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Transcranial Direct Current Stimulation during Sleep Improves Declarative Memory
Open accessAbstract
In humans, weak transcranial direct current stimulation (tDCS) modulates excitability in the motor, visual, and prefrontal cortex. Periods rich in slow-wave sleep (SWS) not only facilitate the consolidation of declarative memories, but in humans, SWS is also accompanied by a pronounced endogenous transcortical DC potential shift of negative polarity over frontocortical areas. To experimentally induce widespread extracellular negative DC potentials, we applied anodal tDCS (0.26 mA) [correction] repeatedly (over 30 min) bilaterally at frontocortical electrode sites during a retention period rich in SWS. Retention of declarative memories (word pairs) and also nondeclarative memories (mirror tracing skills) learned previously was tested after this period and compared with retention performance after placebo stimulation as well as after retention intervals of wakefulness. Compared with placebo stimulation, anodal tDCS during SWS-rich sleep distinctly increased the retention of word pairs (p < 0.005). When applied during the wake retention interval, tDCS did not affect declarative memory. Procedural memory was also not affected by tDCS. Mood was improved both after tDCS during sleep and during wake intervals. tDCS increased sleep depth toward the end of the stimulation period, whereas the average power in the faster frequency bands (,alpha, and beta) was reduced. Acutely, anodal tDCS increased slow oscillatory activity <3 Hz. We conclude that effects of tDCS involve enhanced generation of slow oscillatory EEG activity considered to facilitate processes of neuronal plasticity. Shifts in extracellular ionic concentration in frontocortical tissue (expressed as negative DC potentials during SWS) may facilitate sleep-dependent consolidation of declarative memories.
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“In humans, tDCS that oscillated at a very low frequency (0.003 Hz; 30-s on/30-s off) and was applied to the prefrontal cortex during early noctur-nal non-REM sleep, increased endogenous SWA, and produced a significant improvement in the overnight retention of word pair memories (785).”
From About Sleep's Role in Memory (2013) · cites this paper as [785]
Experimental — accuracy not yet measuredIn the citing paper
“By using transcranial oscillating direct current stimulation (toDCS) at 0.75 Hz during SWS in young healthy adults, Marshall and colleagues increased SO power, resulting in boosted sleep-dependent consolidation of declarative memory [32,33].”
In the citing paper
“As shown by Marshall and colleagues, frontally applied anodal toDCS in healthy adults can remarkably improve the sleep-dependent consolidation of declarative memory [32,33].”
In the citing paper
“While healthy adults [32,33], adults suffering from schizophrenia [56], and children with ADHD benefited from toDCS during sleep, elderly healthy participants did not [57].”
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Citations
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
Rechtschaffen, A. (1968) · Medical Entomology and Zoology · Cited by 11,772
Distributed hierarchical processing in the primate cerebral cortex
Felleman, D. J., & Van Essen, D. C. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1 · Cited by 7,783
The ten-twenty electrode system of the international federation
Jasper, H. H. (1958) · Electroencephalography and Clinical Neurophysiology · Cited by 6,567
Preface: Cerebral Cortex Has Come of Age
Goldman, P. S., & RAKIC, P. T. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1-a · Cited by 3,537
Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans
Nitsche, M. A., & Paulus, W. (2001) · Neurology · doi:10.1212/wnl.57.10.1899 · Cited by 2,617
Klem, G. H., Lüders, H. O., Jasper, H. H., & Elger, C. E. (1999) · PubMed · Cited by 2,361
Huber, R., Felice Ghilardi, M., Massimini, M., & Tononi, G. (2004) · Nature · doi:10.1038/nature02663 · Cited by 1,854
Blaney, P. H. (1986) · Psychological Bulletin · doi:10.1037/0033-2909.99.2.229 · Cited by 1,739
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
Nitsche, M. A., Fricke, K., Henschke, U., Schlitterlau, A., Liebetanz, D., Lang, N., Henning, S. J., Tergau, F., & Paulus, W. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.049916 · Cited by 1,587
Liebetanz, D. (2002) · Brain · doi:10.1093/brain/awf238 · Cited by 1,383
Natural waking and sleep states: a view from inside neocortical neurons
Steriade, M., Timofeev, I., & Grenier, F. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.5.1969 · Cited by 1,296
The role of sleep in learning and memory
Maquet, P. (2001) · Science · doi:10.1126/science.1062856 · Cited by 1,177
Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey
Rockland, K. S., & Pandya, D. Ν. (1979) · Brain Research · doi:10.1016/0006-8993(79)90485-2 · Cited by 1,076
The functional logic of cortical connections
Zeki, S., & Shipp, S. (1988) · Nature · doi:10.1038/335311a0 · Cited by 1,067 · cited 2×
“The most superficial layer I of the neocortex contains distal apical dendrites of deeper laying pyramidal cells and represents the site of synaptic terminations from corticocortical projections (Wong-Riley, 1978; Rockland and Pandya, 1979), especially from higher-order cortical areas (Pandya and Yeterian, 1985; Zeki a…”
BackgroundTurning on and off recurrent balanced cortical activity
Shu, Y., Hasenstaub, A., & McCormick, D. A. (2003) · Nature · doi:10.1038/nature01616 · Cited by 1,054
Coordinated 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
Effects of early and late nocturnal sleep on declarative and procedural memory
Plihal, W., & Born, J. (1997) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1997.9.4.534 · Cited by 1,026
Bindman, L. J., Lippold, O. C. J., & Redfearn, J. W. T. (1964) · The Journal of Physiology · doi:10.1113/jphysiol.1964.sp007425 · Cited by 969
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×
“…hippocampus and its hippocampo–neocortical transfer is presumably linked to a sharp wave–ripple pattern in the hippocampus (Kudrimoti et al., 1999; Nadasdy et al., 1999), which at the neocortical level occurs in temporal correlation to sleep spindles, ␦ waves, and their grouping by the slow…”
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
INTRACELLULAR ACTIVITIES AND EVOKED POTENTIAL CHANGES DURING POLARIZATION OF MOTOR CORTEX.
Purpura, D., & McMurtry, J. G. (1965) · Journal of Neurophysiology · doi:10.1152/jn.1965.28.1.166 · Cited by 875
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-citationNucleus basalis and thalamic control of neocortical activity in the freely moving rat
Buzsaki, G., Bickford, R., Ponomareff, G., Thal, L., Mandel, R., & Gage, F. (1988) · The Journal of Neuroscience · doi:10.1523/jneurosci.08-11-04007.1988 · Cited by 848
Neuromodulation: acetylcholine and memory consolidation
Hasselmo, M. E. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(99)01365-0 · Cited by 809
Sleep, learning, and dreams: off-line memory reprocessing
Stickgold, R., Hobson, J. A., Fosse, R., & Fosse, M. (2001) · Science · doi:10.1126/science.1063530 · Cited by 762
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
Bikson, M., Inoue, M., Akiyama, H., Deans, J. K., Fox, J. E., Miyakawa, H., & Jefferys, J. G. R. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2003.055772 · Cited by 744
Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions
Jefferys, J. G. R. (1995) · Physiological Reviews · doi:10.1152/physrev.1995.75.4.689 · Cited by 684
Neuronal Plasticity in Thalamocortical Networks during Sleep and Waking Oscillations
Steriade, M., & Timofeev, I. (2003) · Neuron · doi:10.1016/s0896-6273(03)00065-5 · Cited by 659
Nitsche, M. A., Liebetanz, D., Antal, A., Lang, N., Tergau, F., & Paulus, W. (2003) · Supplements to Clinical neurophysiology · doi:10.1016/s1567-424x(09)70230-2 · Cited by 613
Sleep-dependent learning: A nap is as good as a night
Mednick, S., Nakayama, K., & Stickgold, R. (2003) · Nature Neuroscience · doi:10.1038/nn1078 · Cited by 594
Architecture and Connections of Cortical Association Areas
Pandya, D. Ν., & Yeterian, E. H. (1985) · Cerebral cortex · doi:10.1007/978-1-4757-9619-3_1 · Cited by 589
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
Early sleep triggers memory for early visual discrimination skills
Gais, S., Plihal, W., Wagner, U., & Born, J. (2000) · Nature Neuroscience · doi:10.1038/81881 · Cited by 558
Influence of transcortical d-c currents on cortical neuronal activity
Creutzfeldt, O. D., Fromm, G. H., & Kapp, H. (1962) · Experimental Neurology · doi:10.1016/0014-4886(62)90056-0 · Cited by 555
Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons
Schiller, J., Schiller, Y., Stuart, G. J., & Sakmann, B. J. (1997) · The Journal of Physiology · doi:10.1111/j.1469-7793.1997.605ba.x · Cited by 528
Priori, A. (2003) · Clinical Neurophysiology · doi:10.1016/s1388-2457(02)00437-6 · Cited by 507
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
A refined model of sleep and the time course of memory formation
Walker, M. P. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000026 · Cited by 481
Steriade, M., Dossi, R. C., & Nunez, A. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-10-03200.1991 · Cited by 480
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
Timofeev, I., Grenier, F., & Steriade, M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.4.1924 · Cited by 455
Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation
Gais, S., & Born, J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0305404101 · Cited by 412
Mood and memory: Evaluating the network theory of affect
Singer, J. A., & Salovey, P. (1988) · Clinical Psychology Review · doi:10.1016/0272-7358(88)90060-8 · Cited by 400
Effects of early and late nocturnal sleep on priming and spatial memory
Plihal, W., & Born, J. (1999) · Psychophysiology · doi:10.1111/1469-8986.3650571 · Cited by 364
Sleep states and memory processes in humans: procedural versus declarative memory systems
Smith, C. (2001) · Sleep Medicine Reviews · doi:10.1053/smrv.2001.0164 · Cited by 355
Bindman, L. J., Lippold, O. C. J., & Redfearn, J. W. T. (1962) · Nature · doi:10.1038/196584a0 · Cited by 315
Kim, H., & Connors, B. W. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-12-05301.1993 · Cited by 305
Brickenkamp, R., & Zilmer, E. (1998) · PsycTESTS Dataset · doi:10.1037/t03299-000 · Cited by 296
Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex
Cauller, L., & Connors, B. W. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00751.1994 · Cited by 250
Maquet, P., Smith, C. T., & Stickgold, R. (2003) · doi:10.1093/acprof:oso/9780198574002.001.0001 · Cited by 241
Shepherd, G. M., Brayton, R. K., Miller, J. P., Segev, I., Rinzel, J., & Rall, W. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.7.2192 · Cited by 220
Amzica, F., Massimini, M., & Manfridi, A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-01042.2002 · Cited by 208
Persistent Cortical Activity: Mechanisms of Generation and Effects on Neuronal Excitability
McCormick, D. A. (2003) · Cerebral Cortex · doi:10.1093/cercor/bhg104 · Cited by 200
Massimini, M., & Amzica, F. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.3.1346 · Cited by 160
Neuronal and Glial Membrane Potentials during Sleep and Paroxysmal Oscillations in the Neocortex
Amzica, F., & Steriade, M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06648.2000 · Cited by 157
A role for dendritic protein synthesis in hippocampal late LTP
Bradshaw, K., Emptage, N., & Bliss, T. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03054.x · Cited by 148
Neurobiology of Sleep and Memory
(1977) · Elsevier eBooks · doi:10.1016/b978-0-12-222350-1.x5001-6 · Cited by 112
GARTSIDE, I. B. (1968) · Nature · doi:10.1038/220382a0 · Cited by 110
Wong‐Riley, M. T. T. (1978) · Brain Research · doi:10.1016/0006-8993(78)90781-3 · Cited by 98
THE EFFECT OF SLEEP ON HUMAN LONG-TERM MEMORY
EKSTRAND, B. R., BARRETT, T. R., WEST, J. N., & MAIER, W. G. (1977) · Neurobiology of Sleep and Memory · doi:10.1016/b978-0-12-222350-1.50029-5 · Cited by 70
Brain polarization: behavioral and therapeutic effects.
Stepke, F. L. (1977) · PubMed · Cited by 68
The Role of Dendritic Filtering in Associative Long-Term Synaptic PlasticityPreprint
Sourdet, V., & Debanne, D. (1999) · Learning & Memory · doi:10.1101/lm.6.5.422 · 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
Scalp recorded direct current brain potentials during human sleep
Marshall, L., Mölle, M., Fehm, H. L., & Jan Born, A. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00131.x · Cited by 55
Self-citationOff-Line Reprocessing of Recent Memory and its Role in Memory Consolidation: A Progress Report
McNaughton, B. L., Barnes, C. A., Battaglia, F. P., Bower, M. R., Cowen, S. L., Ekstrom, A. D., Gerrard, J. L., Hoffman, K. L., Houston, F. P., Karten, Y. J. G., et al. (2003) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198574002.003.0013 · Cited by 53
Dynamic depolarization fields in the cerebral cortex
Roland, P. E. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)02125-1 · Cited by 47
Marshall, L., Mölle, M., & Jan Born, A. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00458-5 · Cited by 37
Self-citationRoles of Early and Late Nocturnal Sleep for the Consolidation of Human Memories
Jan Born, A., & Gais, S. (2003) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198574002.003.0004 · Cited by 18
Islam, N., Moriwaki, A., Hattori, Y., & Hori, Y. (1994) · Neuroscience Research · doi:10.1016/0168-0102(94)90159-7 · Cited by 14
Safety Assessment of NMR Clinical Equipment
Schmidt, K. (1987) · Cited by 11
Islam, N., Moriwaki, A., & Hori, Y. (1995) · PubMed · Cited by 9
Research works printed but not linked: 7
- 1991, Cereb Cortex, 1, 1
- 1995, Indian J Physiol Pharmacol, 39, 209
- 1958, Electroencephalogr Clin Neurophysiol, 10, 371
- 1977, Biol Psychiatry, 12, 37
- 10.1017/S0048577299971536 · DOI · Paper page
- 10.1073/pnas.041430398 · DOI
- 1998, J Pers Soc Psychol, 54, 1063
Cited by
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Transcranial direct current stimulation: State of the art 2008
Nitsche, M. A., Cohen, L. G., Wassermann, E. M., Priori, A., Lang, N., Antal, A., Paulus, W., Hummel, F., Boggio, P. S., Fregni, F., et al. (2008) · Brain Stimulation · doi:10.1016/j.brs.2008.06.004 · Cited by 3,057
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783
“Spindles are also present during SWS and superimposed on delta activity, and then form less clearly discrete spindles (38, 53, 303, 426, 440, 442, 785, 1083, 1221, 1355).”
BackgroundMethodEvidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS)
Lefaucheur, J., Antal, A., Ayache, S. S., Benninger, D. H., Brunelin, J., Cogiamanian, F. M., Cotelli, M., Ridder, D. D., Ferrucci, R., Langguth, B., et al. (2016) · Clinical Neurophysiology · doi:10.1016/j.clinph.2016.10.087 · Cited by 1,968
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-citationBrunoni, A. R., Nitsche, M. A., Bolognini, N., Bikson, M., Wagner, T., Merabet, L., Edwards, D. J., Valero-Cabre, A., Rotenberg, A., Pascual-Leone, A., et al. (2012) · Brain stimulation · doi:10.1016/j.brs.2011.03.002 · Cited by 1,445
Metadata
- Authors
- Marshall, L., Mölle, M., Hallschmid, M., & Born, J.
- Affiliations
- University of Lübeck (DE)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2004-11-03
- Volume
- 24
- Issue
- 44
- Pages
- 9985-9992
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6730231
- OpenAlex
- W2097201141
- Cited by
- 548
- References
- 75
- Citations by year
- 2026: 10 · 2025: 12 · 2024: 20 · 2023: 19 · 2022: 18 · 2021: 28 · 2020: 38 · 2019: 35 · 2018: 30 · 2017: 37 · 2016: 37 · 2015: 34 · 2014: 45 · 2013: 32 · 2012: 41
- FWCI
- 6.60
- 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
- Deutsche Forschungsgemeinschaft (MA 2053, BO 854)
- Topics
- Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- transcranial direct current stimulation, sleep, slow-wave sleep, declarative memory, memory consolidation, anodal tDCS, slow oscillations, procedural memory, mirror tracing, mood, sleep depth, neuroplasticity
- MeSH terms
- Adult, Brain, Cerebral Cortex, Double-Blind Method, Electric Stimulation, Electroencephalography, Humans, Male, Memory, Paired-Associate Learning, Mental Recall, Sleep, Sleep Stages, Wakefulness, Polysomnography, Cross-Over Studies
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