Abstract
During the last decade the interest in the manipulation of learning and memory by non-invasive techniques in humans has increased dramatically. Many studies focus on sleep as a beneficial or even necessary state for the consolidation of many types of memories. For manipulation methods of transcranial electric stimulation, TMS, deep brain stimulation, cued reactivation, sensory stimulation, especially auditory stimulation have been employed. Techniques closely comparable to the non-invasive human methods have also been developed in rodents. In addition optogenetic tools have enabled the functional causality of very specific pathways to be investigated in a complimentary way. This chapter focuses on effects induced by weak electric stimulation on consolidation during sleep but includes also manipulations aside from weak electric stimulation in a complimentary fashion. As of recent the variability in the efficiency of weak electric stimulation has come into the spotlight. Specifically, the relevance not only of the technical parameters of stimulation, but also of the electrophysiologically defined ‘brain state’ at the time of stimulation, as well as cognitive features of the individual per se have been addressed.
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References
Albouy G, Sterpenich V, Vandewalle G, Darsaud A, Gais S, Rauchs G, Desseilles M, Boly M, Dang-Vu T, Balteau E, Degueldre C, Phillips C, Luxen A, Maquet P (2013) Interaction between hippocampal and striatal systems predicts subsequent consolidation of motor sequence memory. PLoS ONE 8:e59490
Ali MM, Sellers KK, Frohlich F (2013) Transcranial alternating current stimulation modulates large-scale cortical network activity by network resonance. J Neurosci: Official J Soc Neurosci 33:11262–11275
Anastassiou CA, Perin R, Markram H, Koch C (2011) Ephaptic coupling of cortical neurons. Nat Neurosci 14:217–223
Barham MP, Enticott PG, Conduit R, Lum JA (2016) Transcranial electrical stimulation during sleep enhances declarative (but not procedural) memory consolidation: evidence from a meta-analysis. Neurosci Biobehav Rev 63:65–77
Batsikadze G, Moliadze V, Paulus W, Kuo MF, Nitsche MA (2013) Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans. J Physiol 591:1987–2000
Bergmann TO, Groppa S, Seeger M, Molle M, Marshall L, Siebner HR (2009) Acute changes in motor cortical excitability during slow oscillatory and constant anodal transcranial direct current stimulation. J Neurophysiol 102:2303–2311
Berryhill ME, Peterson DJ, Jones KT, Stephens JA (2014) Hits and misses: leveraging tDCS to advance cognitive research. Front Psychol 5:800
Binder S, Rawohl J, Born J, Marshall L (2014a) Transcranial slow oscillation stimulation during NREM sleep enhances acquisition of the radial maze task and modulates cortical network activity in rats. Front Behav Neurosci 7:220
Binder S, Berg K, Gasca F, Lafon B, Parra LC, Born J, Marshall L (2014b) Transcranial slow oscillation stimulation during sleep enhances memory consolidation in rats. Brain stimulation 7:508–515
Boyce R, Glasgow SD, Williams S, Adamantidis A (2016) Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation. Science (New York, NY) 352:812–816
Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science (New York, NY) 313:1626–1628
Datta A, Bansal V, Diaz J, Patel J, Reato D, Bikson M (2009) Gyri-precise head model of transcranial direct current stimulation: improved spatial focality using a ring electrode versus conventional rectangular pad. Brain stimulation 2:201–207
David F, Schmiedt JT, Taylor HL, Orban G, Di Giovanni G, Uebele VN, Renger JJ, Lambert RC, Leresche N, Crunelli V (2013) Essential thalamic contribution to slow waves of natural sleep. J Neurosci: Official J Soc Neurosci 33:19599–19610
de Souza Custodio JC, Martins CW, Lugon MD, Fregni F, Nakamura-Palacios EM (2013) Epidural direct current stimulation over the left medial prefrontal cortex facilitates spatial working memory performance in rats. Brain Stimulation 6:261–269
Del Felice A, Magalini A, Masiero S (2015) Slow-oscillatory transcranial direct current stimulation modulates memory in temporal lobe epilepsy by altering sleep spindle generators: a possible rehabilitation tool. Brain stimulation 8:567–573
Dockery CA, Liebetanz D, Birbaumer N, Malinowska M, Wesierska MJ (2011) Cumulative benefits of frontal transcranial direct current stimulation on visuospatial working memory training and skill learning in rats. Neurobiol Learn Mem 96:452–460
Edwards D, Cortes M, Datta A, Minhas P, Wassermann EM, Bikson M (2013) Physiological and modeling evidence for focal transcranial electrical brain stimulation in humans: a basis for high-definition tDCS. NeuroImage 74:266–275
Euston DR, Gruber AJ, McNaughton BL (2012) The role of medial prefrontal cortex in memory and decision making. Neuron 76:1057–1070
Ferrucci R, Brunoni AR, Parazzini M, Vergari M, Rossi E, Fumagalli M, Mameli F, Rosa M, Giannicola G, Zago S, Priori A (2013) Modulating human procedural learning by cerebellar transcranial direct current stimulation. Cerebellum (London, England) 12:485–492
Filmer HL, Dux PE, Mattingley JB (2014) Applications of transcranial direct current stimulation for understanding brain function. Trends Neurosci 37:742–753
Fritsch B, Reis J, Martinowich K, Schambra HM, Ji Y, Cohen LG, Lu B (2010) Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 66:198–204
Frohlich F (2015) Experiments and models of cortical oscillations as a target for noninvasive brain stimulation. Prog Brain Res 222:41–73
Frohlich F, McCormick DA (2010) Endogenous electric fields may guide neocortical network activity. Neuron 67:129–143
Garside P, Arizpe J, Lau CI, Goh C, Walsh V (2015) Cross-hemispheric alternating current stimulation during a nap disrupts slow wave activity and associated memory consolidation. Brain stimulation 8:520–527
Gasca F, Marshall L, Binder S, Schlaefer A, Hofmann UG, Schweikard A (2011) Finite element simulation of transcranial current stimulation in realistic rat head model. Neural Eng 3
Greenberg A, Whitten TA, Dickson CT (2016) Stimulating forebrain communications: Slow sinusoidal electric fields over frontal cortices dynamically modulate hippocampal activity and cortico-hippocampal interplay during slow-wave states. NeuroImage 133:189–206
Helfrich RF, Schneider TR, Rach S, Trautmann-Lengsfeld SA, Engel AK, Herrmann CS (2014) Entrainment of brain oscillations by transcranial alternating current stimulation. Curr Biol: CB 24:333–339
Herrmann CS, Rach S, Neuling T, Struber D (2013) Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes. Front Human Neurosci 7:279
Jefferys JG (1995) Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol Rev 75:689–723
Kanai R, Chaieb L, Antal A, Walsh V, Paulus W (2008) Frequency-dependent electrical stimulation of the visual cortex. Curr Biol: CB 18:1839–1843
Kim A, Latchoumane C, Lee S, Kim GB, Cheong E, Augustine GJ, Shin HS (2012) Optogenetically induced sleep spindle rhythms alter sleep architectures in mice. Proc Natl Acad Sci USA 109:20673–20678
Kirov R, Weiss C, Siebner HR, Born J, Marshall L (2009) Slow oscillation electrical brain stimulation during waking promotes EEG theta activity and memory encoding. Proc Natl Acad Sci USA 106:15460–15465
Kuki T, Ohshiro T, Ito S, Ji ZG, Fukazawa Y, Matsuzaka Y, Yawo H, Mushiake H (2013) Frequency-dependent entrainment of neocortical slow oscillation to repeated optogenetic stimulation in the anesthetized rat. Neurosci Res 75:35–45
Leffa DT, de Souza A, Scarabelot VL, Medeiros LF, de Oliveira C, Grevet EH, Caumo W, de Souza DO, Rohde LA, Torres IL (2016) Transcranial direct current stimulation improves short-term memory in an animal model of attention-deficit/hyperactivity disorder. Eur Neuropsychopharmacol 26:368–377
Li LM, Uehara K, Hanakawa T (2015) The contribution of interindividual factors to variability of response in transcranial direct current stimulation studies. Front Cell Neurosci 9:181
Liebetanz D, Koch R, Mayenfels S, Konig F, Paulus W, Nitsche MA (2009) Safety limits of cathodal transcranial direct current stimulation in rats. Clin Neurophysiol: Official J Int Fed Clin Neurophysiol 120:1161–1167
Lustenberger C, Boyle MR, Sankaraleengam A, Mellin J, Vaughn B, Flavio F (2016) Feedback-controlled transcranial alternating current stimulation reveals a functional role of sleep spindles in motor consolidation. Current Biology 26(16): 2127–2136
Marshall L, Born J (2011) Brain Stimulation During Sleep. Sleep Med Clin 6:10
Marshall L, Binder S (2013) Contribution of transcranial oscillatory stimulation to research on neural networks: an emphasis on hippocampo-neocortical rhythms. Front Human Neurosci 7:614
Marshall L, Mölle M, Hallschmid M, Born J (2004) Transcranial direct current stimulation during sleep improves declarative memory. J Neurosci: Official J Soc Neurosci 24:9985–9992
Marshall L, Helgadottir H, Mölle M, Born J (2006) Boosting slow oscillations during sleep potentiates memory. Nature 444:610–613
Marshall L, Kirov R, Brade J, Mölle M, Born J (2011) Transcranial electrical currents to probe EEG brain rhythms and memory consolidation during sleep in humans. PLoS ONE 6:e16905
Miranda PC, Lomarev M, Hallett M (2006) Modeling the current distribution during transcranial direct current stimulation. Clin Neurophysiol: Official J Int Fed Clin Neurophysiol 117:1623–1629
Monai H, Ohkura M, Tanaka M, Oe Y, Konno A, Hirai H, Mikoshiba K, Itohara S, Nakai J, Iwai Y, Hirase H (2016) Calcium imaging reveals glial involvement in transcranial direct current stimulation-induced plasticity in mouse brain. Nat Commun 7:11100
Monte-Silva K, Kuo MF, Hessenthaler S, Fresnoza S, Liebetanz D, Paulus W, Nitsche MA (2013) Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain stimulation 6:424–432
Munz MT, Prehn-Kristensen A, Thielking F, Mölle M, Goder R, Baving L (2015) Slow oscillating transcranial direct current stimulation during non-rapid eye movement sleep improves behavioral inhibition in attention-deficit/hyperactivity disorder. Front Cell Neurosci 9:307
Nettersheim A, Hallschmid M, Born J, Diekelmann S (2015) The role of sleep in motor sequence consolidation: stabilization rather than enhancement. J Neurosci: Official J Soc Neurosci 35:6696–6702
Neuling T, Wagner S, Wolters CH, Zaehle T, Herrmann CS (2012) Finite-element model predicts current density distribution for clinical applications of tDCS and tACS. Front psychiatry 3:83
Niknazar M, Krishnan GP, Bazhenov M, Mednick SC (2015) Coupling of thalamocortical sleep oscillations are important for memory consolidation in humans. PLoS ONE 10:e0144720
Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Paulus W, Hummel F, Boggio PS, Fregni F, Pascual-Leone A (2008) Transcranial direct current stimulation: state of the art 2008. Brain stimulation 1:206–223
Nitsche MA, Jakoubkova M, Thirugnanasambandam N, Schmalfuss L, Hullemann S, Sonka K, Paulus W, Trenkwalder C, Happe S (2010) Contribution of the premotor cortex to consolidation of motor sequence learning in humans during sleep. J Neurophysiol 104:2603–2614
Ozen S, Sirota A, Belluscio MA, Anastassiou CA, Stark E, Koch C, Buzsáki G (2010) Transcranial electric stimulation entrains cortical neuronal populations in rats. The Journal of neuroscience: the official journal of the Society for Neuroscience 30:11476–11485
Pelletier SJ, Cicchetti F (2015) Cellular and molecular mechanisms of action of transcranial direct current stimulation: evidence from in vitro and in vivo models. Int J Neuropsychopharmacol 18
Pennartz CM, Lee E, Verheul J, Lipa P, Barnes CA, McNaughton BL (2004) The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples. The Journal of neuroscience: the official journal of the Society for Neuroscience 24:6446–6456
Pereira de Vasconcelos A, Cassel JC (2015) The nonspecific thalamus: A place in a wedding bed for making memories last? Neurosci Biobehav Rev 54:175–196
Prehn-Kristensen A, Munz M, Goder R, Wilhelm I, Korr K, Vahl W, Wiesner CD, Baving L (2014) Transcranial oscillatory direct current stimulation during sleep improves declarative memory consolidation in children with attention-deficit/hyperactivity disorder to a level comparable to healthy controls. Brain stimulation 7:793–799
Priori A (2003) Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability. Clin Neurophysiol: Official J Int Fed Clin Neurophysiol 114:589–595
Radman T, Ramos RL, Brumberg JC, Bikson M (2009) Role of cortical cell type and morphology in subthreshold and suprathreshold uniform electric field stimulation in vitro. Brain stimulation 2:215–228
Rasch B, Born J (2013) About sleep’s role in memory. Physiol Rev 93:681–766
Rolls A, Colas D, Adamantidis A, Carter M, Lanre-Amos T, Heller HC, de Lecea L (2011) Optogenetic disruption of sleep continuity impairs memory consolidation. Proc Natl Acad Sci USA 108:13305–13310
Savic B, Meier B (2016) How transcranial direct current stimulation can modulate implicit motor sequence learning and consolidation: a brief review. Front Human Neurosci 10:26
Stagg CJ, Best JG, Stephenson MC, O’Shea J, Wylezinska M, Kincses ZT, Morris PG, Matthews PM, Johansen-Berg H (2009) Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J Neurosci: Official J Soc Neurosci 29:5202–5206
Stagg CJ, Lin RL, Mezue M, Segerdahl A, Kong Y, Xie J, Tracey I (2013) Widespread modulation of cerebral perfusion induced during and after transcranial direct current stimulation applied to the left dorsolateral prefrontal cortex. J Neurosci: Official J Soc Neurosci 33:11425–11431
Struber D, Rach S, Neuling T, Herrmann CS (2015) On the possible role of stimulation duration for after-effects of transcranial alternating current stimulation. Front Cell Neurosci 9:311
Tecchio F, Zappasodi F, Assenza G, Tombini M, Vollaro S, Barbati G, Rossini PM (2010) Anodal transcranial direct current stimulation enhances procedural consolidation. J Neurophysiol 104:1134–1140
Vossen A, Gross J, Thut G (2015) Alpha power increase after transcranial alternating current stimulation at alpha frequency (alpha-tACS) reflects plastic changes rather than entrainment. Brain stimulation 8:499–508
Wagner T, Fregni F, Fecteau S, Grodzinsky A, Zahn M, Pascual-Leone A (2007) Transcranial direct current stimulation: a computer-based human model study. NeuroImage 35:1113–1124
Wagner S, Rampersad SM, Aydin U, Vorwerk J, Oostendorp TF, Neuling T, Herrmann CS, Stegeman DF, Wolters CH (2014) Investigation of tDCS volume conduction effects in a highly realistic head model. J Neural Eng 11:016002
Weiss SA, Faber DS (2010) Field effects in the CNS play functional roles. Front Neural Circ 4:15
Westerberg CE, Florczak SM, Weintraub S, Mesulam MM, Marshall L, Zee PC, Paller KA (2015) Memory improvement via slow-oscillatory stimulation during sleep in older adults. Neurobiol Aging 36:2577–2586
Woods AJ, Antal A, Bikson M, Boggio PS, Brunoni AR, Celnik P, Cohen LG, Fregni F, Herrmann CS, Kappenman ES, Knotkova H, Liebetanz D, Miniussi C, Miranda PC, Paulus W, Priori A, Reato D, Stagg C, Wenderoth N, Nitsche MA (2016) A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin Neurophysiol: Official J Int Fed Clin Neurophysiol 127:1031–1048
Acknowledgements
This work was funded by the Deutsche Forschungsgemeinschaft (TR/SFB 654 and SPP1665), and NIH/NSF/BMBF/CRCNS: US-German Collaboration in Computational Neuroscience (German Ministry of Education and Research BMBF, grant 01GQ1008).
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Campos-Beltrán, D., Marshall, L. (2017). Electric Stimulation to Improve Memory Consolidation During Sleep. In: Axmacher, N., Rasch, B. (eds) Cognitive Neuroscience of Memory Consolidation. Studies in Neuroscience, Psychology and Behavioral Economics. Springer, Cham. https://doi.org/10.1007/978-3-319-45066-7_18
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