10 Minutes Frontal 40 Hz tACS-Effects on Working Memory Tested by Luck-Vogel Task
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
2022
Programme Cooperatio, Third Faculty of Medicine, Charles University in Prague.
PubMed
36661611
PubMed Central
PMC9855106
DOI
10.3390/bs13010039
PII: bs13010039
Knihovny.cz E-resources
- Keywords
- EEG, Luck–Vogel task, coherence, power spectral density, reaction time, transcranial alternating-current stimulation (tACS), working memory,
- Publication type
- Journal Article MeSH
Working memory is a cognitive process that involves short-term active maintenance, flexible updating, and processing of goal- or task-relevant information. All frequency bands are involved in working memory. The activities of the theta and gamma frequency bands in the frontoparietal network are highly involved in working memory processes; theta oscillations play a role in the temporal organization of working memory items, and gamma oscillations influence the maintenance of information in working memory. Transcranial alternating current stimulation (tACS) results in frequency-specific modulation of endogenous oscillations and has shown promising results in cognitive neuroscience. The electrophysiological and behavioral changes induced by the modulation of endogenous gamma frequency in the prefrontal cortex using tACS have not been extensively studied in the context of working memory. Therefore, we aimed to investigate the effects of frontal gamma-tACS on working memory outcomes. We hypothesized that a 10-min gamma tACS administered over the frontal cortex would significantly improve working memory outcomes. Young healthy participants performed Luck-Vogel cognitive behavioral tasks with simultaneous pre- and post-intervention EEG recording (Sham versus 40 Hz tACS). Data from forty-one participants: sham (15 participants) and tACS (26 participants), were used for the statistical and behavioral analysis. The relative changes in behavioral outcomes and EEG due to the intervention were analyzed. The results show that tACS caused an increase in the power spectral density in the high beta and low gamma EEG bands and a decrease in left-right coherence. On the other hand, tACS had no significant effect on success rates and response times. Conclusion: 10 min of frontal 40 Hz tACS was not sufficient to produce detectable behavioral effects on working memory, whereas electrophysiological changes were evident. The limitations of the current stimulation protocol and future directions are discussed in detail in the following sections.
Faculty Hospital Královské Vinohrady 100 00 Prague Czech Republic
Faculty of Biomedical Engineering Czech Technical University 272 01 Kladno Czech Republic
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Başar E. Brain oscillations in neuropsychiatric disease. Dialogues Clin. Neurosci. 2013;15:291–300. doi: 10.31887/DCNS.2013.15.3/ebasar. PubMed DOI PMC
Düzel E., Penny W.D., Burgess N. Brain oscillations and memory. Curr. Opin. Neurobiol. 2010;20:143–149. doi: 10.1016/j.conb.2010.01.004. PubMed DOI
Merker B. Cortical gamma oscillations: The functional key is activation, not cognition. Neurosci. Biobehav. Rev. 2013;37:401–417. doi: 10.1016/j.neubiorev.2013.01.013. PubMed DOI
Symons A.E., El-Deredy W., Schwartze M., Kotz S.A. The functional role of neural oscillations in non-verbal emotional communication. Front. Hum. Neurosci. 2016;10:239. doi: 10.3389/fnhum.2016.00239. PubMed DOI PMC
Marzetti L., Basti A., Chella F., D’Andrea A., Syrjälä J., Pizzella V. Brain Functional Connectivity Through Phase Coupling of Neuronal Oscillations: A Perspective From Magnetoencephalography. Front. Neurosci. 2019;13:964. doi: 10.3389/fnins.2019.00964. PubMed DOI PMC
Andersen L.M., Jerbi K., Dalal S.S. Can EEG and MEG detect signals from the human cerebellum? Neuroimage. 2020;215:116817. doi: 10.1016/j.neuroimage.2020.116817. PubMed DOI PMC
Canolty R.T., Edwards E., Dalal S.S., Soltani M., Nagarajan S.S., Kirsch H.E., Berger M.S., Barbaro N.M., Knight R.T. High gamma power is phase-locked to theta oscillations in human neocortex. Science. 2006;313:1626–1628. doi: 10.1126/science.1128115. PubMed DOI PMC
Lakatos P., Shah A.S., Knuth K.H., Ulbert I., Karmos G., Schroeder C.E. An Oscillatory Hierarchy Controlling Neuronal Excitability and Stimulus Processing in the Auditory Cortex. J. Neurophysiol. 2005;94:1904–1911. doi: 10.1152/jn.00263.2005. PubMed DOI
Canolty R.T., Knight R.T. The functional role of cross-frequency coupling. Trends Cogn. Sci. 2010;14:506–515. doi: 10.1016/j.tics.2010.09.001. PubMed DOI PMC
Siems M., Siegel M. Dissociated neuronal phase- and amplitude-coupling patterns in the human brain. Neuroimage. 2020;209:116538. doi: 10.1016/j.neuroimage.2020.116538. PubMed DOI PMC
Jirsa V., Müller V. Cross-frequency coupling in real and virtual brain networks. Front. Comput. Neurosci. 2013;7:78. doi: 10.3389/fncom.2013.00078. PubMed DOI PMC
Jensen O., Colgin L.L. Cross-frequency coupling between neuronal oscillations. Trends Cogn. Sci. 2007;11:267–269. doi: 10.1016/j.tics.2007.05.003. PubMed DOI
Lynn P.A., Sponheim S.R. Disturbed theta and gamma coupling as a potential mechanism for visuospatial working memory dysfunction in people with schizophrenia. Neuropsychiatr. Electrophysiol. 2016;2:1–30. doi: 10.1186/s40810-016-0022-3. DOI
Wang J., Fang Y., Wang X., Yang H., Yu X., Wang H. Enhanced gamma activity and cross-frequency interaction of resting-state electroencephalographic oscillations in patients with Alzheimer’s disease. Front. Aging Neurosci. 2017;9:243. doi: 10.3389/fnagi.2017.00243. PubMed DOI PMC
Kiesel A., Steinhauser M., Wendt M., Falkenstein M., Jost K., Philipp A.M., Koch I. Control and interference in task switching-a review. Psychol. Bull. 2010;136:849–874. doi: 10.1037/a0019842. PubMed DOI
Pettigrew C., Martin R.C. Cognitive declines in healthy aging: Evidence from multiple aspects of interference resolution. Psychol. Aging. 2014;29:187–204. doi: 10.1037/a0036085. PubMed DOI
Jeffries S., Everatt J. Working memory: Its role in dyslexia and other specific learning difficulties. Dyslexia. 2004;10:196–214. doi: 10.1002/dys.278. PubMed DOI
Logie R.H. The Functional Organization and Capacity Limits of Working Memory. Curr. Dir. Psychol. Sci. 2011;20:240–245. doi: 10.1177/0963721411415340. DOI
Todd J.J., Marois R. Capacity limit of visual short-term memory in human posterior parietal cortex. Nature. 2004;428:751–754. doi: 10.1038/nature02466. PubMed DOI
Curtis C.E., D’Esposito M. Persistent activity in the prefrontal cortex during working memory. Trends Cogn. Sci. 2003;7:415–423. doi: 10.1016/S1364-6613(03)00197-9. PubMed DOI
Smith E.E., Jonides J. Storage and Executive Processes in the Frontal Lobes. Science. 1999;283:1657–1661. doi: 10.1126/science.283.5408.1657. PubMed DOI
Cowan N. The magical number 4 in short-term memory: A reconsideration of mental storage capacity. Behav. Brain Sci. 2001;24:87–114. doi: 10.1017/S0140525X01003922. PubMed DOI
Kawasaki M., Kitajo K., Yamaguchi Y. Dynamic links between theta executive functions and alpha storage buffers in auditory and visual working memory. Eur. J. Neurosci. 2010;31:1683–1689. doi: 10.1111/j.1460-9568.2010.07217.x. PubMed DOI PMC
Mizuhara H., Yamaguchi Y. Human cortical circuits for central executive function emerge by theta phase synchronization. Neuroimage. 2007;36:232–244. doi: 10.1016/j.neuroimage.2007.02.026. PubMed DOI
Wu X., Chen X., Li Z., Han S., Zhang D. Binding of verbal and spatial information in human working memory involves large-scale neural synchronization at theta frequency. Neuroimage. 2007;35:1654–1662. doi: 10.1016/j.neuroimage.2007.02.011. PubMed DOI
Lisman J.E., Idiart M.A.P. Storage of 7 ± 2 short-term memories in oscillatory subcycles. Science. 1995;267:1512–1515. doi: 10.1126/science.7878473. PubMed DOI
Jensen O., Lisman J.E. Novel lists of 7 ± 2 known items can be reliably stored in an oscillatory short-term memory network: Interaction with long-term memory. Learn Mem. 1996;3:257–263. doi: 10.1101/lm.3.2-3.257. PubMed DOI
Roux F., Uhlhaas P.J. Working memory and neural oscillations: Alpha-gamma versus theta-gamma codes for distinct WM information? Trends Cogn. Sci. 2014;18:16–25. doi: 10.1016/j.tics.2013.10.010. PubMed DOI
Herrmann C.S., Rach S., Neuling T., Strüber D. Transcranial alternating current stimulation: A review of the underlying mechanisms and modulation of cognitive processes. Front. Hum. Neurosci. 2013;7:279. doi: 10.3389/fnhum.2013.00279. PubMed DOI PMC
Van Vugt M.K., Chakravarthi R., Lachaux J.-P. For whom the bell tolls: Periodic reactivation of sensory cortex in the gamma band as a substrate of visual working memory maintenance. Front. Hum. Neurosci. 2014;8:696. doi: 10.3389/fnhum.2014.00696. PubMed DOI PMC
Smith E.H., Banks G.P., Mikell C., Cash S.S., Patel S.R., Eskandar E.N., Sheth S.A. Frequency-Dependent Representation of Reinforcement-Related Information in the Human Medial and Lateral Prefrontal Cortex. J. Neurosci. 2015;35:15827. doi: 10.1523/JNEUROSCI.1864-15.2015. PubMed DOI PMC
Ruffini G., Wendling F., Merlet I., Molaee-Ardekani B., Mekonnen A., Salvador R., Soria-Frisch A., Grau C., Dunne S., Miranda P.C. Transcranial current brain stimulation (tCS): Models and technologies. IEEE Trans. Neural. Syst. Rehabil. Eng. 2013;21:333–345. doi: 10.1109/TNSRE.2012.2200046. PubMed DOI
Terney D., Chaieb L., Moliadze V., Antal A., Paulus W. Increasing Human Brain Excitability by Transcranial High-Frequency Random Noise Stimulation. J. Neurosci. 2008;28:14147. doi: 10.1523/JNEUROSCI.4248-08.2008. PubMed DOI PMC
Bikson M., Bulow P., Stiller J.W., Datta A., Battaglia F., Karnup S.V., Postolache T.T. Transcranial Direct Current Transcranial Direct Current Stimulation for Major Depression: Stimulation for Major Depression: A General System for Quantifying A General System for Quantifying Transcranial Electrotherapy Dosage Transcranial Electrotherapy Dosage Opinion statement. Curr. Treat. Options Neurol. 2008;10:377–385. PubMed
Auvichayapat N., Rotenberg A., Gersner R., Ngodklang S., Tiamkao S., Tassaneeyakul W., Auvichayapat P. Transcranial direct current stimulation for treatment of refractory childhood focal epilepsy. Brain Stimul. 2013;6:696–700. doi: 10.1016/j.brs.2013.01.009. PubMed DOI
Frank E., Schecklmann M., Landgrebe M., Burger J., Kreuzer P., Poeppl T.B., Kleinjung T., Hajak G., Langguth B. Treatment of chronic tinnitus with repeated sessions of prefrontal transcranial direct current stimulation: Outcomes from an open-label pilot study. J. Neurol. 2011;259:327–333. doi: 10.1007/s00415-011-6189-4. PubMed DOI
Fregni F., Boggio P.S., Santos M.C., Lima M., Vieira A.L., Rigonatti S.P., Silva M.T.A., Barbosa E.R., Nitsche M.A., Pascual-Leone A. Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson’s disease. Mov. Disord. 2006;21:1693–1702. doi: 10.1002/mds.21012. PubMed DOI
Fregni F., Gimenes R., Valle A.C., Ferreira M.J.L., Rocha R.R., Natalle L., Bravo R., Rigonatti S.P., Freedman S.D., Nitsche M.A., et al. A randomized, sham-controlled, proof of principle study of transcranial direct current stimulation for the treatment of pain in fibromyalgia. Arthritis Rheum. 2006;54:3988–3998. doi: 10.1002/art.22195. PubMed DOI
Fregni F., Freedman S., Pascual-Leone A. Recent advances in the treatment of chronic pain with non-invasive brain stimulation techniques. Lancet Neurol. 2007;6:188–191. doi: 10.1016/S1474-4422(07)70032-7. PubMed DOI
Schlaug G., Renga V., Nair D. Transcranial Direct Current Stimulation in Stroke Recovery. Arch. Neurol. 2008;65:1571–1576. doi: 10.1001/archneur.65.12.1571. PubMed DOI PMC
Baker J.M., Rorden C., Fridriksson J. Using transcranial direct current stimulation (tDCS) to treat stroke patients with aphasia. Stroke. 2010;41:1229. doi: 10.1161/STROKEAHA.109.576785. PubMed DOI PMC
Jacobson L., Koslowsky M., Lavidor M. tDCS polarity effects in motor and cognitive domains: A meta-analytical review. Exp. Brain Res. 2011;216:1–10. doi: 10.1007/s00221-011-2891-9. PubMed DOI
Nitsche M.A., Paulus W. Transcranial direct current stimulation—Update 2011. Restor. Neurol. Neurosci. 2011;29:463–492. doi: 10.3233/RNN-2011-0618. PubMed DOI
Nitsche M.A., Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 2001;57:1899–1901. doi: 10.1212/WNL.57.10.1899. PubMed DOI
Nitsche M.A., Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. 2000;527:633. doi: 10.1111/j.1469-7793.2000.t01-1-00633.x. PubMed DOI PMC
Nitsche M.A., Fricke K., Henschke U., Schlitterlau A., Liebetanz D., Lang N., Henning S., Tergau F., Paulus W. Pharmacological Modulation of Cortical Excitability Shifts Induced by Transcranial Direct Current Stimulation in Humans. J. Physiol. 2003;553:293–301. doi: 10.1113/jphysiol.2003.049916. PubMed DOI PMC
Bindman L.J., Lippold O.C.J., Redfearn J.W.T. 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. 1964;172:369–382. doi: 10.1113/jphysiol.1964.sp007425. PubMed DOI PMC
Lee S.B., Youn J., Jang W., Yang H.O. Neuroprotective effect of anodal transcranial direct current stimulation on 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced neurotoxicity in mice through modulating mitochondrial dynamics. Neurochem. Int. 2019;129:104491. doi: 10.1016/j.neuint.2019.104491. PubMed DOI
Lee S.B., Kim H.T., Yang H.O., Jang W. Anodal transcranial direct current stimulation prevents methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced neurotoxicity by modulating autophagy in an in vivo mouse model of Parkinson’s disease. Sci. Rep. 2018;8:15165. doi: 10.1038/s41598-018-33515-7. PubMed DOI PMC
Scelzo E., Giannicola G., Rosa M., Ciocca M., Ardolino G., Cogiamanian F., Ferrucci R., Fumagalli M., Mameli F., Barbieri S., et al. Increased short latency afferent inhibition after anodal transcranial direct current stimulation. Neurosci. Lett. 2011;498:167–170. doi: 10.1016/j.neulet.2011.05.007. PubMed DOI
Marshall L., Mölle M., Hallschmid M., Born J. Transcranial Direct Current Stimulation during Sleep Improves Declarative Memory. J. Neurosci. 2004;24:9985. doi: 10.1523/JNEUROSCI.2725-04.2004. PubMed DOI PMC
Fregni F., Boggio P.S., Nitsche M., Bermpohl F., Antal A., Feredoes E., Marcolin M.A., Rigonatti S.P., Silva M.T., Paulus W., et al. Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Exp. Brain. Res. 2005;166:23–30. doi: 10.1007/s00221-005-2334-6. PubMed DOI
Reis J., Fritsch B. Modulation of motor performance and motor learning by transcranial direct current stimulation. Curr. Opin. Neurol. 2011;24:590–596. doi: 10.1097/WCO.0b013e32834c3db0. PubMed DOI
Pereira J.B., Junqué C., Bartrés-Faz D., Martí M.J., Sala-Llonch R., Compta Y., Falcón C., Vendrell P., Pascual-Leone Á., Valls-Solé J., et al. Modulation of verbal fluency networks by transcranial direct current stimulation (tDCS) in Parkinson’s disease. Brain Stimul. 2013;6:16–24. doi: 10.1016/j.brs.2012.01.006. PubMed DOI
Dockery C.A., Hueckel-Weng R., Birbaumer N., Plewnia C. Enhancement of planning ability by transcranial direct current stimulation. J. Neurosci. 2009;29:7271–7277. doi: 10.1523/JNEUROSCI.0065-09.2009. PubMed DOI PMC
Huang Y., A Liu A., Lafon B., Friedman D., Dayan M., Wang X., Bikson M., Doyle W.K., Devinsky O., Parra L.C. Measurements and models of electric fields in the in vivo human brain during transcranial electric stimulation. Elife. 2017;6:e18834. doi: 10.7554/eLife.18834. PubMed DOI PMC
Kuo M.F., Nitsche M.A. Effects of Transcranial Electrical Stimulation on Cognition. Clin. EEG Neurosci. 2012;43:192–199. doi: 10.1177/1550059412444975. PubMed DOI
Thut G., Miniussi C. New insights into rhythmic brain activity from TMS-EEG studies. Trends Cogn. Sci. 2009;13:182–189. doi: 10.1016/j.tics.2009.01.004. PubMed DOI
Kirov R., Weiss C., Siebner H.R., Born J., Marshall L. Slow oscillation electrical brain stimulation during waking promotes EEG theta activity and memory encoding. Proc. Natl. Acad. Sci. USA. 2009;106:15460–15465. doi: 10.1073/pnas.0904438106. PubMed DOI PMC
Zaehle T., Rach S., Herrmann C.S. Transcranial Alternating Current Stimulation Enhances Individual Alpha Activity in Human EEG. PLoS ONE. 2010;5:e13766. doi: 10.1371/journal.pone.0013766. PubMed DOI PMC
Zaghi S., Rezende L.D.F., Oliveira L., El-Nazer R., Menning S., Tadini L., Fregni F. Inhibition of motor cortex excitability with 15 Hz transcranial alternating current stimulation (tACS) Neurosci. Lett. 2010;479:211–214. doi: 10.1016/j.neulet.2010.05.060. PubMed DOI
Wach C., Krause V., Moliadze V., Paulus W., Schnitzler A., Pollok B. Effects of 10 Hz and 20 Hz transcranial alternating current stimulation (tACS) on motor functions and motor cortical excitability. Behav. Brain Res. 2013;241:1–6. doi: 10.1016/j.bbr.2012.11.038. PubMed DOI
Schutter D.J.L.G., Hortensius R. Brain oscillations and frequency-dependent modulation of cortical excitability. Brain Stimul. 2011;4:97–103. doi: 10.1016/j.brs.2010.07.002. PubMed DOI
Veniero D., Vossen A., Gross J., Thut G. Lasting EEG/MEG aftereffects of rhythmic transcranial brain stimulation: Level of control over oscillatory network activity. Front. Cell. Neurosci. 2015;9:477. doi: 10.3389/fncel.2015.00477. PubMed DOI PMC
Bland N.S., Sale M.V. Current challenges: The ups and downs of tACS. Exp. Brain Res. 2019;237:3071–3088. doi: 10.1007/s00221-019-05666-0. PubMed DOI
Kanai R., Chaieb L., Antal A., Walsh V., Paulus W. Frequency-Dependent Electrical Stimulation of the Visual Cortex. Curr. Biol. 2008;18:1839–1843. doi: 10.1016/j.cub.2008.10.027. PubMed DOI
Laczó B., Antal A., Niebergall R., Treue S., Paulus W. Transcranial alternating stimulation in a high gamma frequency range applied over V1 improves contrast perception but does not modulate spatial attention. Brain Stimul. 2012;5:484–491. doi: 10.1016/j.brs.2011.08.008. PubMed DOI
Antal A., Boros K., Poreisz C., Chaieb L., Terney D., Paulus W. Comparatively weak after-effects of transcranial alternating current stimulation (tACS) on cortical excitability in humans. Brain Stimul. 2008;1:97–105. doi: 10.1016/j.brs.2007.10.001. PubMed DOI
Pogosyan A., Gaynor L.D., Eusebio A., Brown P. Boosting Cortical Activity at Beta-Band Frequencies Slows Movement in Humans. Curr. Biol. 2009;19:1637. doi: 10.1016/j.cub.2009.07.074. PubMed DOI PMC
Feurra M., Bianco G., Santarnecchi E., del Testa M., Rossi A., Rossi S. Frequency-Dependent Tuning of the Human Motor System Induced by Transcranial Oscillatory Potentials. J. Neurosci. 2011;31:12165–12170. doi: 10.1523/JNEUROSCI.0978-11.2011. PubMed DOI PMC
Brignani D., Ruzzoli M., Mauri P., Miniussi C. Is Transcranial Alternating Current Stimulation Effective in Modulating Brain Oscillations? PLoS ONE. 2013;8:e56589. doi: 10.1371/journal.pone.0056589. PubMed DOI PMC
Wach C., Krause V., Moliadze V., Paulus W., Schnitzler A., Pollok B. The effect of 10 Hz transcranial alternating current stimulation (tACS) on corticomuscular coherence. Front. Hum. Neurosci. 2013;7:511. doi: 10.3389/fnhum.2013.00511. PubMed DOI PMC
Mulquiney P.G., Hoy K.E., Daskalakis Z.J., Fitzgerald P.B. Improving working memory: Exploring the effect of transcranial random noise stimulation and transcranial direct current stimulation on the dorsolateral prefrontal cortex. Clin. Neurophysiol. 2011;122:2384–2389. doi: 10.1016/j.clinph.2011.05.009. PubMed DOI
Boggio P.S., Rigonatti S.P., Ribeiro R., Myczkowski M.L., Nitsche M.A., Pascual-Leone A., Fregni F. A randomized, double-blind clinical trial on the efficacy of cortical direct current stimulation for the treatment of major depression. Int. J. Neuropsychopharmacol. 2008;11:249–254. doi: 10.1017/S1461145707007833. PubMed DOI PMC
Polanía R., Nitsche M.A., Korman C., Batsikadze G., Paulus W. The importance of timing in segregated theta phase-coupling for cognitive performance. Curr. Biol. 2012;22:1314–1318. doi: 10.1016/j.cub.2012.05.021. PubMed DOI
Cappelletti M., Gessaroli E., Hithersay R., Mitolo M., Didino D., Kanai R., Kadosh R.C., Walsh V. Transfer of Cognitive Training across Magnitude Dimensions Achieved with Concurrent Brain Stimulation of the Parietal Lobe. J. Neurosci. 2013;33:14899. doi: 10.1523/JNEUROSCI.1692-13.2013. PubMed DOI PMC
Grabner R.H., Krenn J., Fink A., Arendasy M., Benedek M. Effects of alpha and gamma transcranial alternating current stimulation (tACS) on verbal creativity and intelligence test performance. Neuropsychologia. 2018;118:91–98. doi: 10.1016/j.neuropsychologia.2017.10.035. PubMed DOI
Santarnecchi E., Polizzotto N.R., Godone M., Giovannelli F., Feurra M., Matzen L., Rossi A., Rossi S. Frequency-dependent enhancement of fluid intelligence induced by transcranial oscillatory potentials. Curr. Biol. 2013;23:1449–1453. doi: 10.1016/j.cub.2013.06.022. PubMed DOI
Sauseng P., Griesmayr B., Freunberger R., Klimesch W. Control mechanisms in working memory: A possible function of EEG theta oscillations. Neurosci. Biobehav. Rev. 2010;34:1015–1022. doi: 10.1016/j.neubiorev.2009.12.006. PubMed DOI
Jaušovec N., Jaušovec K. Increasing working memory capacity with theta transcranial alternating current stimulation (tACS) Biol. Psychol. 2014;96:42–47. doi: 10.1016/j.biopsycho.2013.11.006. PubMed DOI
Jaušovec N., Jaušovec K., Pahor A. The influence of theta transcranial alternating current stimulation (tACS) on working memory storage and processing functions. Acta Psychol. 2014;146:1–6. doi: 10.1016/j.actpsy.2013.11.011. PubMed DOI
Pahor A., Jaušovec N. The effects of theta transcranial alternating current stimulation (tACS) on fluid intelligence. Int. J. Psychophysiol. 2014;93:322–331. doi: 10.1016/j.ijpsycho.2014.06.015. PubMed DOI
Neuling T., Rach S., Herrmann C.S. Orchestrating neuronal networks: Sustained after-effects of transcranial alternating current stimulation depend upon brain states. Front. Hum. Neurosci. 2013;7:161. doi: 10.3389/fnhum.2013.00161. PubMed DOI PMC
Klimesch W. Alpha-band oscillations, attention, and controlled access to stored information. Trends Cogn. Sci. 2012;16:606–617. doi: 10.1016/j.tics.2012.10.007. PubMed DOI PMC
Voss U., Holzmann R., Hobson A., Paulus W., Koppehele-Gossel J., Klimke A., A Nitsche M. Induction of self awareness in dreams through frontal low current stimulation of gamma activity. Nat. Neurosci. 2014;17:810–812. doi: 10.1038/nn.3719. PubMed DOI
Klink K., Paßmann S., Kasten F.H., Peter J. The modulation of cognitive performance with transcranial alternating current stimulation: A systematic review of frequency-specific effects. Brain Sci. 2020;10:932. doi: 10.3390/brainsci10120932. PubMed DOI PMC
Schutter D.J.L.G., Wischnewski M. A meta-analytic study of exogenous oscillatory electric potentials in neuroenhancement. Neuropsychologia. 2016;86:110–118. doi: 10.1016/j.neuropsychologia.2016.04.011. PubMed DOI
Figee M., Mayberg H. The future of personalized brain stimulation. Nat. Med. 2021;27:196–197. doi: 10.1038/s41591-021-01243-7. PubMed DOI
Frohlich F., Riddle J. Conducting double-blind placebo-controlled clinical trials of transcranial alternating current stimulation (tACS) Transl. Psychiatry. 2021;11:1–12. doi: 10.1038/s41398-021-01391-x. PubMed DOI PMC
Van Driel J., Sligte I.G., Linders J., Elport D., Cohen M.X. Frequency Band-Specific Electrical Brain Stimulation Modulates Cognitive Control Processes. PLoS ONE. 2015;10:e0138984. doi: 10.1371/journal.pone.0138984. PubMed DOI PMC
Onslow A.C.E., Bogacz R., Jones M.W. Quantifying phase–amplitude coupling in neuronal network oscillations. Prog. Biophys. Mol. Biol. 2011;105:49–57. doi: 10.1016/j.pbiomolbio.2010.09.007. PubMed DOI
Meiron O., Lavidor M. Prefrontal oscillatory stimulation modulates access to cognitive control references in retrospective metacognitive commentary. Clin. Neurophysiol. 2014;125:77–82. doi: 10.1016/j.clinph.2013.06.013. PubMed DOI
Gonzalez-Perez M., Wakui E., Thoma V., Nitsche M.A., Rivolta D. Transcranial alternating current stimulation (tACS) at 40 Hz enhances face and object perception. Neuropsychologia. 2019;135:107237. doi: 10.1016/j.neuropsychologia.2019.107237. PubMed DOI
Abellaneda-Pérez K., Vaqué-Alcázar L., Perellón-Alfonso R., Bargalló N., Kuo M.F., Pascual-Leone A., Nitsche M.A., Bartrés-Faz D. Differential tDCS and tACS Effects on Working Memory-Related Neural Activity and Resting-State Connectivity. Front. Neurosci. 2020;13:1440. doi: 10.3389/fnins.2019.01440. PubMed DOI PMC
Sahu P.P., Tseng P. Frontoparietal theta tACS nonselectively enhances encoding, maintenance, and retrieval stages in visuospatial working memory. Neurosci. Res. 2021;172:41–50. doi: 10.1016/j.neures.2021.05.005. PubMed DOI
Chander B.S., Witkowski M., Braun C., Robinson S.E., Born J., Cohen L.G., Birbaumer N., Soekadar S.R. tACS Phase Locking of Frontal Midline Theta Oscillations Disrupts Working Memory Performance. Front. Cell. Neurosci. 2016;10:120. doi: 10.3389/fncel.2016.00120. PubMed DOI PMC
Vosskuhl J., Huster R.J., Herrmann C.S. Increase in short-term memory capacity induced by down-regulating individual theta frequency via transcranial alternating current stimulation. Front. Hum. Neurosci. 2015;9:257. doi: 10.3389/fnhum.2015.00257. PubMed DOI PMC
Alekseichuk I., Pabel S.C., Antal A., Paulus W. Intrahemispheric theta rhythm desynchronization impairs working memory. Restor. Neurol. Neurosci. 2017;35:147–158. doi: 10.3233/RNN-160714. PubMed DOI
Tseng P., Iu K.C., Juan C.H. The critical role of phase difference in theta oscillation between bilateral parietal cortices for visuospatial working memory. Sci. Rep. 2018;8:1–9. doi: 10.1038/s41598-017-18449-w. PubMed DOI PMC
Violante I.R., Li L.M., Carmichael D.W., Lorenz R., Leech R., Hampshire A., Rothwell J.C., Sharp D.J. Externally induced frontoparietal synchronization modulates network dynamics and enhances working memory performance. Elife. 2017;6:e22001. doi: 10.7554/eLife.22001. PubMed DOI PMC
Kleinert M.L., Szymanski C., Müller V. Frequency-unspecific effects of θ-tACS related to a visuospatial working memory task. Front. Hum. Neurosci. 2017;11:367. doi: 10.3389/fnhum.2017.00367. PubMed DOI PMC
Becher A.K., Höhne M., Axmacher N., Chaieb L., Elger C.E., Fell J. Intracranial electroencephalography power and phase synchronization changes during monaural and binaural beat stimulation. Eur. J. Neurosci. 2015;41:254–263. doi: 10.1111/ejn.12760. PubMed DOI
Fries P. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 2009;32:209–224. doi: 10.1146/annurev.neuro.051508.135603. PubMed DOI
Jia X., Kohn A. Gamma Rhythms in the Brain. PLoS Biol. 2011;9:e1001045. doi: 10.1371/journal.pbio.1001045. PubMed DOI PMC
Hoy K.E., Bailey N., Arnold S., Windsor K., John J., Daskalakis Z.J., Fitzgerald P.B. The effect of γ-tACS on working memory performance in healthy controls. Brain. Cogn. 2015;101:51–56. doi: 10.1016/j.bandc.2015.11.002. PubMed DOI
Tseng P., Chang Y.T., Chang C.F., Liang W.K., Juan C.H. The critical role of phase difference in gamma oscillation within the temporoparietal network for binding visual working memory. Sci. Rep. 2016;6:32138. doi: 10.1038/srep32138. PubMed DOI PMC
Möller A., Nemmi F., Karlsson K., Klingberg T. Transcranial Electric Stimulation Can Impair Gains during Working Memory Training and Affects the Resting State Connectivity. Front. Hum. Neurosci. 2017;11:364. doi: 10.3389/fnhum.2017.00364. PubMed DOI PMC
Misselhorn J., Göschl F., Higgen F.L., Hummel F.C., Gerloff C., Engel A.K. Sensory capability and information integration independently explain the cognitive status of healthy older adults. Sci. Rep. 2020;10:22437. doi: 10.1038/s41598-020-80069-8. PubMed DOI PMC
Santarnecchi E., Muller T., Rossi S., Sarkar A., Polizzotto N., Rossi A., Kadosh R.C. Individual differences and specificity of prefrontal gamma frequency-tACS on fluid intelligence capabilities. Cortex. 2016;75:33–43. doi: 10.1016/j.cortex.2015.11.003. PubMed DOI
Pahor A., Jaušovec N. The effects of theta and gamma tacs on working memory and electrophysiology. Front. Hum. Neurosci. 2018;11:651. doi: 10.3389/fnhum.2017.00651. PubMed DOI PMC
Lisman J.E., Jensen O. The Theta-Gamma Neural Code. Neuron. 2013;77:1002–1016. doi: 10.1016/j.neuron.2013.03.007. PubMed DOI PMC
de Lara G.A., Alekseichuk I., Turi Z., Lehr A., Antal A., Paulus W. Perturbation of theta-gamma coupling at the temporal lobe hinders verbal declarative memory. Brain Stimul. 2018;11:509–517. doi: 10.1016/j.brs.2017.12.007. PubMed DOI
Turi Z., Mittner M., Lehr A., Bürger H., Antal A., Paulus W. θ-γ Cross-Frequency Transcranial Alternating Current Stimulation over the Trough Impairs Cognitive Control. ENeuro. 2020;7:1–12. doi: 10.1523/ENEURO.0126-20.2020. PubMed DOI PMC
Riddle J., McFerren A., Frohlich F. Causal role of cross-frequency coupling in distinct components of cognitive control. Prog. Neurobiol. 2021;202:102033. doi: 10.1016/j.pneurobio.2021.102033. PubMed DOI PMC
Alekseichuk I., Turi Z., Amador de Lara G., Antal A., Paulus W. Spatial Working Memory in Humans Depends on Theta and High Gamma Synchronization in the Prefrontal Cortex. Curr. Biol. 2016;26:1513–1521. doi: 10.1016/j.cub.2016.04.035. PubMed DOI
Delorme A., Makeig S. EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods. 2004;134:9–21. doi: 10.1016/j.jneumeth.2003.10.009. PubMed DOI
Benesty J., Chen J., Huang Y. A generalized MVDR spectrum. IEEE Signal. Process. Lett. 2005;12:827–830. doi: 10.1109/LSP.2005.859517. DOI
Grover S., Wen W., Viswanathan V., Gill C.T., Reinhart R.M.G. Long-lasting, dissociable improvements in working memory and long-term memory in older adults with repetitive neuromodulation. Nat. Neurosci. 2022;25:1237–1246. doi: 10.1038/s41593-022-01132-3. PubMed DOI PMC
Pittman-polletta B., Hsieh W.H., Kaur S., Lo M.T., Hu K. Detecting phase-amplitude coupling with high frequency resolution using adaptive decompositions. J. Neurosci. Methods. 2014;226:15–32. doi: 10.1016/j.jneumeth.2014.01.006. PubMed DOI PMC
Joundi R.A., Jenkinson N., Brittain J.S., Aziz T.Z., Brown P. Driving Oscillatory Activity in the Human Cortex Enhances Motor Performance. Curr. Biol. 2012;22:403. doi: 10.1016/j.cub.2012.01.024. PubMed DOI PMC
Kasten F.H., Dowsett J., Herrmann C.S. Sustained aftereffect of α-tACS lasts up to 70 min after stimulation. Front. Hum. Neurosci. 2016;10:245. doi: 10.3389/fnhum.2016.00245. PubMed DOI PMC
Elyamany O., Leicht G., Herrmann C.S., Mulert C. Transcranial alternating current stimulation (tACS): From basic mechanisms towards first applications in psychiatry. Eur. Arch. Psychiatry Clin. Neurosci. 2021;271:135–156. doi: 10.1007/s00406-020-01209-9. PubMed DOI PMC
Moussavi Z., Kimura K., Kehler L., de Oliveira Francisco C., Lithgow B. A Novel Program to Improve Cognitive Function in Individuals With Dementia Using Transcranial Alternating Current Stimulation (tACS) and Tutored Cognitive Exercises. Front. Aging. 2021;2:632545. doi: 10.3389/fragi.2021.632545. PubMed DOI PMC
Kehler L., Francisco C.O., Uehara M.A., Moussavi Z. The effect of transcranial alternating current stimulation (tACS) on cognitive function in older adults with dementia; Proceedings of the 2020 42nd Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC); Montreal, QC, Canada. 20–24 July 2020; pp. 3649–3653. PubMed DOI
Haller N., Hasan A., Padberg F., Brunelin J., da Costa Lane Valiengo L., Palm U. Gamma transcranial alternating current stimulation in patients with negative symptoms in schizophrenia: A case series. Neurophysiol. Clin. 2020;50:301–304. doi: 10.1016/j.neucli.2020.06.004. PubMed DOI
Bréchet L., Yu W., Biagi M.C., Ruffini G., Gagnon M., Manor B., Pascual-Leone A. Patient-Tailored, Home-Based Non-invasive Brain Stimulation for Memory Deficits in Dementia Due to Alzheimer’s Disease. Front. Neurol. 2021;12:775. doi: 10.3389/fneur.2021.598135. PubMed DOI PMC