Top

Published in:

01-11-2019 | Review

Recovering Brain Dynamics During Concurrent tACS-M/EEG: An Overview of Analysis Approaches and Their Methodological and Interpretational Pitfalls

Authors: Florian H. Kasten, Christoph S. Herrmann

Published in: Brain Topography | Issue 6/2019

Abstract

Transcranial alternating current stimulation (tACS) is increasingly used as a tool to non-invasively modulate brain oscillations in a frequency specific manner. A growing body of neuroscience research utilizes tACS to probe causal relationships between neuronal oscillations and cognitive processes or explore its capability of restoring dysfunctional brain oscillations implicated in various neurological and psychiatric disease. However, the underlying mechanisms of action are yet poorly understood. Due to a massive electromagnetic artifact, overlapping with the frequency of interest, direct insights to effects during stimulation from electrophysiological signals (i.e. EEG/MEG) are methodologically challenging. In the current review, we provide an overview of analysis approaches to recover brain signals in M/EEG during tACS, detailing their underlying concepts as well as limitations and methodological and interpretational pitfalls. While different analysis strategies can achieve strong attenuation of the tACS artifact in M/EEG signals, a compete removal of it is not feasible so far. However, we argue that with a combination of careful experimental designs, robust outcome measures and appropriate control analyses, valid and important insights to online effects of tACS can be revealed, enriching our understanding of its basic underlying mechanisms.

Available only for authorised users

Ali MM, Sellers KK, Frohlich F (2013) Transcranial alternating current stimulation modulates large-scale cortical network activity by network resonance. J Neurosci 33:11262–11275. https://doi.org/10.1523/jneurosci.5867-12.2013 CrossRefPubMedPubMedCentral

Dowsett J, Herrmann CS (2016) Transcranial alternating current stimulation with sawtooth waves: simultaneous stimulation and EEG recording. Front Hum Neurosci 10:1–10. https://doi.org/10.3389/fnhum.2016.00135 CrossRef

Fröhlich F, McCormick DA (2010) Endogenous electric fields may guide neocortical network activity. Neuron 67:129–143. https://doi.org/10.1016/j.neuron.2010.06.005 CrossRefPubMedPubMedCentral

Gross J, Kujala J, Hamalainen M et al (2001) Dynamic imaging of coherent sources: studying neural interactions in the human brain. Proc Natl Acad Sci USA 98:694–699. https://doi.org/10.1073/pnas.98.2.694 CrossRefPubMed

Helfrich RF, Schneider TR, Rach S et al (2014) Entrainment of brain oscillations by transcranial alternating current stimulation. Curr Biol 24:333–339. https://doi.org/10.1016/j.cub.2013.12.041 CrossRefPubMed

Herring JD, Esterer S, Marshall TR et al (2019) Low-frequency alternating current stimulation rhythmically suppresses gamma-band oscillations and impairs perceptual performance. Neuroimage 184:440–449. https://doi.org/10.1016/j.neuroimage.2018.09.047 CrossRefPubMed

Herrmann CS, Rach S, Neuling T, Strüber D (2013) Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes. Front Hum Neurosci 7:1–13. https://doi.org/10.3389/fnhum.2013.00279 CrossRef

Herrmann CS, Strüber D, Helfrich RF, Engel AK (2016) EEG oscillations: from correlation to causality. Int J Psychophysiol 103:12–21. https://doi.org/10.1016/j.ijpsycho.2015.02.003 CrossRefPubMed

Kasten FH, Herrmann CS (2017) Transcranial alternating current stimulation (tACS) enhances mental rotation performance during and after stimulation. Front Hum Neurosci 11:1–16. https://doi.org/10.3389/fnhum.2017.00002 CrossRef

Kasten FH, Dowsett J, Herrmann CS (2016) Sustained aftereffect of α-tACS lasts up to 70 min after stimulation. Front Hum Neurosci 10:245. https://doi.org/10.3389/fnhum.2016.00245 CrossRefPubMedPubMedCentral

Kasten FH, Maess B, Herrmann CS (2018a) Facilitated event-related power modulations during transcranial alternating current stimulation (tACS) revealed by concurrent tACS-MEG. eNeuro. https://doi.org/10.1523/eneuro.0069-18.2018 CrossRefPubMedPubMedCentral

Kasten FH, Negahbani E, Fröhlich F, Herrmann CS (2018b) 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 179:134–143. https://doi.org/10.1016/j.neuroimage.2018.05.068 CrossRefPubMed

Kohli S, Casson AJ (2015) Removal of transcranial a.c. current stimulation artifact from simultaneous EEG recordings by superposition of moving averages. In: Proceedings of annual international conference of IEEE Engineering in Medicine and Biology Society 2015, pp 3436–3439. https://doi.org/10.1109/embc.2015.7319131

Lustenberger C, Boyle MR, Foulser AA et al (2015) Functional role of frontal alpha oscillations in creativity. Cortex 67:74–82. https://doi.org/10.1016/j.cortex.2015.03.012 CrossRefPubMedPubMedCentral

Mäkelä N, Sarvas J, Ilmoniemi RJ (2017) Proceedings #17. A simple reason why beamformer may (not) remove the tACS-induced artifact in MEG. Brain Stimul 10:e66–e67. https://doi.org/10.1016/j.brs.2017.04.110 CrossRef

Minami S, Amano K (2017) Illusory jitter perceived at the frequency of alpha oscillations. Curr Biol 27:2344–2351.e4. https://doi.org/10.1016/j.cub.2017.06.033 CrossRefPubMed

Negahbani E, Kasten FH, Herrmann CS, Frohlich F (2018) Targeting alpha-band oscillations in a cortical model with amplitude-modulated high-frequency transcranial electric stimulation. Neuroimage 173:3–12. https://doi.org/10.1016/j.neuroimage.2018.02.005 CrossRefPubMedPubMedCentral

Neuling T, Rach S, Herrmann CS (2013) Orchestrating neuronal networks: sustained after-effects of transcranial alternating current stimulation depend upon brain states. Front Hum Neurosci 7:161. https://doi.org/10.3389/fnhum.2013.00161 CrossRefPubMedPubMedCentral

Neuling T, Ruhnau P, Fuscà M et al (2015) Friends, not foes: magnetoencephalography as a tool to uncover brain dynamics during transcranial alternating current stimulation. Neuroimage 118:406–413. https://doi.org/10.1016/j.neuroimage.2015.06.026 CrossRefPubMedPubMedCentral

Neuling T, Ruhnau P, Weisz N et al (2017) Faith and oscillations recovered: on analyzing EEG/MEG signals during tACS. Neuroimage 147:960–963. https://doi.org/10.1016/j.neuroimage.2016.11.022 CrossRefPubMed

Noury N, Siegel M (2017) Phase properties of transcranial electrical stimulation artifacts in electrophysiological recordings. Neuroimage 158:406–416. https://doi.org/10.1016/j.neuroimage.2017.07.010 CrossRefPubMed

Noury N, Siegel M (2018) Analyzing EEG and MEG signals recorded during tES, a reply. Neuroimage 167:53–61. https://doi.org/10.1016/j.neuroimage.2017.11.023 CrossRefPubMed

Noury N, Hipp JF, Siegel M (2016) Physiological processes non-linearly affect electrophysiological recordings during transcranial electric stimulation. Neuroimage 140:99–109. https://doi.org/10.1016/j.neuroimage.2016.03.065 CrossRefPubMed

Ozen S, Sirota A, Belluscio MA et al (2010) Transcranial electric stimulation entrains cortical neuronal populations in rats. J Neurosci 30:11476–11485. https://doi.org/10.1523/jneurosci.5252-09.2010 CrossRefPubMedPubMedCentral

Palomba D, Angrilli A, Mini A (1997) Visual evoked potentials, heart rate responses and memory to emotional pictorial stimuli. Int J Psychophysiol 27:55–67. https://doi.org/10.1016/s0167-8760(97)00751-4 CrossRefPubMed

Pfurtscheller G, Lopes Da Silva FH (1999) Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110:1842–1857. https://doi.org/10.1016/s1388-2457(99)00141-8 CrossRefPubMed

Pollatos O, Herbert BM, Matthias E, Schandry R (2007) Heart rate response after emotional picture presentation is modulated by interoceptive awareness. Int J Psychophysiol 63:117–124. https://doi.org/10.1016/j.ijpsycho.2006.09.003 CrossRefPubMed

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 30:15067–15079. https://doi.org/10.1523/jneurosci.2059-10.2010 CrossRefPubMedPubMedCentral

Soekadar SR, Witkowski M, Cossio EG et al (2013) In vivo assessment of human brain oscillations during application of transcranial electric currents. Nat Commun 4:2032. https://doi.org/10.1038/ncomms3032 CrossRefPubMedPubMedCentral

Van Veen BDBD, Buckley KMKM (1988) Beamforming: a versatile approach to spatial filtering. IEEE ASSP Mag 5:4–24. https://doi.org/10.1109/53.665 CrossRef

Van Veen BD, Van Drongelen W, Yuchtman M, Suzuki A (1997) Localization of brain electrical activity via linearly constrained minimum variance spatial filtering. IEEE Trans Biomed Eng 44:867–880. https://doi.org/10.1109/10.623056 CrossRefPubMed

Voss U, Holzmann R, Hobson A et al (2014) Induction of self awareness in dreams through frontal low current stimulation of gamma activity. Nat Neurosci 17:810–812. https://doi.org/10.1038/nn.3719 CrossRefPubMed

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 8:499–508. https://doi.org/10.1016/j.brs.2014.12.004 CrossRefPubMedPubMedCentral

Vosskuhl J, Huster RJ, Herrmann CS (2015) Increase in short-term memory capacity induced by down-regulating individual theta frequency via transcranial alternating current stimulation. Front Hum Neurosci 9:257. https://doi.org/10.3389/fnhum.2015.00257 CrossRefPubMedPubMedCentral

Wach C, Krause V, Moliadze V et al (2013) Effects of 10 Hz and 20 Hz transcranial alternating current stimulation (tACS) on motor functions and motor cortical excitability. Behav Brain Res 241:1–6. https://doi.org/10.1016/j.bbr.2012.11.038 CrossRefPubMed

Wischnewski M, Engelhardt M, Salehinejad MA et al (2018) NMDA receptor-mediated motor cortex plasticity after 20 Hz transcranial alternating current stimulation. Cereb Cortex. https://doi.org/10.1093/cercor/bhy160 CrossRef

Witkowski M, Garcia-Cossio E, Chander BS et al (2016) Mapping entrained brain oscillations during transcranial alternating current stimulation (tACS). Neuroimage 140:89–98. https://doi.org/10.1016/j.neuroimage.2015.10.024 CrossRefPubMed

Zaehle T, Rach S, Herrmann CS (2010) Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PLoS ONE 5:13766. https://doi.org/10.1371/journal.pone.0013766 CrossRef

Title: Recovering Brain Dynamics During Concurrent tACS-M/EEG: An Overview of Analysis Approaches and Their Methodological and Interpretational Pitfalls
Authors: Florian H. Kasten
Christoph S. Herrmann
Publication date: 01-11-2019
Publisher: Springer US
Published in: Brain Topography / Issue 6/2019
Print ISSN: 0896-0267
Electronic ISSN: 1573-6792
DOI: https://doi.org/10.1007/s10548-019-00727-7

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Recovering Brain Dynamics During Concurrent tACS-M/EEG: An Overview of Analysis Approaches and Their Methodological and Interpretational Pitfalls

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 6/2019

“Plis de passage” Deserve a Role in Models of the Cortical Folding Process

The Emotional Facet of Subjective and Neural Indices of Similarity

Applications of Functional Near-Infrared Spectroscopy in Fatigue, Sleep Deprivation, and Social Cognition

Current Opinions in Brain Imaging Methods and Applications

Individual Differences as a Key Factor to Uncover the Neural Underpinnings of Hedonic and Social Functions of Human Olfaction: Current Findings from PET and fMRI Studies and Future Considerations

The Role of the Temporoparietal Junction in Self-Other Distinction