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Electric field dynamics in the brain during multi-electrode transcranial electric stimulation.

ABSTRACT: Neural oscillations play a crucial role in communication between remote brain areas. Transcranial electric stimulation with alternating currents (TACS) can manipulate these brain oscillations in a non-invasive manner. Recently, TACS using multiple electrodes with phase shifted stimulation currents were developed to alter long-range connectivity. Typically, an increase in coordination between two areas is assumed when they experience an in-phase stimulation and a disorganization through an anti-phase stimulation. However, the underlying biophysics of multi-electrode TACS has not been studied in detail. Here, we leverage direct invasive recordings from two non-human primates during multi-electrode TACS to characterize electric field magnitude and phase as a function of the phase of stimulation currents. Further, we report a novel "traveling wave" stimulation where the location of the electric field maximum changes over the stimulation cycle. Our results provide a mechanistic understanding of the biophysics of multi-electrode TACS and enable future developments of novel stimulation protocols.

SUBMITTER: Alekseichuk I

PROVIDER: S-EPMC6561925 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Electric field dynamics in the brain during multi-electrode transcranial electric stimulation.

Alekseichuk Ivan I Falchier Arnaud Y AY Linn Gary G Xu Ting T Milham Michael P MP Schroeder Charles E CE Opitz Alexander A

Nature communications 20190612 1

Neural oscillations play a crucial role in communication between remote brain areas. Transcranial electric stimulation with alternating currents (TACS) can manipulate these brain oscillations in a non-invasive manner. Recently, TACS using multiple electrodes with phase shifted stimulation currents were developed to alter long-range connectivity. Typically, an increase in coordination between two areas is assumed when they experience an in-phase stimulation and a disorganization through an anti-p ...[more]

PMID: 31189931

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Project description:Brain oscillations, e.g. measured by electro- or magnetoencephalography (EEG/MEG), are causally linked to brain functions that are fundamental for perception, cognition and learning. Recent advances in neurotechnology provide means to non-invasively target these oscillations using frequency-tuned amplitude-modulated transcranial alternating current stimulation (AM-tACS). However, online adaptation of stimulation parameters to ongoing brain oscillations remains an unsolved problem due to stimulation artifacts that impede such adaptation, particularly at the target frequency. Here, we introduce a real-time compatible artifact rejection algorithm (Stimulation Artifact Source Separation, SASS) that overcomes this limitation. SASS is a spatial filter (linear projection) removing EEG signal components that are maximally different in the presence versus absence of stimulation. This enables the reliable removal of stimulation-specific signal components, while leaving physiological signal components unaffected. For validation of SASS, we evoked brain activity with known phase and amplitude using 10 Hz visual flickers across 7 healthy human volunteers. 64-channel EEG was recorded during and in absence of 10 Hz AM-tACS targeting the visual cortex. Phase differences between AM-tACS and the visual stimuli were randomized, so that steady-state visually evoked potentials (SSVEPs) were phase-locked to the visual stimuli but not to the AM-tACS signal. For validation, distributions of single-trial amplitude and phase of EEG signals recorded during and in absence of AM-tACS were compared for each participant. When no artifact rejection method was applied, AM-tACS stimulation artifacts impeded assessment of single-trial SSVEP amplitude and phase. Using SASS, amplitude and phase of single trials recorded during and in absence of AM-tACS were comparable. These results indicate that SASS can be used to establish adaptive (closed-loop) AM-tACS, a potentially powerful tool to target various brain functions, and to investigate how AM-tACS interacts with electric brain oscillations.

Project description:There is considerable individual variability in the reported effectiveness of non-invasive brain stimulation. This variability has often been ascribed to differences in the neuroanatomy and resulting differences in the induced electric field inside the brain. In this study, we addressed the question whether individual differences in the induced electric field can predict the neurophysiological and behavioral consequences of gamma band tACS. In a within-subject experiment, bi-hemispheric gamma band tACS and sham stimulation was applied in alternating blocks to the participants' superior temporal lobe, while task-evoked auditory brain activity was measured with concurrent functional magnetic resonance imaging (fMRI) and a dichotic listening task. Gamma tACS was applied with different interhemispheric phase lags. In a recent study, we could show that anti-phase tACS (180° interhemispheric phase lag), but not in-phase tACS (0° interhemispheric phase lag), selectively modulates interhemispheric brain connectivity. Using a T1 structural image of each participant's brain, an individual simulation of the induced electric field was computed. From these simulations, we derived two predictor variables: maximal strength (average of the 10,000 voxels with largest electric field values) and precision of the electric field (spatial correlation between the electric field and the task evoked brain activity during sham stimulation). We found considerable variability in the individual strength and precision of the electric fields. Importantly, the strength of the electric field over the right hemisphere predicted individual differences of tACS induced brain connectivity changes. Moreover, we found in both hemispheres a statistical trend for the effect of electric field strength on tACS induced BOLD signal changes. In contrast, the precision of the electric field did not predict any neurophysiological measure. Further, neither strength, nor precision predicted interhemispheric integration. In conclusion, we found evidence for the dose-response relationship between individual differences in electric fields and tACS induced activity and connectivity changes in concurrent fMRI. However, the fact that this relationship was stronger in the right hemisphere suggests that the relationship between the electric field parameters, neurophysiology, and behavior may be more complex for bi-hemispheric tACS.

Dataset Information

Electric field dynamics in the brain during multi-electrode transcranial electric stimulation.

Publications

Electric field dynamics in the brain during multi-electrode transcranial electric stimulation.

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