Slow oscillation electrical brain stimulation during waking promotes EEG theta activity and memory encoding
Open accessAbstract
The application of transcranial slow oscillation stimulation (tSOS; 0.75 Hz) was previously shown to enhance widespread endogenous EEG slow oscillatory activity when applied during a sleep period characterized by emerging endogenous slow oscillatory activity. Processes of memory consolidation typically occurring during this state of sleep were also enhanced. Here, we show that the same tSOS applied in the waking brain also induced an increase in endogenous EEG slow oscillations (0.4-1.2 Hz), although in a topographically restricted fashion. Applied during wakefulness tSOS, additionally, resulted in a marked and widespread increase in EEG theta (4-8 Hz) activity. During wake, tSOS did not enhance consolidation of memories when applied after learning, but improved encoding of hippocampus-dependent memories when applied during learning. We conclude that the EEG frequency and related memory processes induced by tSOS critically depend on brain state. In response to tSOS during wakefulness the brain transposes stimulation by responding preferentially with theta oscillations and facilitated encoding.
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?
Theta rhythm substantially correlates with episodic and emotional memory in waking EEG studies.
“waking EEG studies showing that the theta rhythm substantially correlates with episodic and emotional memory”
From The Functional Role of Dreaming in Emotional Processes (2019) · cites this paper as Kirov et al., 2009
The Discussion (page unavailable) reports that waking EEG theta activity is associated with episodic-memory encoding and retrieval. It does not report a corresponding relationship with emotional memory, so that part of the claim is unsupported. (LLM, conf=0.87)
Experimental — accuracy not yet measuredEffects of SO-tDCS depend on brain state: when applied during waking (rather than during non-REM sleep), tDCS induced a widespread increase in 4-8 Hz theta and 16-14 Hz beta activity, rather than slow oscillation activity, and these increases were associated with an enhanced encoding of declarative memory (for words), particularly in later learning trials (R5, R6), whereas consolidation across the
“D: effects of SO-tDCS depend on brain state: when applied during waking (rather than during non-REM sleep), tDCS induced a widespread increase in 4 -8 Hz theta and 16 -14 Hz beta activity, rather than slow oscillation activity, and these increases were associated with an enhanced encoding of declarative memory (for words), particularly in later learning trials (R5, R6), whereas consolidation”
From About Sleep's Role in Memory (2013) · cites this paper as [643]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredApplying the 0.75 Hz slow oscillatory stimulation during wakefulness induced a widespread increase in theta (4-8 Hz), rather than slow oscillation activity, and this increase in theta activity was associated with a significant improvement in the encoding of declarative memories, rather than affecting retention of these memories.
“Applying the 0.75 Hz slow oscillatory stimulation during wakefulness induced a widespread increase in theta (4 -8 Hz), rather than slow oscillation activity, and this increase in theta activity was associated with a significant improvement in the encoding of declarative memories, rather than affecting retention of these memories (FIGURE 5D, Ref. 643).”
From About Sleep's Role in Memory (2013) · cites this paper as [643]
toDCS only at 0.75 Hz (not at 5 Hz) and applied only during sleep leads to an increase of memory consolidation.
“In addition, there is evidence that toDCS only at 0.75 Hz (not at 5 Hz) and applied only during sleep leads to an increase of memory consolidation [32,52,53].”
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
Development and validation of brief measures of positive and negative affect: The PANAS scales.
Watson, D., Clark, L. A., & Tellegen, A. (1988) · Journal of Personality and Social Psychology · doi:10.1037/0022-3514.54.6.1063 · Cited by 32,433 · see citing works
A new method for off-line removal of ocular artifact
Gratton, G., Coles, M. G. H., & Donchin, E. (1983) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(83)90135-9 · Cited by 5,055 · see citing works
Steriade, M., Nunez, A., & Amzica, F. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-08-03252.1993 · Cited by 1,903 · 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-citationThe 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
Walker, M. P., & Stickgold, R. (2006) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070307 · Cited by 1,075 · cited 1× · see citing works
“Stimulation parameters were the same as in a previous study of our lab (1, 8) and as follows.”
ResultLaufs, H., Krakow, K., Sterzer, P., Eger, E., Beyerle, A., Salek-Haddadi, A., & Kleinschmidt, A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1831638100 · Cited by 1,028 · see citing works
Theta and gamma oscillations during encoding predict subsequent recall
Sederberg, P. B., Kahana, M. J., Howard, M. W., Donner, E. J., & Madsen, J. R. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-34-10809.2003 · Cited by 750 · see citing works
Synchronization between prefrontal and posterior association cortex during human working memory
Sarnthein, J., Petsche, H., Rappelsberger, P., Shaw, G. L., & von Stein, A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.12.7092 · Cited by 716 · see citing works
Origin of Slow Cortical Oscillations in Deafferented Cortical Slabs
Timofeev, I. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.12.1185 · Cited by 710 · see citing works
Theta and gamma oscillations predict encoding and retrieval of declarative memory
Osipova, D., Takashima, A., Oostenveld, R., Fernández, G., Maris, E., & Jensen, O. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1948-06.2006 · Cited by 671 · 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
Self-citationGrouping 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-citationMemory 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 · see citing works
Low-frequency (<1Hz) oscillations in the human sleep electroencephalogram
Achermann, P., & Borbély, A. A. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00186-3 · Cited by 577 · see citing works
State-dependency in brain stimulation studies of perception and cognition
Silvanto, J., Muggleton, N., & Walsh, V. (2008) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2008.09.004 · Cited by 572 · see citing works
Frontal-midline theta from the perspective of hippocampal “theta”
Mitchell, D. J., McNaughton, N., Flanagan, D., & Kirk, I. J. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2008.09.005 · Cited by 549 · see citing works
Kahana, M. J., Seelig, D., & Madsen, J. R. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(01)00278-1 · Cited by 485 · see citing works
Source modeling sleep slow waves
Murphy, M., Riedner, B. A., Huber, R., Massimini, M., Ferrarelli, F., & Tononi, G. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807933106 · Cited by 454 · see citing works
Finelli, L. A., Baumann, H., Borbély, A. A., & Achermann, P. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00409-7 · Cited by 447 · see citing works
Frequency-dependent electrical stimulation of the visual cortex.
Kanai, R., Chaieb, L., Antal, A., Walsh, V., & Paulus, W. (2008) · Current Biology · doi:10.1016/j.cub.2008.10.027 · Cited by 427 · see citing works
Modeling Sleep and Wakefulness in the Thalamocortical System
Hill, S., & Tononi, G. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00915.2004 · Cited by 417 · see citing works
Tulving, E., & Madigan, S. A. (1970) · Annual Review of Psychology · doi:10.1146/annurev.ps.21.020170.002253 · Cited by 391 · see citing works
Sauseng, P., Hoppe, J., Klimesch, W., Gerloff, C. P., & Hummel, F. C. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05286.x · Cited by 365 · see citing works
Hasselmo, M. E., & Wyble, B. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00048-x · Cited by 337 · see citing works
The Cognitive Correlates of Human Brain Oscillations
Kahana, M. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3737-05c.2006 · Cited by 319 · see citing works
Esser, S. K., Hill, S. L., & Tononi, G. (2007) · Sleep · doi:10.1093/sleep/30.12.1617 · Cited by 315 · see citing works
Differential Encoding Mechanisms for Subsequent Associative Recognition and Free Recall
Staresina, B. P., & Davachi, L. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2877-06.2006 · Cited by 306 · 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
Network Oscillations: Emerging Computational Principles
Sejnowski, T. J., & Paulsen, O. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3737-05d.2006 · Cited by 284 · see citing works
Long-range EEG synchronization during word encoding correlates with successful memory performance
Weiß, S., & Rappelsberger, P. (2000) · Cognitive Brain Research · doi:10.1016/s0926-6410(00)00011-2 · Cited by 278 · see citing works
Restoring theta‐like rhythmicity in rats restores initial learning in the Morris water maze
McNaughton, N., Ruan, M., & Woodnorth, M. (2006) · Hippocampus · doi:10.1002/hipo.20235 · Cited by 255 · see citing works
Sammer, G., Blecker, C. R., Gebhardt, H., Bischoff, M., Stark, R. M., Morgen, K., & Vaitl, D. (2006) · Human Brain Mapping · doi:10.1002/hbm.20309 · Cited by 245 · see citing works
Maintaining memories by reactivation
Rasch, B., & Born, J. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.11.007 · Cited by 240 · see citing works
Self-citationHuber, 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
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-citationTheta activity in the waking EEG is a marker of sleep propensity in the rat
Vyazovskiy, V. V., & Tobler, I. (2005) · Brain Research · doi:10.1016/j.brainres.2005.05.022 · Cited by 210 · see citing works
Theta coupling in the human electroencephalogram during a working memory task
Sauseng, P., Klimesch, W., Doppelmayr, M. M., Hanslmayr, S., Schabus, M., & Gruber, W. R. (2003) · Neuroscience Letters · doi:10.1016/j.neulet.2003.10.002 · Cited by 204 · see citing works
Klimesch, W., Doppelmayr, M. M., Stadler, W., Pöllhuber, D., Sauseng, P., & Roehm, D. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)01656-1 · Cited by 201 · see citing works
Human cortical circuits for central executive function emerge by theta phase synchronization
Mizuhara, H., & Yamaguchi, Y. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.02.026 · Cited by 175 · see citing works
A long-range cortical network emerging with theta oscillation in a mental task
Mizuhara, H., Wang, L., KOBAYASHI, K., & Yamaguchi, Y. (2004) · Neuroreport · doi:10.1097/01.wnr.0000126755.09715.b3 · Cited by 152 · see citing works
Rasch, B. H., Born, J., & Gais, S. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.5.793 · Cited by 137 · see citing works
Self-citationEEG 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 · see citing works
Self-citationBoggio, P. S., Fregni, F., Valasek, C. A., Ellwood, S., Chi, R., Gallate, J. E., Pascual‐Leone, Á., & Snyder, A. W. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004959 · Cited by 114 · see citing works
Theta synchronization predicts efficient memory encoding of concrete and abstract nouns
Weiß, S., Müller, H. M., & Rappelsberger, P. (2000) · Neuroreport · doi:10.1097/00001756-200008030-00005 · Cited by 109 · see citing works
Physiology, Pharmacology, and Topography of Cholinergic Neocortical Oscillations In Vitro
Lukatch, H. S., & MacIver, M. B. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.5.2427 · Cited by 82 · see citing works
The Upshot of Up States in the Neocortex: From Slow Oscillations to Memory Formation
Hoffman, K., Battaglia, F., Harris, K., MacLean, J., Marshall, L., & Mehta, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3501-07.2007 · Cited by 72 · see citing works
Self-citationBabiloni, C., Vecchio, F., Mirabella, G., Buttiglione, M., Sebastiano, F., Picardi, A., Gennaro, G. D., Quarato, P. P., Grammaldo, L. G., Buffo, P., et al. (2008) · Human Brain Mapping · doi:10.1002/hbm.20648 · Cited by 69 · see citing works
Bao, W., & Wu, J. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00715.2002 · Cited by 65 · see citing works
Reducing false memories by magnetic pulse stimulation
Gallate, J. E., Chi, R., Ellwood, S., & Snyder, A. W. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.11.021 · Cited by 55 · see citing works
The roles of EEG oscillations in learning relational information
Caplan, J. B., & Glaholt, M. G. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.07.054 · Cited by 53 · 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-citationAdvances in Cognitive Neurodynamics ICCN 2007
Wang, R., Shen, E., & Gu, F. (2008) · Springer eBooks · doi:10.1007/978-1-4020-8387-7 · Cited by 35 · see citing works
Corticothalamic Projections Control Synchronization in Locally Coupled Bistable Thalamic Oscillators
Mayer, J., Schuster, H. G., Claussen, J. C., et al. (2007) · Physical Review Letters · doi:10.1103/physrevlett.99.068102 · Cited by 18 · see citing works
Staying awake puts pressure on brain arousal systems
Tononi, G., & Cirelli, C. (2007) · Journal of Clinical Investigation · doi:10.1172/jci34250 · Cited by 13 · see citing works
Oscillating current stimulation – slow oscillation stimulation during sleep
Marshall, L., Mölle, M., & Jan Born, A. (2006) · Protocol Exchange · doi:10.1038/nprot.2006.299 · Cited by 10 · see citing works
Self-citationBattaglia, F. P., Benchenane, K., Khamassi, M., et al. (2008) · Springer eBooks · doi:10.1007/978-1-4020-8387-7_50 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [56]Janke W, Debus G. Die Eigenschaftswörterliste EWL. Eine mehrdimensionale Methode zur Beschreibung von Aspekten des Befindens. Göttingen, Germany: Hogrefe; 1978. [Google Scholar]
- [57]Aschenbrenner S, Tucha KW, Lange W. Regensburg Word Fluency Test. Göttingen, Germany: Hogrefe; 2000. in German. [Google Scholar]
Cited by
Sorted by citations
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
Self-citationComorbidity: a network perspective
Cramer, A. O. J., Waldorp, L. J., van der Maas, H. L. J., & Borsboom, D. (2010) · Behavioral and Brain Sciences · doi:10.1017/s0140525x09991567 · Cited by 1,575 · see citing works
Endogenous electric fields may guide neocortical network activity
Fröhlich, F., & McCormick, D. A. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.005 · Cited by 913 · 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
Marshall, L., Kirov, R., Brade, J., Mölle, M., & Born, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016905 · Cited by 188 · see citing works
The Functional Role of Dreaming in Emotional Processes
Scarpelli, S., Bartolacci, C., D'Atri, A., Gorgoni, M., & De Gennaro, L. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.00459 · Cited by 190 · see citing works
“It is worth noting that taken together, these results are in line with the waking EEG studies showing that the theta rhythm substantially correlates with episodic and emotional memory (Klimesch et al., 1996; Klimesch, 1999; Kirov et al., 2009; Uribe et al., 2011).”
ResultPrehn-Kristensen, A., Munz, M., Göder, R., Wilhelm, I., Korr, K., Vahl, W., Wiesner, C. D., & Baving, L. (2014) · Brain Stimulation · doi:10.1016/j.brs.2014.07.036 · Cited by 176 · see citing works
Imaging human brain networks to improve the clinical efficacy of non-invasive brain stimulation
Sale, M. V., Mattingley, J. B., Zalesky, A., & Cocchi, L. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.09.010 · Cited by 145 · see citing works
Transcranial slow oscillation stimulation during sleep enhances memory consolidation in rats
Binder, S., Berg, K., Gasca, F., Lafon, B., Parra, L. C., Born, J., & Marshall, L. (2014) · Brain Stimulation · doi:10.1016/j.brs.2014.03.001 · Cited by 74 · see citing works
Self-citationGroppa, S., Bergmann, T. O., Siems, C., Mölle, M., Marshall, L., & Siebner, H. R. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.01.019 · Cited by 67 · see citing works
Self-citationSalfi, F., D’Atri, A., Tempesta, D., De Gennaro, L., & Ferrara, M. (2020) · Brain Sciences · doi:10.3390/brainsci10050300 · Cited by 36 · see citing works
Lin, H.-C., Pan, H.-C., Lin, S.-H., Lo, Y.-C., Shen, E. T.-H., Liao, L.-D., Liao, P.-H., Chien, Y.-W., Liao, K.-D., Jaw, F.-S., et al. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00087 · Cited by 29 · see citing works
Control of cortical oscillatory frequency by a closed-loop system
D’Andola, M., Giulioni, M., Dante, V., Del Giudice, P., & Sanchez-Vives, M. V. (2019) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/s12984-018-0470-z · Cited by 16 · see citing works
- Authors
- Kirov, R., Weiss, C., Siebner, H. R., Born, J., & Marshall, L.
- Affiliations
- Bulgarian Academy of Sciences (BG)
- University of Lübeck (DE)
- Copenhagen University Hospital (DK)
- Department of Neuroendocrinology, University of Lübeck, 23538 Lübeck, Germany;
- Corresponding author
- Marshall, Lisa
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-09-08
- Volume
- 106
- Issue
- 36
- Pages
- 15460-15465
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2730962
- OpenAlex
- W2008440125
- Cited by
- 208
- References
- 58
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 5 · 2023: 4 · 2022: 15 · 2021: 14 · 2020: 6 · 2019: 17 · 2018: 16 · 2017: 10 · 2016: 18 · 2015: 12 · 2014: 20 · 2013: 18 · 2012: 16
- FWCI
- 6.80
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- transcranial electrical stimulation, theta oscillations, memory encoding, memory consolidation, hippocampal-dependent memory, wakefulness
- MeSH terms
- Adult, Analysis of Variance, Brain, Electric Stimulation Therapy, Germany, Humans, Learning, Memory, Oscillometry, Theta Rhythm, Wakefulness
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
