A local signature of LTP‐ and LTD‐like plasticity in human NREM sleep
Abstract
Paired associative stimulation (PAS) repeatedly pairs electrical nerve stimulation with transcranial magnetic stimulation of the contralateral motor hand area (M1 HAND). Depending on the interstimulus interval, PAS can induce a long‐term potentiation (LTP)‐like facilitation or long‐term depression (LTD)‐like suppression of cortical excitability. In three experimental sessions, 12 awake men received PAS of the right median nerve and left M1 HAND in the evening before sleep. To optimize the timing of paired stimulation in M1 HAND, the interstimulus interval of PAS was adjusted to the individual N20‐latency of the somatosensory evoked potential to induce LTP‐like effects (PAS N20+2ms), LTD‐like effects (PAS N20−5ms), or no timing‐dependent after‐effects (PAS control). Motor‐evoked potentials (MEPs) showed high interindividual variations in the conditioning effects of PAS N20+2ms and PAS N20−5ms on cortical excitability. However, PAS control allowed us to adjust for any unspecific stimulation effects and the MEP increase after PAS N20+2ms differed significantly from the MEP decrease after PAS N20−5ms. PAS N20+2ms and PAS N20−5ms also had a differential effect on regional expression of slow waves and slow spindle activity during the first hour of subsequent non‐rapid eye movement (NREM) sleep. At the electrode sites overlying the conditioned M1 HAND and the adjacent premotor cortex, local expression of slow spindle activity was significantly correlated with interindividual differences in the efficacy of PAS N20+2ms and PAS N20−5ms to potentiate or suppress cortical excitability. This correlation indicates that PAS shapes the local regulation of slow sleep spindles during subsequent NREM sleep.
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Similar effects of PAS stimulation on SWA were associated with local changes in slow spindle activity.
“In another study, similar effects of PAS stimulation on SWA were associated with local changes in slow spindle activity (85).”
From About Sleep's Role in Memory (2013) · cites this paper as [85]
In humans, the local expression of spindle activity during non-REM sleep increased or decreased depending on whether LTP-like or LTD-like plasticity had been induced through TMS before sleep.
“Correspondingly in humans, the local expression of spindle activity during non-REM sleep increased or decreased depending on whether LTP-like or LTD-like plasticity had been induced through transcranial magnetic stimulation (TMS) before sleep (85).”
From About Sleep's Role in Memory (2013) · cites this paper as [85]
Cites
Rechtschaffen, A. (1968) · Medical Entomology and Zoology · Cited by 11,772 · see citing works
Nonparametric permutation tests for functional neuroimaging: A primer with examples
Nichols, T. E., & Holmes, A. P. (2002) · Human Brain Mapping · doi:10.1002/hbm.1058 · Cited by 6,256 · see citing works
Hobson, J. A. (1969) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(69)90021-2 · Cited by 5,215 · 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
Sleep-dependent memory consolidation
Stickgold, R. (2005) · Nature · doi:10.1038/nature04286 · Cited by 1,857 · see citing works
Huber, R., Felice Ghilardi, M., Massimini, M., & Tononi, G. (2004) · Nature · doi:10.1038/nature02663 · Cited by 1,854 · 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
Self-citationBreakdown of cortical effective connectivity during sleep
Massimini, M., Ferrarelli, F., Huber, R., Esser, S. K., Singh, H., & Tononi, G. (2005) · Science · doi:10.1126/science.1117256 · Cited by 1,534 · see citing works
Induction of plasticity in the human motor cortex by paired associative stimulation
Stefan, K. (2000) · Brain · doi:10.1093/brain/123.3.572 · Cited by 1,484 · 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
Gennaro, L. D., & Ferrara, M. (2003) · Sleep Medicine Reviews · doi:10.1053/smrv.2002.0252 · Cited by 925 · see citing works
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 · see citing works
Self-citationThe 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
Self-citationStefan, K., Kunesch, E., Benecke, R., Cohen, L. G., & Claßen, J. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.023317 · Cited by 643 · see citing works
A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex.
Wolters, A., Sandbrink, F., Schlottmann, A., Kunesch, E., Stefan, K., Cohen, L., Benecke, R., & Classen, J. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00900.2002 · Cited by 633 · 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-citationZiemann, U., Ilic, T. V., Pauli, C., Meintzschel, F., & Ruge, D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5016-03.2004 · Cited by 587 · see citing works
Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity
Huber, R., Ghilardi, M. F., Massimini, M., Ferrarelli, F., Riedner, B. A., Peterson, M. J., & Tononi, G. (2006) · Nature Neuroscience · doi:10.1038/nn1758 · Cited by 579 · see citing works
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 · see citing works
Born, J., Rasch, B., & Gais, S. (2006) · The Neuroscientist · doi:10.1177/1073858406292647 · Cited by 557 · see citing works
Self-citationDaytime naps, motor memory consolidation and regionally specific sleep spindles
Nishida, M., & Walker, M. P. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000341 · Cited by 531 · see citing works
Magnetic brain stimulation with a double coil: the importance of coil orientation
Mills, K. R., Boniface, S. J., & Schubert, M. (1992) · Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section · doi:10.1016/0168-5597(92)90096-t · Cited by 516 · see citing works
Triggering sleep slow waves by transcranial magnetic stimulation
Massimini, M., Ferrarelli, F., Esser, S. K., Riedner, B. A., Huber, R., Murphy, M., Peterson, M. J., & Tononi, G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702495104 · Cited by 489 · 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
Modulation of Associative Human Motor Cortical Plasticity by Attention
Stefan, K., Wycislo, M., & Claßen, J. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00383.2003 · Cited by 464 · 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
Overnight 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 · see citing works
Abnormal associative plasticity of the human motor cortex in writer's cramp
Quartarone, A. (2003) · Brain · doi:10.1093/brain/awg273 · Cited by 400 · 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
Sale, M. V., Ridding, M. C., & Nordstrom, M. A. (2007) · Experimental Brain Research · doi:10.1007/s00221-007-0960-x · Cited by 291 · 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
FOGEL, S., SMITH, C., & COTE, K. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.02.037 · Cited by 246 · see citing works
Huber, R., Esser, S. K., Ferrarelli, F., Massimini, M., Peterson, M. J., & Tononi, G. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000276 · Cited by 232 · see citing works
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 · see citing works
Nitsche, M. A., Roth, A., Kuo, M., Fischer, A., Liebetanz, D., Lang, N., Tergau, F., & Paulus, W. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5348-06.2007 · Cited by 222 · see citing works
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 · see citing works
Self-citationAnderer, P., Klösch, G., Gruber, G., Trenker, E., Pascual-Marqui, R. D., Zeitlhofer, J., Barbanoj, M. J., Rappelsberger, P., & Saletu, B. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00028-8 · Cited by 220 · see citing works
The two sides of associative plasticity in writer's cramp
Weise, D. (2006) · Brain · doi:10.1093/brain/awl221 · Cited by 198 · see citing works
Timing‐dependent plasticity in human primary somatosensory cortex
Wolters, A., Schmidt, A., Schramm, A., Zeller, D., Naumann, M. K., Kunesch, E., Benecke, R., Reiners, K., & Claßen, J. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.084954 · Cited by 191 · see citing works
Gilio, F., Rizzo, V., Siebner, H. R., & Rothwell, J. C. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.044313 · Cited by 183 · 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
Müller, J. F. M., Orekhov, Y., Liu, Y., & Ziemann, U. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05603.x · Cited by 175 · 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
Suppression of LTP-like plasticity in human motor cortex by the GABAB receptor agonist baclofen
McDonnell, M. N., Orekhov, Y., & Ziemann, U. (2007) · Experimental Brain Research · doi:10.1007/s00221-006-0849-0 · Cited by 147 · see citing works
Fratello, F., Veniero, D., Curcio, G., Ferrara, M., Marzano, C., Moroni, F., Pellicciari, M. C., Bertini, M., Rossini, P. M., & Gennaro, L. D. (2006) · Clinical Neurophysiology · doi:10.1016/j.clinph.2006.07.315 · Cited by 113 · see citing works
Paired associative stimulation.
Claßen, J., Wolters, A., Stefan, K., Wycislo, M., Sandbrink, F., Schmidt, A., & Kunesch, E. (2004) · PubMed · Cited by 111 · see citing works
Chapter 59 Paired associative stimulation
Claßen, J., Wolters, A., Stefan, K., Wycislo, M., Sandbrink, F., Schmidt, A., & Kunesch, E. (2004) · Supplements to Clinical neurophysiology · doi:10.1016/s1567-424x(09)70395-2 · Cited by 100 · see citing works
Werk, C. M., Harbour, V. L., & Chapman, C. A. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.12.020 · Cited by 60 · see citing works
Murakami, T., Sakuma, K., Nomura, T., Uemura, Y., Hashimoto, I., & Nakashima, K. (2007) · Experimental Brain Research · doi:10.1007/s00221-007-1103-0 · Cited by 32 · see citing works
Long-term depression in the sensorimotor cortex induced by repeated delivery of 10 Hz trains in vivo
Werk, C. M., Klein, H. S., Nesbitt, C., & Chapman, C. A. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.02.004 · Cited by 23 · see citing works
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- Authors
- Bergmann, T. O., Mölle, M., Marshall, L., Kaya‐Yildiz, L., Born, J., & Roman Siebner, H.
- Affiliations
- Christian-Albrechts-Universität zu Kiel (DE)
- University of Lübeck (DE)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2008-04-25
- Volume
- 27
- Issue
- 9
- Pages
- 2241-2249
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2063608151
- Cited by
- 67
- References
- 50
- Citations by year
- 2025: 2 · 2024: 5 · 2021: 1 · 2020: 6 · 2019: 2 · 2018: 5 · 2017: 1 · 2016: 6 · 2015: 2 · 2014: 4 · 2013: 6 · 2012: 4
- FWCI
- 5.03
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Bundesministerium für Bildung und Forschung
- Topics
- Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- paired associative stimulation, long-term potentiation, long-term depression, NREM sleep, sleep spindles, slow waves, motor cortex excitability, individual differences, somatosensory evoked potentials, motor evoked potentials, premotor cortex, cortical plasticity
- MeSH terms
- Adult, Brain, Electric Stimulation, Electroencephalography, Hand, Humans, Male, Median Nerve, Memory, Sleep, Polysomnography, Long-Term Potentiation, Evoked Potentials, Motor, Long-Term Synaptic Depression, Transcranial Magnetic Stimulation
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