tACS Artifact Research Articles

Comb filters for the removal of transcranial current stimulation artifacts from single channel EEG recordings

Abstract The combination of transcranial alternating current stimulation (tACS) and electroencephalogram (EEG) for mobile and home-based interventions offers the potential for control and adaptation of stimulation parameters. Yet, during stimulation, the EEG is heavily affected by stimulation artifacts. Spatial filters are often unsuited because too few channels are recorded and hardware capabilities are limited. Due to their speed and as they can be used for single channels, we explore the performance of single-channel weighted comb filters on artifact removal. At any given time point t, the recording r(t) is a superposition of a neurophysiological signal n(t), the stimulation artifact a(t) and noise e(t). Now, we can estimate the artifact a(t) based on the recording from an earlier (or later) time-point shifted by the artifacts period. A weighted estimate based on multiple time points has the potential to improve the signal recovery. Therefore, we explored several approaches and evaluated their performance on simulated and real data. The comb kernel filters were implemented in Matlab (https://github.com/agricolab/ARtACS) and Python (https://github.com/agricolab/pyARtACS), and the code is open access under an X11-license. We found that independent of the weighting function, all comb filters exhibit similarity in their suppression of the DC component, the artifacts frequency, and its harmonics. Yet, different weighting functions exhibit different pass-band performance, evident as ringing and amplification, and their induction of time-domain echoes. Interestingly, we note that a causal uniform filter is comparable to more complex approaches, while offering the option for real-time filtering. Comb filters are able to remove tACS artifacts even if only a single channel is available. As comb filters require no assumptions about the shape of the artifact, they might also be useful for filtering of non-sinusoidal, e.g. pulsed or saw-tooth, transcranial current stimulation.

Signal-Space Projection Suppresses the tACS Artifact in EEG Recordings.

BackgroundTo probe the functional role of brain oscillations, transcranial alternating current stimulation (tACS) has proven to be a useful neuroscientific tool. Because of the excessive tACS-caused artifact at the stimulation frequency in electroencephalography (EEG) signals, tACS + EEG studies have been mostly limited to compare brain activity between recordings before and after concurrent tACS. Critically, attempts to suppress the artifact in the data cannot assure that the entire artifact is removed while brain activity is preserved. The current study aims to evaluate the feasibility of specific artifact correction techniques to clean tACS-contaminated EEG data.New MethodIn the first experiment, we used a phantom head to have full control over the signal to be analyzed. Driving pre-recorded human brain-oscillation signals through a dipolar current source within the phantom, we simultaneously applied tACS and compared the performance of different artifact-correction techniques: sine subtraction, template subtraction, and signal-space projection (SSP). In the second experiment, we combined tACS and EEG on one human subject to demonstrate the best-performing data-correction approach in a proof of principle.ResultsThe tACS artifact was highly attenuated by SSP in the phantom and the human EEG; thus, we were able to recover the amplitude and phase of the oscillatory activity. In the human experiment, event-related desynchronization could be restored after correcting the artifact.Comparison With Existing MethodsThe best results were achieved with SSP, which outperformed sine subtraction and template subtraction.ConclusionOur results demonstrate the feasibility of SSP by applying it to a phantom measurement with pre-recorded signal and one human tACS + EEG dataset. For a full validation of SSP, more data are needed.

A computationally efficient method for the attenuation of alternating current stimulation artifacts in electroencephalographic recordings

Objective. Recent studies suggest that the use of noninvasive closed-loop neuromodulation combining electroencephalography (EEG) and transcranial alternating current stimulation (tACS) may be a promising avenue for the treatment of neurological disorders. However, the attenuation of tACS artifacts in EEG data is particularly challenging, and computationally efficient methods are needed to enable closed-loop neuromodulation experiments. Here we introduce an original method to address this methodological issue. Approach. Our alternating current regression (AC-REG) method is an adaptive (time-varying) spatial filtering method. It relies on a data buffer of preset size, on which principal component analysis (PCA) is applied. The resulting components are used to build a spatial filter capable of regressing periodic signals in phase with the stimulation. PCA is performed each time that a new sample enters the buffer, such that the spatial filter can be continuously updated and applied to the EEG data. Main results. The AC-REG accuracy in terms of tACS artifact attenuation was assessed using simulated and real EEG data. Alternative offline processing techniques, such as the superimposition of moving averages (SMA) and the Helfrich method (HeM), were used as benchmark. Using simulations, we found that AC-REG can yield a more reliable reconstruction of the stimulation signal for any frequency between 1 and 80 Hz. Analysis of real EEG data of 18 healthy volunteers showed that AC-REG was able to better recover hidden neural activity as compared to SMA and HeM. Also, significantly higher correlations between power spectrum densities in tACS on and off conditions, respectively, were obtained using AC-REG (r = 0.90) than using SMA (r = 0.80) and HeM (r = 0.86). Significance. Thanks to its low computational complexity, the AC-REG method can be employed in noninvasive closed-loop neuromodulation experiments, with potential applications both in healthy individuals and in neurological patients.

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

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.

Removal of Gross Artifacts of Transcranial Alternating Current Stimulation in Simultaneous EEG Monitoring.

Transcranial electrical stimulation is a widely used non-invasive brain stimulation approach. To date, EEG has been used to evaluate the effect of transcranial Direct Current Stimulation (tDCS) and transcranial Alternating Current Stimulation (tACS), but most studies have been limited to exploring changes in EEG before and after stimulation due to the presence of stimulation artifacts in the EEG data. This paper presents two different algorithms for removing the gross tACS artifact from simultaneous EEG recordings. These give different trade-offs in removal performance, in the amount of data required, and in their suitability for closed loop systems. Superposition of Moving Averages and Adaptive Filtering techniques are investigated, with significant emphasis on verification. We present head phantom testing results for controlled analysis, together with on-person EEG recordings in the time domain, frequency domain, and Event Related Potential (ERP) domain. The results show that EEG during tACS can be recovered free of large scale stimulation artifacts. Previous studies have not quantified the performance of the tACS artifact removal procedures, instead focusing on the removal of second order artifacts such as respiration related oscillations. We focus on the unresolved challenge of removing the first order stimulation artifact, presented with a new multi-stage validation strategy.

Facilitated Event-Related Power Modulations during Transcranial Alternating Current Stimulation (tACS) Revealed by Concurrent tACS-MEG.

Non-invasive approaches to modulate oscillatory activity in the brain are increasingly popular in the scientific community. Transcranial alternating current stimulation (tACS) has been shown to modulate neural oscillations in a frequency-specific manner. However, due to a massive stimulation artifact at the targeted frequency, little is known about effects of tACS during stimulation. It remains unclear how the continuous application of tACS affects event-related oscillations during cognitive tasks. Depending on whether tACS influences pre- or post-stimulus oscillations, or both, the endogenous, event-related oscillatory dynamics could be pushed in various directions or not at all. A better understanding of these effects is crucial to plan, predict, and understand outcomes of solely behavioral tACS experiments. In the present study, a recently proposed procedure to suppress tACS artifacts by projecting MEG data into source-space using spatial filtering was utilized to recover event-related power modulations in the alpha-band during a mental rotation task. MEG data of 25 human subjects was continuously recorded. After 10-minute baseline measurement, participants received either 20 minutes of tACS at their individual alpha frequency or sham stimulation. Another 40 minutes of MEG data were acquired thereafter. Data were projected into source-space and carefully examined for residual artifacts. Results revealed strong facilitation of event-related power modulations in the alpha-band during tACS application. These results provide first direct evidence that tACS does not counteract top-down suppression of intrinsic oscillations, but rather enhances pre-existent power modulations within the range of the individual alpha (= stimulation) frequency.

Proceedings #17. A simple reason why beamformer may (not) remove the tACS-induced artifact in MEG

Transcranial alternating current simulation (tACS) combined synchronously with magnetoencephalography (MEG) could be a useful tool for studying brain oscillations and their relation to cognitive functions, but the method, however, suffers from large tACS-induced MEG artifacts. Conventional beamformer methods have been suggested for removing—or at least reducing—the artifact, but its functioning principle is not yet fully understood. We demonstrate the reason behind the beamformer’s ability to remove/reduce the tACS artifact (and other mutually correlated noise sources) with simple theoretical reasoning and simulations. In addition, at odds with previous suggestions, we show how the imperfections of this removal method could be explained with basic linear algebra without any need to consider nonlinear effects.

P189 Transcranial modulation of visually induced gamma power: a concurrent TACS-MEG study

Introduction Alpha oscillations (8–12 Hz) are proposed to mediate ‘attentional gating’ by suppressing neuronal processing in task-irrelevant sensory regions, reflected by ‘pulsed-inhibition’ of stimulus-induced gamma-band activity (40–100 Hz). Concurrent TACS-MEG has the potential to reveal TACS entrainment of alpha oscillations at the stimulation site and thus their causal impact on neuronal activity representing stimulus processing. Objectives We aimed to provide evidence that TACS can entrain the phase of alpha oscillations in the visual cortex by assessing its modulatory impact on the power of visual stimulus-induced gamma oscillations via simultaneous MEG recordings. Materials & methods TACS was applied during MEG in intermingled 5.4s trials either in Oz-Cz or FPz-Cz montage. Montage and stimulation frequency were randomized across trials, applying either individual alpha frequency (IAF), IAF−4 Hz, IAF+4 Hz, or no stimulation, resulting in a 2 (Montage) × 3 (Frequency) design plus a ‘NoStim’ condition. Stimulation intensity for both montages was adjusted separately to 95% retinal phosphene threshold. Participants performed a simple visual detection task, attending an inward moving grating, known to induce strong occipital gamma responses. TACS artifacts were reduced via regression methods, LCMV beamformer time-course extraction from the visual cortex, and high-pass filtering. Importantly, the gamma frequency of interest (∼50–60 Hz) was largely unaffected by TACS artifacts. We compared TACS-to-gamma phase-power coupling (PAC) for the respective experimental conditions. Results We found a rhythmic modulation of stimulus-induced gamma power by TACS at IAF (i.e., TACS-gamma phase-amplitude coupling) for the Oz-Cz montage, but not for the FPz-Cz montage which was introduced to control for subthreshold retinal entrainment effects. Conclusion Our findings (i) demonstrate that concurrent TACS-MEG can principally be used to study cross-frequency-coupling between transcranially entrained slower and spontaneous or stimulus-related faster oscillations, (ii) cannot merely result from subthreshold retinal entrainment, and (iii) suggest that alpha oscillations are indeed a possible means for top-down suppression of bottom-up sensory processing.

P166 Evidence for state dependent direct effects of alpha band transcranial alternating current stimulation

Introduction Transcranial alternating current stimulation (tACS) is used to modulate brain oscillations to measure changes in cognitive function. It is only since recently that brain activity in human subjects during tACS can be investigated. Objectives In the current study we examine entrainment effects caused by tACS at the individual alpha frequency (IAF) in humans. Material & methods We analyze magnetoencephalographic (MEG) data transformed to source space following a method we recently showed to diminish the tACS artifact, which makes analysis of brain activity during tACS possible. Using source level data from our previous study here we investigate the phase relationship (coherence) between the external tACS and the neural signal in two resting state condition. Results We find proof of entrainment in visual cortex areas. Interestingly, this entrainment is only significant when subjects had their eyes open; visual areas were not significantly entrained to tACS when subjects closed their eyes. Furthermore, we find considerable variation across subjects in the delay between tACS and the entrained brain activity. Conclusion In conclusion, tACS at individual alpha frequency entrains brain activity in visual cortices, however, in a state dependent manner as this effect can only clearly be observed with eyes open.

Faith and oscillations recovered: On analyzing EEG/MEG signals during tACS

Despite recent success in analyzing brain oscillations recorded during transcranial alternating current stimulation (tACS), the field still requires further research to establish standards in artifact removal methods. This includes taking a step back from the removal of the tACS artifact and thoroughly characterizing the to-be-removed artifact. A recent study by Noury et al. (2016) contributed importantly to this endeavour by showing the existence of nonlinear artefacts in the tACS signal as seen by MEG and EEG. Unfortunately however this paper conveys the message that current artifact removal attempts have failed altogether and that—based on these available tools—brain oscillations recorded during tACS cannot be analyzed using MEG and EEG. Here we want to balance this overly pessimistic conclusion: In-depth reanalyses of our own data and phantom-head measurements indicate that nonlinearities can occur, but only when technical limits of the stimulator are reached. As such they are part of the “real” stimulation and not a specific MEG analysis problem. Future tACS studies should consider these technical limits to avoid any nonlinear modulations of the tACS artifact. We conclude that even with current approaches, brain oscillations recorded during tACS can be meaningfully studied in many practical cases.

Concurrent Electroencephalography Recording During Transcranial Alternating Current Stimulation (tACS)

Oscillatory brain activities are considered to reflect the basis of rhythmic changes in transmission efficacy across brain networks and are assumed to integrate cognitive neural processes. Transcranial alternating current stimulation (tACS) holds the promise to elucidate the causal link between specific frequencies of oscillatory brain activity and cognitive processes. Simultaneous electroencephalography (EEG) recording during tACS would offer an opportunity to directly explore immediate neurophysiological effects of tACS. However, it is not trivial to measure EEG signals during tACS, as tACS creates a huge artifact in EEG data. Here we explain how to set up concurrent tACS-EEG experiments. Two necessary considerations for successful EEG recording while applying tACS are highlighted. First, bridging of the tACS and EEG electrodes via leaking EEG gel immediately saturates the EEG amplifier. To avoid bridging via gel, the viscosity of the EEG gel is the most important parameter. The EEG gel must be viscous to avoid bridging, but at the same time sufficiently fluid to create contact between the tACS electrode and the scalp. Second, due to the large amplitude of the tACS artifact, it is important to consider using an EEG system with a high resolution analog-to-digital (A/D) converter. In particular, the magnitude of the tACS artifact can exceed 100 mV at the vicinity of a stimulation electrode when 1 mA tACS is applied. The resolution of the A/D converter is of importance to measure good quality EEG data from the vicinity of the stimulation site. By following these guidelines for the procedures and technical considerations, successful concurrent EEG recording during tACS will be realized.

Concurrent Electroencephalography Recording During Transcranial Alternating Current Stimulation (tACS).

Oscillatory brain activities are considered to reflect the basis of rhythmic changes in transmission efficacy across brain networks and are assumed to integrate cognitive neural processes. Transcranial alternating current stimulation (tACS) holds the promise to elucidate the causal link between specific frequencies of oscillatory brain activity and cognitive processes. Simultaneous electroencephalography (EEG) recording during tACS would offer an opportunity to directly explore immediate neurophysiological effects of tACS. However, it is not trivial to measure EEG signals during tACS, as tACS creates a huge artifact in EEG data. Here we explain how to set up concurrent tACS-EEG experiments. Two necessary considerations for successful EEG recording while applying tACS are highlighted. First, bridging of the tACS and EEG electrodes via leaking EEG gel immediately saturates the EEG amplifier. To avoid bridging via gel, the viscosity of the EEG gel is the most important parameter. The EEG gel must be viscous to avoid bridging, but at the same time sufficiently fluid to create contact between the tACS electrode and the scalp. Second, due to the large amplitude of the tACS artifact, it is important to consider using an EEG system with a high resolution analog-to-digital (A/D) converter. In particular, the magnitude of the tACS artifact can exceed 100 mV at the vicinity of a stimulation electrode when 1 mA tACS is applied. The resolution of the A/D converter is of importance to measure good quality EEG data from the vicinity of the stimulation site. By following these guidelines for the procedures and technical considerations, successful concurrent EEG recording during tACS will be realized.

A novel approach for the removal of tACS artifacts from high-density EEG recordings

Event Abstract Back to Event A novel approach for the removal of tACS artifacts from high-density EEG recordings Thiago Santos Monteiro1, Kirstin F. Heise1*, Stephan P. Swinnen1 and Dante Mantini1, 2 1 KU Leuven, Faculty of Kinesiology and Rehabilitation Science, Belgium 2 ETH Zurich, Department of Health Sciences and Technology, Switzerland Concurrent application of electroencephalography (EEG) and non-invasive brain stimulation with alternating electrical current (tACS) holds great potential for retrieving information about causal relationships between neural activity and behaviour (1). Principal component analysis (PCA) is the method currently used to separate neural activity and stimulation artifacts that are mixed in EEG recordings PCA (2). Importantly, the use of PCA may alter phase relationships between target areas. Furthermore, the approach has been developed for and applied to few EEG electrodes, and has not been implemented for high-density (hd-) EEG recordings. Based on a validation procedure using real resting-state hd-EEG data and a simulated tACS artefact we compared the performance of PCA with a novel combination of advanced filtering methods (Hampel filtering based on windowed version of autoregressive modelled artefact, wAR/HF) (3). While the wAR/HF approach is more precise in removing the excessive tACS artefact from the hd-EEG signal thereby retaining the frequencies of interest (figure 1A depicts deviation from original signal after artefact removal averaged across all channels, figure 1B indicates deviation in relative power distribution), the PCA is more stable for retaining the interregional phase relationships. This work constitutes a critical methodological step to allow for the application of concurrent tACS in hd-EEG, which may permit the study of causal relationship between oscillatory activity in the brain and behaviour. Figure 1