Immediate neurophysiological effects of transcranial electrical stimulation

Liu, Anli; Vöröslakos, Mihály; Kronberg, Greg; Henin, Simon; Krause, Matthew R.; Huang, Yu; Opitz, Alexander; Mehta, Ashesh D.; Pack, Christopher C.; Krekelberg, Bart; Berényi, Antal; Parra, Lucas C.; Melloni, Lucía; Devinsky, Orrin; Buzsáki, György

doi:10.1038/s41467-018-07233-7

Cited by 374 publications

(363 citation statements)

References 126 publications

(198 reference statements)

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“…For a given DCS polarity, the model predicts a linear relationship between field magnitude and mean plasticity effects ( Figure 8E). To first order this implies population mean effects of ~1% for fields of 1V/m (we observe ~20% effects for 20 V/m), in line with effect sizes observed for acute effects of DCS (70). However, experimentally we observe a saturation with increasing stimulation intensity ( Figure 8F).…”

Section: Dose Responsesupporting

confidence: 86%

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Direct current stimulation boosts associative Hebbian synaptic plasticity and maintains its pathway specificity

Kronberg

Rahman

Lafon³

et al. 2019

Preprint

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Background: There is evidence that transcranial direct current stimulation (tDCS) can improve learning performance. Arguably, this effect is related to long term potentiation (LTP), but the precise biophysical mechanisms remain unknown. Hypothesis: We propose that direct current stimulation (DCS) causes small changes in postsynaptic membrane potential during ongoing endogenous synaptic activity. The altered voltage dynamics in the postsynaptic neuron then modify synaptic strength via the machinery of endogenous voltage-dependent Hebbian plasticity. This hypothesis predicts that DCS should exhibit Hebbian properties, namely pathway specificity and associativity. Methods: We studied the effects of DCS applied during the induction of LTP in the CA1 region of rat hippocampal slices and using a biophysical computational model. Results: DCS enhanced LTP, but only at synapses that were undergoing plasticity, confirming that DCS respects Hebbian pathway specificity. When different synaptic pathways cooperated to produce LTP, DCS enhanced this cooperation, boosting Hebbian associativity. Further slice experiments and computer simulations support a model where polarization of postsynaptic pyramidal neurons drives these plasticity effects through endogenous Hebbian mechanisms. The model is able to reconcile several experimental results by capturing the complex interaction between the induced electric field, neuron morphology, and endogenous neural activity. Conclusions: These results suggest that tDCS can enhance associative learning. We propose that clinical tDCS should be applied during tasks that induce Hebbian plasticity to harness this phenomenon, and that the effects should be task specific through their interaction with endogenous plasticity mechanisms. Models that incorporate brain state and plasticity mechanisms may help to improve prediction of tDCS outcomes.Abbreviations: tDCS (transcranial direct current stimulation); DCS (direct current stimulation); LTP (long term potentiation); TBS (theta burst stimulation); STDP (spike-timing dependent plasticity) Effect of DCS on LTP is pathway specificHebbian synaptic plasticity is classically characterized as a pathway specific process, i.e. only pathways that are coactive with the postsynaptic neuron are strengthened (35). Our proposal that DCS enhances LTP through membrane potential implies that the effects of DCS should follow this pathway specificity. We tested this by monitoring two independent synaptic pathways in CA1 (Figure 2A). During induction, the strong pathway received TBS while the other inactive pathway was not stimulated. As expected, LTP was observed in the strong pathway ( Figure 2B black; 1.377+-0.052, N=16, p=2.8E-6), but not the inactive pathway ( Figure 2B gray; 0.986+-0.031, N=14, p=0.657), demonstrating the wellestablished pathway specificity of LTP (35). When this induction protocol was paired with anodal DCS, LTP was enhanced only in the strong pathway ( Figure 2B red; 1.613+-0.071, N=14, p=0.011 vs. control), while the inactive pathway was unaff...

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Section: Dose Responsesupporting

confidence: 86%

“…Perhaps the most well characterized cellular effect of electrical stimulation is the modulation of somatic membrane potential and firing probability (18,20,61,(65)(66)(67)(68)(69)(70). In human tDCS studies, it is the modulation of motor-evoked potentials, which have been linked to long-term plasticity (48,71,72).…”

Section: Mechanismmentioning

confidence: 99%

Direct current stimulation boosts associative Hebbian synaptic plasticity and maintains its pathway specificity

Kronberg

Rahman

Lafon³

et al. 2019

Preprint

Self Cite

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“…It may be possible to combine these influences to produce more effective stimulation 9 . Additionally, scalp stimulation may affect the vagus or other cranial nerves 10 . These effects will necessarily vary across brain regions and stimulation protocols, frustrating any simplistic interpretation of the tACS literature.…”

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confidence: 99%

tACS entrains neural activity while somatosensory input is blocked

Vieira

Krause

Pack

2019

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Recent results suggest that transcranial alternating current stimulation (tACS) can noninvasively change humans' mental states, but the neural mechanisms behind these exciting results remain poorly understood. Although tACS is traditionally thought to produce electrical fields that directly affect neurons in the targeted area, much of the current never reaches the brain, and flows through the skin instead. Since the skin is packed with somatosensory afferents, this shunted current can produce tactile percepts that affect subjects' behavior, even if the targeted brain area is otherwise unaffected.

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“…As suggested in some studies, processes leading to online effects of tACS and those leading to offline effects that sustain (or even manifest) after stimulation may rely on different neural mechanisms (Reato et al, 2010;Strüber et al, 2015). In a recent review paper on the immediate effects of tACS (Liu et al, 2018), five possible neural mechanisms were suggested: "stochastic resonance, rhythm resonance, temporal biasing of neuronal spikes, entrainment of network patterns, and imposed patterns". Importantly, how these mechanisms contribute to observed effects specifically and how they interact or compensate each other is largely unknown.…”

Section: Introductionmentioning

confidence: 99%

Transient amplitude modulation of alpha-band oscillations by short-time intermittent closed-loop tACS

Zarubin

Gundlach

Nikulin

et al. 2020

Preprint

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Non-invasive brain stimulation techniques such as transcranial alternating current stimulation (tACS) have recently become extensively utilized due to their potential to modulate ongoing neuronal oscillatory activity and consequently to induce cortical plasticity relevant for various cognitive functions. However, the neurophysiological basis for stimulation effects as well as their interindividual differences are not yet understood. In the present study we used a closed-loop EEG transcranial alternating current stimulation protocol (EEG-tACS) to examine the modulation of alpha oscillations generated in occipito-parietal areas. In particular, we investigated the effects of a repeated short-time intermittent stimulation protocol (1 s in every trial) applied over the visual cortex (Cz and Oz) and adjusted according to the phase and frequency of visual alpha oscillations on the amplitude of these oscillations. Based on previous findings, we expected higher increases in alpha amplitudes for tACS applied in-phase with ongoing oscillations as compared to an application in antiphase and this modulation to be present in low-alpha amplitude states of the visual system (eyes opened) but not high (eyes closed). Contrary to our expectations, we found a transient suppression of alpha power in inter-individually derived spatially specific parieto-occipital components obtained via the estimation of spatial filters by using the common spatial patterns approach. The amplitude modulation was independent of the phase relationship between tACS signal and alpha oscillations, and the state of the visual system manipulated via closed-and open-eye conditions. It was also absent in conventionally analyzed single-channel and multi-channel data from an average parieto-occipital region. The fact that the tACS modulation of oscillations was phase-independent suggests that mechanisms driving the effects of tACS may not be explained by entrainment alone, but rather require neuroplastic changes or transient disruption of neural oscillations. Our study also supports the notion that the response to tACS is subject specific, where the modulatory effects are shaped by the interplay between the stimulation and different alpha generators. This favors stimulation protocols as well as analysis regimes exploiting inter-individual differences, such as spatial filters to reveal otherwise hidden stimulation effects and, thereby, comprehensively induce and study the effects and underlying mechanisms of tACS.

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Immediate neurophysiological effects of transcranial electrical stimulation

Cited by 374 publications

References 126 publications

Direct current stimulation boosts associative Hebbian synaptic plasticity and maintains its pathway specificity

Direct current stimulation boosts associative Hebbian synaptic plasticity and maintains its pathway specificity

tACS entrains neural activity while somatosensory input is blocked

Transient amplitude modulation of alpha-band oscillations by short-time intermittent closed-loop tACS

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