Current challenges: the ups and downs of tACS
Abstract
The non-invasive delivery of electric currents through the scalp (transcranial electrical stimulation) is a popular tool for neuromodulation, mostly due to its highly adaptable nature (waveform, montage) and tolerability at low intensities (< 2 mA). Applied rhythmically, transcranial alternating current stimulation (tACS) may entrain neural oscillations in a frequency- and phase-specific manner, providing a causal perspective on brain–behaviour relationships. While the past decade has seen many behavioural and electrophysiological effects of tACS that suggest entrainment-mediated effects in the brain, it has been difficult to reconcile such reports with the weak intracranial field strengths (< 1 V/m) achievable at conventional intensities. In this review, we first describe the ongoing challenges faced by users of tACS. We outline the biophysics of electrical brain stimulation and the factors that contribute to the weak field intensities achievable in the brain. Since the applied current predominantly shunts through the scalp—stimulating the nerves that innervate it—the plausibility of transcutaneous (rather than transcranial) effects of tACS is also discussed. In examining the effects of tACS on brain activity, the complex problem of salvaging electrophysiological recordings from artefacts of tACS is described. Nevertheless, these challenges by no means mark the rise and fall of tACS: the second part of this review outlines the recent advancements in the field. We describe some ways in which artefacts of tACS may be better managed using high-frequency protocols, and describe innovative methods for current interactions within the brain that offer either dynamic or more focal current distributions while also minimising transcutaneous effects.
Keywords
Transcranial Stimulation Electric field Oscillation Artefact PhaseNotes
Author contributions
Conceptualisation: NB and MS; formal analysis, investigation, and writing—original draft: NB; writing—review and editing: NB and MS.
Funding
NB and MS were funded by the Office of Naval Research (N62909-17-1-2139).
Compliance with ethical standards
Conflict of interest
The authors state that they have no conflict of interest.
References
- Abd Hamid AI, Gall C, Speck O, Antal A, Sabel BA (2015) Effects of alternating current stimulation on the healthy and diseased brain. Front Neurosci 9:391PubMedPubMedCentralGoogle Scholar
- Alagapan S, Schmidt SL, Lefebvre J, Hadar E, Shin HW, Frӧhlich F (2016) Modulation of cortical oscillations by low-frequency direct cortical stimulation is state- dependent. PLoS Biol 14(3):e1002424PubMedPubMedCentralGoogle Scholar
- Alekseichuk I, Falchier AY, Linn G, Xu T, Milham MP, Schroeder CE, Opitz A (2019a) Electric field dynamics in the brain during multi-electrode transcranial electric stimulation. Nat Commun 10(1):2573PubMedPubMedCentralGoogle Scholar
- Alekseichuk I, Mantell K, Shirinpour S, Opitz A (2019b) Comparative modeling of transcranial magnetic and electric stimulation in mouse, monkey, and human. NeuroImage 194:136–148PubMedGoogle Scholar
- Ali MM, Sellers KK, Fröhlich F (2013) Transcranial alternating current stimulation modulates large-scale cortical network activity by network resonance. J Neurosci 33(27):11262–11275PubMedPubMedCentralGoogle Scholar
- Anastassiou CA, Montgomery SM, Barahona M, Buzsáki G, Koch C (2010) The effect of spatially inhomogeneous extracellular electric fields on neurons. J Neurosci 30(5):1925–1936PubMedPubMedCentralGoogle Scholar
- Anastassiou CA, Perin R, Markram H, Koch C (2011) Ephaptic coupling of cortical neurons. Nat Neurosci 14(2):217–224PubMedGoogle Scholar
- Antal A, Herrmann CS (2016) Transcranial alternating current and random noise stimulation: possible mechanisms. Neural Plast. https://doi.org/10.1155/2016/3616807 CrossRefPubMedPubMedCentralGoogle Scholar
- Antal A, Paulus W (2013) Transcranial alternating current stimulation (tACS). Front Hum Neurosci 7:317PubMedPubMedCentralGoogle Scholar
- Asamoah B, Khatoun A, McLaughlin M (2019a) tACS motor system effects can be caused by transcutaneous stimulation of peripheral nerves. Nat Commun 10(1):266PubMedPubMedCentralGoogle Scholar
- Asamoah B, Khatoun A, McLaughlin M (2019b) Analytical bias accounts for some of the reported effects of tACS on auditory perception. Brain Stimul 12(4):1001–1009PubMedGoogle Scholar
- Barker AT, Jalinous R, Freeston IL (1985) Non-invasive magnetic stimulation of human motor cortex. Lancet 325(8437):1106–1107Google Scholar
- Başar E, Schmiedt-Fehr C, Mathes B, Femir B, Emek-Savaş DD, Tülay E, Yener G (2016) What does the broken brain say to the neuroscientist? Oscillations and connectivity in schizophrenia, Alzheimer’s disease, and bipolar disorder. Int J Psychophysiol 103:135–148PubMedGoogle Scholar
- Bastos AM, Vezoli J, Fries P (2015) Communication through coherence with inter-areal delays. Curr Opin Neurobiol 31:173–180PubMedGoogle Scholar
- 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(7):1987–2000PubMedPubMedCentralGoogle Scholar
- Berényi A, Belluscio M, Mao D, Buzsáki G (2012) Closed-loop control of epilepsy by transcranial electrical stimulation. Science 337(6095):735–737PubMedPubMedCentralGoogle Scholar
- Bergmann TO, Karabanov A, Hartwigsen G, Thielscher A, Siebner HR (2016) Combining non-invasive transcranial brain stimulation with neuroimaging and electrophysiology: Current approaches and future perspectives. NeuroImage 140:4–19PubMedGoogle Scholar
- Bestmann S, Walsh V (2017) Transcranial electrical stimulation. Curr Biol 27(23):R1258–R1262PubMedGoogle Scholar
- Bestmann S, de Berker AO, Bonaiuto J (2015) Understanding the behavioural consequences of noninvasive brain stimulation. TrendsCognit Sci 19(1):13–20Google Scholar
- Bikson M, Inoue M, Akiyama H, Deans JK, Fox JE, Miyakawa H, Jefferys JG (2004) Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro. J Physiol 557(1):175–190PubMedPubMedCentralGoogle Scholar
- Bikson M, Grossman P, Thomas C, Zannou AL, Jiang J, Adnan T, Brunoni AR (2016) Safety of transcranial direct current stimulation: evidence based update 2016. Brain Stimul 9(5):641–661PubMedPubMedCentralGoogle Scholar
- Bikson M, Brunoni AR, Charvet LE, Clark VP, Cohen LG, Deng ZD, Lim KO (2018) Rigor and reproducibility in research with transcranial electrical stimulation: an NIMH-sponsored workshop. Brain Stimul 11(3):465–480PubMedGoogle Scholar
- Bikson M, Esmaeilpour Z, Adair D, Kronberg G, Tyler WJ, Antal A, Edwards D (2019) Transcranial electrical stimulation nomenclature. Brain Stimul. https://doi.org/10.1016/j.brs.2019.07.010 CrossRefPubMedGoogle Scholar
- Bindman LJ, Lippold OCJ, Redfearn JWT (1962) Long-lasting changes in the level of the electrical activity of the cerebral cortex produced by polarizing currents. Nature 196(4854):584–585PubMedGoogle Scholar
- Bindman LJ, Lippold OCJ, Redfearn JWT (1964) The action of brief polarizing currents on the cerebral cortex of the rat (1) during current flow and (2) in the production of long-lasting after-effects. J Physiol 172(3):369–382PubMedPubMedCentralGoogle Scholar
- Bland NS, Mattingley JB, Sale MV (2018) No evidence for phase-specific effects of 40 Hz HD–tACS on multiple object tracking. Front Psychol 9:304PubMedPubMedCentralGoogle Scholar
- Brittain JS, Cagnan H, Mehta AR, Saifee TA, Edwards MJ, Brown P (2015) Distinguishing the central drive to tremor in Parkinson’s disease and essential tremor. J Neurosci 35(2):795–806PubMedPubMedCentralGoogle Scholar
- Brown CC (1975) Electroanesthesia and electrosleep. Am Psychol 30(3):402–410PubMedGoogle Scholar
- Cancelli A, Cottone C, Tecchio F, Truong DQ, Dmochowski J, Bikson M (2016) A simple method for EEG guided transcranial electrical stimulation without models. J Neural Eng 13(3):036022PubMedGoogle Scholar
- Carandini M, Ferster D (2000) Membrane potential and firing rate in cat primary visual cortex. J Neurosci 20(1):470–484PubMedPubMedCentralGoogle Scholar
- Chan CY, Nicholson C (1986) Modulation by applied electric fields of Purkinje and stellate cell activity in the isolated turtle cerebellum. J Physiol 371(1):89–114PubMedPubMedCentralGoogle Scholar
- Chan CY, Hounsgaard J, Nicholson C (1988) Effects of electric fields on transmembrane potential and excitability of turtle cerebellar Purkinje cells in vitro. J Physiol 402(1):751–771PubMedPubMedCentralGoogle Scholar
- Chander BS, Witkowski M, Braun C, Robinson SE, Born J, Cohen LG, Soekadar SR (2016) tACS phase locking of frontal midline theta oscillations disrupts working memory performance. Front Cell Neurosci 10:120PubMedPubMedCentralGoogle Scholar
- Chhatbar PY, Sawers JR, Feng W (2016) Response to the response to “does tDCS actually deliver DC stimulation?”. Brain Stimul Basic Transl Clin Res Neuromodul 9(6):952–954Google Scholar
- Chhatbar PY, Kautz SA, Takacs I, Rowland NC, Revuelta GJ, George MS, Feng W (2018) Evidence of transcranial direct current stimulation-generated electric fields at subthalamic level in human brain in vivo. Brain Stimul 11:727–733PubMedPubMedCentralGoogle Scholar
- Creutzfeldt OD, Fromm GH, Kapp H (1962) Influence of transcortical DC currents on cortical neuronal activity. Exp Neurol 5(6):436–452PubMedGoogle Scholar
- 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 Stimul 2(4):201–207PubMedPubMedCentralGoogle Scholar
- Datta A, Dmochowski JP, Guleyupoglu B, Bikson M, Fregni F (2013) Cranial electrotherapy stimulation and transcranial pulsed current stimulation: a computer based high-resolution modeling study. NeuroImage 65:280–287PubMedGoogle Scholar
- de Graaf TA, Thomson A, Janssens SE, van Bree S, ten Oever S, Sack AT (2019) Does alpha phase modulate visual target detection? Three experiments with tACS phase-based stimulus presentation. bioRxiv 675264. https://doi.org/10.1101/675264
- Deans JK, Powell AD, Jefferys JG (2007) Sensitivity of coherent oscillations in rat hippocampus to AC electric fields. J Physiol 583(2):555–565PubMedPubMedCentralGoogle Scholar
- DeSantana JM, Walsh DM, Vance C, Rakel BA, Sluka KA (2008) Effectiveness of transcutaneous electrical nerve stimulation for treatment of hyperalgesia and pain. Curr Rheumatol Rep 10(6):492–499PubMedPubMedCentralGoogle Scholar
- Dmochowski JP, Datta A, Bikson M, Su Y, Parra LC (2011) Optimized multi-electrode stimulation increases focality and intensity at target. J Neural Eng 8(4):046011PubMedGoogle Scholar
- Dowsett J, Herrmann CS (2016) Transcranial alternating current stimulation with sawtooth waves: simultaneous stimulation and EEG recording. Front Hum Neurosci 10:135PubMedPubMedCentralGoogle Scholar
- 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 74:266–275PubMedPubMedCentralGoogle Scholar
- Esmaeilpour Z, Schestatsky P, Bikson M, Brunoni AR, Pellegrinelli A, Piovesan FX, Fregni F (2017) Notes on human trials of transcranial direct current stimulation between 1960 and 1998. Front Hum Neurosci 11:71PubMedPubMedCentralGoogle Scholar
- Faria P, Hallett M, Miranda PC (2011) A finite element analysis of the effect of electrode area and inter-electrode distance on the spatial distribution of the current density in tDCS. J Neural Eng 8(6):066017PubMedPubMedCentralGoogle Scholar
- Fertonani A, Miniussi C (2017) Transcranial electrical stimulation: what we know and do not know about mechanisms. Neuroscientist 23(2):109–123PubMedGoogle Scholar
- Fertonani A, Ferrari C, Miniussi C (2015) What do you feel if I apply transcranial electric stimulation? Safety, sensations and secondary induced effects. Clin Neurophysiol 126(11):2181–2188PubMedGoogle Scholar
- Fiene M, Schwab BC, Misselhorn J, Herrmann CS, Schneider TR, Engel AK (2019) Phase-specific manipulation of neural oscillations by transcranial alternating current stimulation. bioRxiv 579631. https://doi.org/10.1101/579631
- Filmer HL, Dux PE, Mattingley JB (2014) Applications of transcranial direct current stimulation for understanding brain function. Trends Neurosci 37(12):742–753PubMedGoogle Scholar
- Francis JT, Gluckman BJ, Schiff SJ (2003) Sensitivity of neurons to weak electric fields. J Neurosci 23(19):7255–7261PubMedPubMedCentralGoogle Scholar
- Fries P (2015) Rhythms for cognition: communication through coherence. Neuron 88(1):220–235PubMedPubMedCentralGoogle Scholar
- Fröhlich F, McCormick DA (2010) Endogenous electric fields may guide neocortical network activity. Neuron 67(1):129–143PubMedPubMedCentralGoogle Scholar
- Gartside IB (1968a) Mechanisms of sustained increases of firing rate of neurones in the rat cerebral cortex after polarization: reverberating circuits or modification of synaptic conductance? Nature 220(5165):382–383PubMedGoogle Scholar
- Gartside IB (1968b) Mechanisms of sustained increases of firing rate of neurones in the rat cerebral cortex after polarization: role of protein synthesis. Nature 220(5165):383–384PubMedGoogle Scholar
- Geisler CD, Goldberg JM (1966) A stochastic model of the repetitive activity of neurons. Biophys J 6(1):53–69PubMedPubMedCentralGoogle Scholar
- Goldsworthy MR, Hordacre B (2017) Dose dependency of transcranial direct current stimulation: implications for neuroplasticity induction in health and disease. J Physiol 595(11):3265–3266PubMedPubMedCentralGoogle Scholar
- Grossman N, Bono D, Dedic N, Kodandaramaiah SB, Rudenko A, Suk HJ, Pascual-Leone A (2017) Noninvasive deep brain stimulation via temporally interfering electric fields. Cell 169(6):1029–1041PubMedPubMedCentralGoogle Scholar
- Gundlach C, Müller MM, Nierhaus T, Villringer A, Sehm B (2016) Phasic modulation of human somatosensory perception by transcranially applied oscillating currents. Brain Stimul 9(5):712–719PubMedGoogle Scholar
- Hahn C, Rice J, Macuff S, Minhas P, Rahman A, Bikson M (2013) Methods for extra-low voltage transcranial direct current stimulation: current and time dependent impedance decreases. Clin Neurophysiol 124(3):551–556PubMedGoogle Scholar
- Hanslmayr S, Matuschek J, Fellner MC (2014) Entrainment of prefrontal beta oscillations induces an endogenous echo and impairs memory formation. Curr Biol 24(8):904–909PubMedGoogle Scholar
- Helfrich RF, Knepper H, Nolte G, Strüber D, Rach S, Herrmann CS, Engel AK (2014a) Selective modulation of interhemispheric functional connectivity by HD–tACS shapes perception. PLoS Biol 12(12):e1002031PubMedPubMedCentralGoogle Scholar
- Helfrich RF, Schneider TR, Rach S, Trautmann-Lengsfeld SA, Engel AK, Herrmann CS (2014b) Entrainment of brain oscillations by transcranial alternating current stimulation. Curr Biol 24(3):333–339PubMedPubMedCentralGoogle Scholar
- Helfrich RF, Herrmann CS, Engel AK, Schneider TR (2016) Different coupling modes mediate cortical cross-frequency interactions. NeuroImage 140:76–82PubMedGoogle Scholar
- Héroux ME, Loo CK, Taylor JL, Gandevia SC (2017) Questionable science and reproducibility in electrical brain stimulation research. PLoS One 12(4):e0175635PubMedPubMedCentralGoogle Scholar
- Herring JD, Esterer S, Marshall TR, Jensen O, Bergmann TO (2019) Low-frequency alternating current stimulation rhythmically suppresses gamma-band oscillations and impairs perceptual performance. NeuroImage 184:440–449PubMedGoogle Scholar
- Herrmann CS, Strüber D (2017) What can transcranial alternating current stimulation tell us about brain oscillations? Curr Behav Neurosci Rep 4(2):128–137Google Scholar
- Herrmann CS, Strüber D, Helfrich RF, Engel AK (2016) EEG oscillations: from correlation to causality. Int J Psychophysiol 103:12–21PubMedPubMedCentralGoogle Scholar
- Horvath JC, Forte JD, Carter O (2015a) Evidence that transcranial direct current stimulation (tDCS) generates little-to-no reliable neurophysiologic effect beyond MEP amplitude modulation in healthy human subjects: a systematic review. Neuropsychologia 66:213–236PubMedPubMedCentralGoogle Scholar
- Horvath JC, Forte JD, Carter O (2015b) Quantitative review finds no evidence of cognitive effects in healthy populations from single-session transcranial direct current stimulation (tDCS). Brain Stimul 8(3):535–550PubMedPubMedCentralGoogle Scholar
- Huang Y, Parra LC (2019) Can transcranial electric stimulation with multiple electrodes reach deep targets? Brain Stimul 12(1):30–40PubMedGoogle Scholar
- Huang Y, Liu AA, Lafon B, Friedman D, Dayan M, Wang X, Parra LC (2017) Measurements and models of electric fields in the in vivo human brain during transcranial electric stimulation. eLife 6:e18834PubMedPubMedCentralGoogle Scholar
- Jackson MP, Rahman A, Lafon B, Kronberg G, Ling D, Parra LC, Bikson M (2016) Animal models of transcranial direct current stimulation: methods and mechanisms. Clin Neurophysiol 127(11):3425–3454PubMedPubMedCentralGoogle Scholar
- Jacobson GA, Diba K, Yaron-Jakoubovitch A, Oz Y, Koch C, Segev I, Yarom Y (2005) Subthreshold voltage noise of rat neocortical pyramidal neurones. J Physiol 564(1):145–160PubMedPubMedCentralGoogle Scholar
- Jefferys JGR, Deans J, Bikson M, Fox J (2003) Effects of weak electric fields on the activity of neurons and neuronal networks. Radiat Prot Dosimetry 106(4):321–323PubMedGoogle Scholar
- Kanai R, Chaieb L, Antal A, Walsh V, Paulus W (2008) Frequency-dependent electrical stimulation of the visual cortex. Curr Biol 18(23):1839–1843PubMedGoogle Scholar
- Kar K, Krekelberg B (2012) Transcranial electrical stimulation over visual cortex evokes phosphenes with a retinal origin. J Neurophysiol 108(8):2173–2178PubMedPubMedCentralGoogle Scholar
- Karabanov AN, Saturnino GB, Thielscher A, Siebner HR (2019) Can transcranial electrical stimulation localize brain function? Front Psychol 10:213PubMedPubMedCentralGoogle Scholar
- Kasten FH, Herrmann CS (2019) Recovering brain dynamics during concurrent tACS-M/EEG: an overview of analysis approaches and their methodological and interpretational pitfalls. Brain Topogr. https://doi.org/10.1007/s10548-019-00727-7 CrossRefPubMedPubMedCentralGoogle Scholar
- Kasten FH, Negahbani E, Fröhlich F, Herrmann CS (2018) Non-linear transfer characteristics of stimulation and recording hardware account for spurious low-frequency artifacts during amplitude modulated transcranial alternating current stimulation (AM-tACS). NeuroImage 179:134–143PubMedGoogle Scholar
- Kavirajan HC, Lueck K, Chuang K (2014) Alternating current cranial electrotherapy stimulation (CES) for depression. Cochrane Database Syst Rev 7:Article CD010521Google Scholar
- Khatoun A, Breukers J, de Beeck SO, Nica IG, Aerts JM, Seynaeve L, Mc Laughlin M (2018) Using high-amplitude and focused transcranial alternating current stimulation to entrain physiological tremor. Sci Rep 8(1):4927PubMedPubMedCentralGoogle Scholar
- Kim JH, Kim DW, Chang WH, Kim YH, Kim K, Im CH (2014) Inconsistent outcomes of transcranial direct current stimulation may originate from anatomical differences among individuals: electric field simulation using individual MRI data. Neurosci Lett 564:6–10PubMedGoogle Scholar
- Krause MR, Zanos TP, Csorba BA, Pilly PK, Choe J, Phillips ME, Pack CC (2017) Transcranial direct current stimulation facilitates associative learning and alters functional connectivity in the primate brain. Curr Biol 27(20):3086–3096PubMedGoogle Scholar
- Krause MR, Vieira PG, Csorba BA, Pilly PK, Pack CC (2019) Transcranial alternating current stimulation entrains single-neuron activity in the primate brain. Proc Natl Acad Sci 116(12):5747–5755PubMedGoogle Scholar
- Kwan A, Forbes PA, Mitchell DE, Blouin JS, Cullen KE (2019) Neural substrates, dynamics and thresholds of galvanic vestibular stimulation in the behaving primate. Nat Commun 10(1):1904PubMedPubMedCentralGoogle Scholar
- Laakso I, Hirata A (2013) Computational analysis shows why transcranial alternating current stimulation induces retinal phosphenes. J Neural Eng 10(4):046009PubMedGoogle Scholar
- Lafon B, Henin S, Huang Y, Friedman D, Melloni L, Thesen T, Liu A (2017) Low frequency transcranial electrical stimulation does not entrain sleep rhythms measured by human intracranial recordings. Nat Commun 8(1):1199PubMedPubMedCentralGoogle Scholar
- Lefaucheur JP, André-Obadia N, Antal A, Ayache SS, Baeken C, Benninger DH, Devanne H (2014) Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol 125(11):2150–2206PubMedGoogle Scholar
- Liu A, Vöröslakos M, Kronberg G, Henin S, Krause MR, Huang Y, Berényi A (2018) Immediate neurophysiological effects of transcranial electrical stimulation. Nat Commun 9(1):5092PubMedPubMedCentralGoogle Scholar
- Mäkelä N, Sarvas J, Ilmoniemi RJ (2017) A simple reason why beamformer may (not) remove the tACS-induced artifact in MEG. Brain Stimul 10(4):e66–e67Google Scholar
- Marino M, Liu Q, Del Castello M, Corsi C, Wenderoth N, Mantini D (2018a) Heart–Brain interactions in the MR environment: characterization of the ballistocardiogram in EEG signals collected during simultaneous fMRI. Brain Topogr 31(3):337–345PubMedGoogle Scholar
- Marino M, Liu Q, Koudelka V, Porcaro C, Hlinka J, Wenderoth N, Mantini D (2018b) Adaptive optimal basis set for BCG artifact removal in simultaneous EEG-fMRI. Sci Rep 8(1):8902PubMedPubMedCentralGoogle Scholar
- Marshall L, Helgadóttir H, Mölle M, Born J (2006) Boosting slow oscillations during sleep potentiates memory. Nature 444(7119):610–613PubMedGoogle Scholar
- Marshall TR, Esterer S, Herring JD, Bergmann TO, Jensen O (2016) On the relationship between cortical excitability and visual oscillatory responses—a concurrent tDCS–MEG study. NeuroImage 140:41–49PubMedGoogle Scholar
- Matsumoto H, Ugawa Y (2017) Adverse events of tDCS and tACS: a review. Clin Neurophysiol Pract 2:19–25PubMedGoogle Scholar
- Mehta AR, Brittain JS, Brown P (2014) The selective influence of rhythmic cortical versus cerebellar transcranial stimulation on human physiological tremor. J Neurosci 34(22):7501–7508PubMedPubMedCentralGoogle Scholar
- Mehta AR, Pogosyan A, Brown P, Brittain JS (2015) Montage matters: the influence of transcranial alternating current stimulation on human physiological tremor. Brain Stimul 8(2):260–268PubMedPubMedCentralGoogle Scholar
- Merton PA, Morton HB (1980) Stimulation of the cerebral cortex in the intact human subject. Nature 285(5762):227PubMedGoogle Scholar
- Minami S, Amano K (2017) Illusory jitter perceived at the frequency of alpha oscillations. Curr Biol 27(15):2344–2351PubMedPubMedCentralGoogle Scholar
- Miranda PC, Lomarev M, Hallett M (2006) Modeling the current distribution during transcranial direct current stimulation. Clin Neurophysiol 117(7):1623–1629PubMedGoogle Scholar
- Miranda PC, Mekonnen A, Salvador R, Ruffini G (2013) The electric field in the cortex during transcranial current stimulation. NeuroImage 70:48–58PubMedGoogle Scholar
- Miyaguchi S, Otsuru N, Kojima S, Yokota H, Saito K, Inukai Y, Onishi H (2019) Gamma tACS over M1 and cerebellar hemisphere improves motor performance in a phase-specific manner. Neurosci Lett 694:64–68PubMedGoogle Scholar
- Modolo J, Denoyer Y, Wendling F, Benquet P (2018) Physiological effects of low-magnitude electric fields on brain activity: advances from in vitro, in vivo and in silico models. Curr Opin Biomed Eng 8:38–44PubMedGoogle Scholar
- Monai H, Hirase H (2018) Astrocytes as a target of transcranial direct current stimulation (tDCS) to treat depression. Neurosci Res 126:15–21PubMedGoogle Scholar
- Negahbani E, Kasten FH, Herrmann CS, Fröhlich F (2018) Targeting alpha-band oscillations in a cortical model with amplitude-modulated high-frequency transcranial electric stimulation. NeuroImage 173:3–12PubMedPubMedCentralGoogle Scholar
- Neuling T, Rach S, Wagner S, Wolters CH, Herrmann CS (2012) Good vibrations: oscillatory phase shapes perception. NeuroImage 63(2):771–778PubMedGoogle Scholar
- Neuling T, Ruhnau P, Weisz N, Herrmann CS, Demarchi G (2017) Faith and oscillations recovered: on analyzing EEG/MEG signals during tACS. NeuroImage 147:960–963PubMedGoogle Scholar
- Nimmrich V, Draguhn A, Axmacher N (2015) Neuronal network oscillations in neurodegenerative diseases. NeuroMol Med 17(3):270–284Google Scholar
- Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527(3):633–639PubMedPubMedCentralGoogle Scholar
- Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57(10):1899–1901PubMedPubMedCentralGoogle Scholar
- Nitsche MA, Nitsche MS, Klein CC, Tergau F, Rothwell JC, Paulus W (2003) Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clin Neurophysiol 114(4):600–604PubMedPubMedCentralGoogle Scholar
- Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Pascual- Leone A (2008) Transcranial direct current stimulation: state of the art 2008. Brain Stimul 1(3):206–223PubMedGoogle Scholar
- Noury N, Siegel M (2017) Phase properties of transcranial electrical stimulation artifacts in electrophysiological recordings. NeuroImage 158:406–416PubMedGoogle Scholar
- Noury N, Siegel M (2018) Analyzing EEG and MEG signals recorded during tES, a reply. NeuroImage 167:53–61PubMedGoogle Scholar
- Noury N, Hipp JF, Siegel M (2016) Physiological processes non-linearly affect electrophysiological recordings during transcranial electric stimulation. NeuroImage 140:99–109PubMedGoogle Scholar
- Opitz A, Paulus W, Will S, Antunes A, Thielscher A (2015) Determinants of the electric field during transcranial direct current stimulation. NeuroImage 109:140–150PubMedGoogle Scholar
- Opitz A, Falchier A, Yan CG, Yeagle EM, Linn GS, Megevand P, Schroeder CE (2016) Spatiotemporal structure of intracranial electric fields induced by transcranial electric stimulation in humans and nonhuman primates. Sci Rep 6:31236PubMedPubMedCentralGoogle Scholar
- Opitz A, Falchier A, Linn GS, Milham MP, Schroeder CE (2017) Limitations of ex vivo measurements for in vivo neuroscience. Proc Natl Acad Sci 114(20):5243–5246PubMedGoogle Scholar
- Ozen S, Sirota A, Belluscio MA, Anastassiou CA, Stark E, Koch C, Buzsáki G (2010) Transcranial electric stimulation entrains cortical neuronal populations in rats. J Neurosci 30(34):11476–11485PubMedPubMedCentralGoogle Scholar
- Payne NA, Prudic J (2009) Electroconvulsive therapy Part I: a perspective on the evolution and current practice of ECT. J Psychiatr Pract 15(5):346–368PubMedPubMedCentralGoogle Scholar
- Plewnia C, Rilk AJ, Soekadar SR, Arfeller C, Huber HS, Sauseng P, Gerloff C (2008) Enhancement of long-range EEG coherence by synchronous bifocal transcranial magnetic stimulation. Eur J Neurosci 27(6):1577–1583PubMedGoogle Scholar
- Polanía R, Nitsche MA, Korman C, Batsikadze G, Paulus W (2012) The importance of timing in segregated theta phase-coupling for cognitive performance. Curr Biol 22(14):1314–1318PubMedGoogle Scholar
- Polanía R, Moisa M, Opitz A, Grueschow M, Ruff CC (2015) The precision of value- based choices depends causally on fronto-parietal phase coupling. Nat Commun 6:8090PubMedPubMedCentralGoogle Scholar
- Polanía R, Nitsche MA, Ruff CC (2018) Studying and modifying brain function with non-invasive brain stimulation. Nat Neurosci 21:174–187PubMedGoogle Scholar
- Poreisz C, Boros K, Antal A, Paulus W (2007) Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Res Bull 72(4–6):208–214PubMedPubMedCentralGoogle Scholar
- Priori A (2003) Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability. Clin Neurophysiol 114(4):589–595PubMedGoogle Scholar
- Purpura DP, McMurtry JG (1965) Intracellular activities and evoked potential changes during polarization of motor cortex. J Neurophysiol 28(1):166–185PubMedGoogle Scholar
- Radman T, Su Y, An JH, Parra LC, Bikson M (2007) Spike timing amplifies the effect of electric fields on neurons: implications for endogenous field effects. J Neurosci 27(11):3030–3036PubMedPubMedCentralGoogle Scholar
- 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 Stimul 2(4):215–228PubMedPubMedCentralGoogle Scholar
- Rahman A, Reato D, Arlotti M, Gasca F, Datta A, Parra LC, Bikson M (2013) Cellular effects of acute direct current stimulation: somatic and synaptic terminal effects. J Physiol 591(10):2563–2578PubMedPubMedCentralGoogle Scholar
- Rawji V, Ciocca M, Zacharia A, Soares D, Truong D, Bikson M, Bestmann S (2018) tDCS changes in motor excitability are specific to orientation of current flow. Brain Stimul 11(2):289–298PubMedPubMedCentralGoogle Scholar
- Reato D, Rahman A, Bikson M, Parra LC (2010) Low-intensity electrical stimulation affects network dynamics by modulating population rate and spike timing. J Neurosci 30(45):15067–15079PubMedPubMedCentralGoogle Scholar
- Reato D, Rahman A, Bikson M, Parra LC (2013) Effects of weak transcranial alternating current stimulation on brain activity—a review of known mechanisms from animal studies. Front Hum Neurosci 7:687PubMedPubMedCentralGoogle Scholar
- Reinhart RM, Nguyen JA (2019) Working memory revived in older adults by synchronizing rhythmic brain circuits. Nat Neurosci 22(5):820–827PubMedPubMedCentralGoogle Scholar
- Riecke L, Formisano E, Herrmann CS, Sack AT (2015a) 4-Hz transcranial alternating current stimulation phase modulates hearing. Brain Stimul 8(4):777–783PubMedGoogle Scholar
- Riecke L, Sack AT, Schroeder CE (2015b) Endogenous delta/theta sound-brain phase entrainment accelerates the buildup of auditory streaming. Curr Biol 25(24):3196–3201PubMedGoogle Scholar
- Ruffini G, Wendling F, Merlet I, Molaee-Ardekani B, Mekonnen A, Salvador R, Miranda PC (2013) Transcranial current brain stimulation (tCS): models and technologies. IEEE Trans Neural Syst Rehabil Eng 21(3):333–345PubMedGoogle Scholar
- Ruhnau P, Neuling T, Fuscá M, Herrmann CS, Demarchi G, Weisz N (2016) Eyes wide shut: transcranial alternating current stimulation drives alpha rhythm in a state dependent manner. Sci Rep 6:27138PubMedPubMedCentralGoogle Scholar
- Ruhnau P, Rufener KS, Heinze HJ, Zaehle T (2018) Sailing in a sea of disbelief: in vivo measurements of transcranial electric stimulation in human subcortical structures. Brain Stimul 11(1):241–243PubMedGoogle Scholar
- Ruohonen J, Karhu J (2012) tDCS possibly stimulates glial cells. Clin Neurophysiol 123(10):2006–2009PubMedGoogle Scholar
- Sadleir RJ, Vannorsdall TD, Schretlen DJ, Gordon B (2010) Transcranial direct current stimulation (tDCS) in a realistic head model. NeuroImage 51(4):1310–1318PubMedGoogle Scholar
- Saturnino GB, Madsen KH, Siebner HR, Thielscher A (2017) How to target inter-regional phase synchronization with dual-site transcranial alternating current stimulation. NeuroImage 163:68–80PubMedGoogle Scholar
- Schutter DJ (2016) Cutaneous retinal activation and neural entrainment in transcranial alternating current stimulation: a systematic review. NeuroImage 140:83–88PubMedGoogle Scholar
- Schutter DJ, Hortensius R (2010) Retinal origin of phosphenes to transcranial alternating current stimulation. Clin Neurophysiol 121(7):1080–1084PubMedGoogle Scholar
- Schutter DJ, Wischnewski M (2016) A meta-analytic study of exogenous oscillatory electric potentials in neuroenhancement. Neuropsychologia 86:110–118PubMedGoogle Scholar
- Schwiedrzik CM (2009) Retina or visual cortex? The site of phosphene induction by transcranial alternating current stimulation. Front Integr Neurosci 3:6PubMedPubMedCentralGoogle Scholar
- Shekelle PG, Cook IA, Miake-Lye IM, Booth MS, Beroes JM, Mak S (2018) Benefits and harms of cranial electrical stimulation for chronic painful conditions, depression, anxiety, and insomnia: a systematic review. Ann Intern Med 168(6):414–421PubMedGoogle Scholar
- Soekadar SR, Herring JD, McGonigle D (2016) Transcranial electric stimulation (tES) and neuroimaging: the state-of-the-art, new insights and prospects in basic and clinical neuroscience. NeuroImage 140:1–3PubMedGoogle Scholar
- Spaak E, de Lange FP, Jensen O (2014) Local entrainment of alpha oscillations by visual stimuli causes cyclic modulation of perception. J Neurosci 34(10):3536–3544PubMedPubMedCentralGoogle Scholar
- Tan J, Iyer KK, Tang AD, Jamil A, Martins RN, Sohrabi HR, Fujiyama H (2018) Modulating functional connectivity with non-invasive brain stimulation for the investigation and alleviation of age-associated declines in response inhibition: a narrative review. NeuroImage 185:490–512PubMedGoogle Scholar
- Terzuolo CA, Bullock TH (1956) Measurement of imposed voltage gradient adequate to modulate neuronal firing. Proc Natl Acad Sci USA 42(9):687–694PubMedGoogle Scholar
- Thut G, Bergmann TO, Fröhlich F, Soekadar SR, Brittain JS, Valero-Cabré A, Herrmann CS (2017) Guiding transcranial brain stimulation by EEG/MEG to interact with ongoing brain activity and associated functions: a position paper. Clin Neurophysiol 128(5):843–857PubMedPubMedCentralGoogle Scholar
- Tseng P, Chang YT, Chang CF, Liang WK, Juan CH (2016) The critical role of phase difference in gamma oscillation within the temporoparietal network for binding visual working memory. Sci Rep 6:32138PubMedPubMedCentralGoogle Scholar
- Veniero D, Vossen A, Gross J, Thut G (2015) Lasting EEG/MEG aftereffects of rhythmic transcranial brain stimulation: level of control over oscillatory network activity. Front Cell Neurosci 9:477PubMedPubMedCentralGoogle Scholar
- Veniero D, Strüber D, Thut G, Herrmann CS (2019) Noninvasive brain stimulation techniques can modulate cognitive processing. Organ Res Methods 22(1):116–147Google Scholar
- Vöröslakos M, Takeuchi Y, Brinyiczki K, Zombori T, Oliva A, Fernández-Ruiz A, Berényi A (2018) Direct effects of transcranial electric stimulation on brain circuits in rats and humans. Nat Commun 9(1):483PubMedPubMedCentralGoogle Scholar
- Vossen A, Gross J, Thut G (2015) Alpha power increase after transcranial alternating current stimulation at alpha frequency (α-tACS) reflects plastic changes rather than entrainment. Brain Stimul 8(3):499–508PubMedPubMedCentralGoogle Scholar
- Vosskuhl J, Strüber D, Herrmann CS (2018) Non-invasive brain stimulation: a paradigm shift in understanding brain oscillations. Front Hum Neurosci 12:211PubMedPubMedCentralGoogle Scholar
- Wagner S, Rampersad SM, Aydin Ü, Vorwerk J, Oostendorp TF, Neuling T, Wolters CH (2013) Investigation of tDCS volume conduction effects in a highly realistic head model. J Neural Eng 11(1):016002PubMedGoogle Scholar
- Widge AS (2018) Cross-species neuromodulation from high-intensity transcranial electrical stimulation. Trends Cognit Sci 22(5):372–374Google Scholar
- Wischnewski M, Schutter DJ (2017) After-effects of transcranial alternating current stimulation on evoked delta and theta power. Clin Neurophysiol 128(11):2227–2232PubMedGoogle Scholar
- Witkowski M, Garcia-Cossio E, Chander BS, Braun C, Birbaumer N, Robinson SE, Soekadar SR (2016) Mapping entrained brain oscillations during transcranial alternating current stimulation (tACS). NeuroImage 140:89–98PubMedGoogle Scholar
- Yavari F, Jamil A, Samani MM, Vidor LP, Nitsche MA (2018) Basic and functional effects of transcranial electrical stimulation (tES)—an introduction. Neurosci Biobehav Rev 85:81–92PubMedGoogle Scholar
- Zaehle T, Rach S, Herrmann CS (2010) Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PLoS One 5(11):e13766PubMedPubMedCentralGoogle Scholar
- Zoefel B, Davis MH, Valente G, Riecke L (2019) How to test for phasic modulation of neural and behavioural responses. NeuroImage 202:116175. https://doi.org/10.1016/j.neuroimage.2019.116175 CrossRefPubMedPubMedCentralGoogle Scholar