tACS motor system effects can be caused by transcutaneous stimulation of peripheral nerves

Asamoah, Boateng; Khatoun, Ahmad; Laughlin, Myles Mc

doi:10.1038/s41467-018-08183-w

Cited by 223 publications

(199 citation statements)

References 66 publications

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“…Stimulation of peripheral nerves in the skin might induce rhythmic activation in the somatosensory cortex. Cutaneous stimulation effects have been shown to largely explain tACS effects on motor cortex, however, it is unclear whether this explanation can be generalized to stimulation effects beyond motor cortex (31). In a recent study by our group, Schwab et al (46) addressed this point by source analysis of neural effects induced by tACS over the parieto-occipital cortex.…”

Section: Discussionmentioning

confidence: 99%

“…Further insight has been provided primarily in the motor domain, by showing tACS-phase-dependent changes in cortical excitability as measured by concurrent motor evoked potentials (24)(25)(26) or tACSinduced enhancement and phase cancellation of peripheral tremor in healthy subjects and patients with Parkinson's disease using closed-loop protocols (27)(28)(29)(30). Yet, latest findings by Asamoah et al (31) revealed that tACS-effects on the motor cortex are dominated by cutaneous stimulation of peripheral nerves in the skin leading to rhythmic activation of the sensorimotor system rather than by transcranial modulation of cortical tissue. Thus, evidence for phasespecific neural effects of tACS in the motor domain might not necessarily be generalizable to transcranial entrainment effects in cortical regions apart from the motor cortex.…”

Section: Introductionmentioning

confidence: 99%

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Phase-specific manipulation of neural oscillatory activity by transcranial alternating current stimulation

Fiene

Schwab

Misselhorn

et al. 2019

Preprint

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Oscillatory phase has been proposed as key parameter defining the spatiotemporal structure of neural activity. Phase alignment of oscillations by transcranial alternating current stimulation (tACS) may offer a unique opportunity to enhance our understanding of brain rhythms and to alter brain function. However, the precise mechanism and effectiveness of tACS are still critically debated. Here, we investigated the phase-specificity of tACS effects on visually evoked steady state responses (SSR) measured by electroencephalography (EEG). Using an intermittent electrical stimulation protocol, we assessed the influence of tACS on SSR amplitude as a function of phase shift between rhythmic sensory and electrical stimulation in the interval immediately following tACS. Visual flicker was delivered at six different phase angles relative to the tACS cycle. Participants were presented with flicker and high-definition tACS over the occipital cortex at 10 Hz in two sessions using active or sham stimulation. We observed that the phase shift between flicker and tACS modulates evoked SSR amplitudes. The amplitude change over phase shift conditions was significant for both general and sinusoidal modulation measures. Neural sources of phase-specific effects were localized in the parietooccipital cortex within flicker-aligned regions. Importantly, tACS effects were stronger in subjects with lower phase locking between EEG and flicker. Overall, our data provide evidence for phase alignment of brain activity by tACS, since the change in SSR amplitude can only result from phase-specific interactions with the applied electric fields. This finding corroborates the physiological efficacy of tACS and highlights its potential for controlled modulation of brain signals. Keywordstranscranial alternating current stimulation (tACS), EEG, phase, alpha oscillations, visual flicker Significance StatementThe lacking proof of phase-specific effects of transcranial alternating current stimulation (tACS) on neural activity in humans still restricts its potential to advance knowledge on the functional significance of brain oscillations. We show that the phase shift between concurrent 10 Hz tACS and precisely controlled oscillatory activity via visual flicker modulated the amplitude of evoked neural oscillations. Interindividual differences in tACS effect size were dependent on the current brain state. Our findings provide electrophysiological evidence for the capability of tACS to phase-align intrinsic neural activity. These mechanistic insights emphasize the value of tACS to advance research on the causal role of brain rhythms and offer important implications for the treatment of disturbed oscillatory patterns and cortical connectivity in brain disorders.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Phase-specific manipulation of neural oscillatory activity by transcranial alternating current stimulation

Fiene

Schwab

Misselhorn

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…While positive results in published studies provide evidence of causality, it remains important to optimize our methods if we to demonstrate causality beyond reasonable doubt: Otherwise any subsequent failure to replicate might be mistakenly interpreted as an absence of a causal role of these mechanisms on underlying neural processes (e.g., speech perception). Furthermore, concerns have already been raised concerning analytic methods used in existing studies (e.g., Asamoah et al, 2019a), and the possibility of peripheral effects of electrical stimulation (e.g., Asamoah, Khatoun, & Mc Laughlin, 2019b).…”

Section: Methodological Implicationsmentioning

confidence: 99%

“…Kleinert, Szymanski, & Müller (2017) also reported that participants are unable to determine whether frontal and parietal regions were stimulated in-or out-of-phase from each other. Nevertheless, a recent study convincingly demonstrated that some tACS effects on the motor system can be explained by stimulation of peripheral nerves (Asamoah et al, 2019b). It is possible that this issue could also affect stimulation of the auditory system, which needs to be addressed in future work.…”

Section: Limitations and Future Directionsmentioning

confidence: 96%

Perception of rhythmic speech is modulated by focal bilateral tACS

Zoefel¹,

Allard²,

Anil³

et al. 2019

Preprint

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Several recent studies have used transcranial alternating stimulation (tACS) to demonstrate a causal role of neural oscillatory activity in speech processing. In particular, it has been shown that the ability to understand speech in a multi-speaker scenario or background noise depends on the timing of speech presentation relative to simultaneously applied tACS. However, it is possible that tACS did not change actual speech perception but rather auditory stream segregation. In this study, we tested whether the phase relation between tACS and the rhythm of degraded words, presented in silence, modulates word report accuracy. We found strong evidence for a tACS-induced modulation of speech perception, but only if the stimulation was applied bilaterally using ring electrodes (not for unilateral left hemisphere stimulation with square electrodes). These results were only obtained when data was analyzed using a statistical approach that was identified as optimal in a previous simulation study. The effect was driven by a phasic disruption of word report scores. Our results suggest a causal role of neural entrainment for speech perception and emphasize the importance of optimizing stimulation protocols and statistical approaches for brain stimulation research.

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“…This neural tracking is linked to speech processing: neural tracking is stronger when sentences are intelligible (Peelle, Gross, and Davis 2013;Ding and Simon 2013) and indicates how the speech signal is parsed in the brain (Kösem et al 2018;Ding et al 2016;Ten Oever and Sack 2015). tACS is thought to influence neural tracking by modulating oscillatory activity of neural networks (Fröhlich and McCormick 2010;Witkowski et al 2016;Thut, Schyns, and Gross 2011) (but see (Asamoah, Khatoun, and Mc Laughlin 2019)), and hence may provide a technique to test for a causal influence of neural tracking on the comprehension of spoken language. So far, most tACS studies on speech have focused on effects of tACS phase, that is, how the temporal alignment of the tACS current and speech envelope affect speech comprehension.…”

Section: Introductionmentioning

confidence: 99%

Biasing the perception of spoken words with tACS

Kösem

Bosker

Jensen

et al. 2019

Preprint

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Recent neuroimaging evidence suggests that the frequency of entrained oscillations in auditory cortices influences the perceived duration of speech segments, impacting word perception (Kösem et al. 2018). We further tested the causal influence of neural entrainment frequency during speech processing, by manipulating entrainment with continuous transcranial alternating current stimulation (tACS) at distinct oscillatory frequencies (3 Hz and 5.5 Hz) above the auditory cortices. Dutch participants listened to speech and were asked to report their percept of a target Dutch word, which contained a vowel with an ambiguous duration. Target words were presented either in isolation (first experiment) or at the end of spoken sentences (second experiment). We predicted that the frequency of the tACS current would influence neural entrainment and therewith how speech is perceptually sampled, leading to a perceptual over-or underestimation of the vowel duration. Experiment 1 revealed no significant result. In contrast, results from experiment 2 showed a significant effect of tACS frequency on target word perception. Faster tACS lead to more long-vowel word percepts, in line with previous findings suggesting that neural oscillations are instrumental in the temporal processing of speech. The different results from the two experiments suggest that the impact of tACS is dependent on the sensory context. tACS may have a stronger effect on spoken word perception when the words are presented in a continuous stream of speech as compared to when they are isolated, potentially because prior (stimulus-induced) entrainment of brain oscillations might be a prerequisite for tACS to be effective.

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tACS motor system effects can be caused by transcutaneous stimulation of peripheral nerves

Cited by 223 publications

References 66 publications

Phase-specific manipulation of neural oscillatory activity by transcranial alternating current stimulation

Phase-specific manipulation of neural oscillatory activity by transcranial alternating current stimulation

Perception of rhythmic speech is modulated by focal bilateral tACS

Biasing the perception of spoken words with tACS

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