an even more finegrained nesting of hippocampal ripples inside single troughs of sleep spindles (Clemens et al. 2011).”
BackgroundSleep-dependent memory consolidation – What can be learnt from children?
Wilhelm, I., Prehn-Kristensen, A., & Born, J. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.03.002 · Cited by 161 · see citing works
Self-citationSlow 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
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
Perrault, A. A., Khani, A., Quairiaux, C., Kompotis, K., Franken, P., Muhlethaler, M., Schwartz, S., & Bayer, L. (2019) · Current Biology · doi:10.1016/j.cub.2018.12.028 · Cited by 113 · 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
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
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
“…NREM sleep (Walker et al., 2002a; Stickgold and Walker, 2007) and hippocampal ripples, which prevail during this sleep stage (coupled with the sleep spindles) (Clemens et al., 2011), have been implicated in learning and reward processes during sleep (Pennartz et al., 2004; Lansink et al., 2008).”
BackgroundTemporal associations between sleep slow oscillations, spindles and ripples
Oyanedel, C. N., Durán, E., Niethard, N., Inostroza, M., & Born, J. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14906 · Cited by 71 · see citing works
Self-citationSpindle 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
Different simultaneous sleep states in the hippocampus and neocortex
Emrick, J. J., Gross, B. A., Riley, B. T., & Poe, G. R. (2016) · Sleep · doi:10.5665/sleep.6326 · Cited by 38 · see citing works
Targeting sleep oscillations to improve memory in schizophrenia
Manoach, D. S., Mylonas, D., & Baxter, B. (2020) · Schizophrenia Research · doi:10.1016/j.schres.2020.01.010 · Cited by 36 · 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
Alizadeh, Z., Azimi, A., & Ghorbani, M. (2022) · The Journal of Neuroscience · doi:10.1523/jneurosci.2515-21.2022 · Cited by 14 · see citing works
Contreras, M. P., Fechner, J., Born, J., & Inostroza, M. (2023) · The Journal of Neuroscience · doi:10.1523/jneurosci.1967-22.2023 · Cited by 9 · see citing works
Self-citationSleep 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
- Clemens, Z., Mölle, M., Erőss, L., Jakus, R., Rásonyi, G., Halász, P., & Born, J.
- Affiliations
- University of Lübeck (DE)
- Pázmány Péter Catholic University (HU)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2010-12-07
- Volume
- 33
- Issue
- 3
- Pages
- 511-520
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W1546739573
- Cited by
- 214
- References
- 49
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 13 · 2023: 11 · 2022: 14 · 2021: 12 · 2020: 23 · 2019: 23 · 2018: 9 · 2017: 15 · 2016: 16 · 2015: 9 · 2014: 8 · 2013: 26 · 2012: 10
- FWCI
- 9.29
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (SFB654)
- Fundação Bial
- 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-wave sleep, memory consolidation, phase locking, parahippocampal cortex, parietal cortex, frontal cortex, epilepsy patients, foramen ovale electrodes, local field potentials
- MeSH terms
- Adult, Electroencephalography, Epilepsy, Hippocampus, Humans, Memory, Middle Aged, Sleep, Neocortex
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