Low-frequency alternating current stimulation rhythmically suppresses gamma-band oscillations and impairs perceptual performance

Abstract

Low frequency oscillations such as alpha (8-12 Hz) are hypothesized to rhythmically gate sensory processing, reflected by 40-100 Hz gamma band activity, via the mechanism of pulsed inhibition. We applied transcranial alternating current stimulation (TACS) at individual alpha frequency (IAF) and flanking frequencies (IAF-4 Hz, IAF+4 Hz) to the occipital cortex of healthy human volunteers during concurrent magnetoencephalography (MEG), while participants performed a visual detection task inducing strong gamma-band responses. Occipital (but not retinal) TACS phasically suppressed stimulus-induced gamma oscillations in the visual cortex and impaired target detection, with stronger phase-to-amplitude coupling predicting behavioral impairments. Retinal control TACS ruled out retino-thalamo-cortical entrainment resulting from (subthreshold) retinal stimulation. All TACS frequencies tested were effective, suggesting that visual gamma-band responses can be modulated by a range of low frequency oscillations. We propose that TACS-induced membrane potential modulations mimic the rhythmic change in cortical excitability by which spontaneous low frequency oscillations may eventually exert their impact when gating sensory processing via pulsed inhibition.

Pulsed Facilitation of Corticospinal Excitability by the Sensorimotor μ-Alpha Rhythm

“…Also visual cortical excitability, indexed by perceptual performance or the probability of transcranial magnetic stimulation (TMS) to induce phosphenes has been inversely linked to occipital alpha power (Thut et al, 2006;Romei et al, 2008a,b;van Dijk et al, 2008) and is modulated by its phase (Busch et al, 2009;Mathewson et al, 2009;Dugué et al, 2011). Accordingly, transcranial alternating current stimulation (TACS) in the alpha range phasically suppressed visual stimulus-induced gamma power in concurrent MEG recordings, with the extent of phasic suppression predicting the accompanying decrease in visual detection performance (Herring et al, 2019).…”

Theta Phase-dependent Modulation of Perception by Concurrent Transcranial Alternating Current Stimulation and Periodic Visual Stimulation

“…Demiralp et al, 2007;Lakatos et al, 2005;Landau, Schreyer, Van Pelt, & Fries, 2015;Spyropoulos, Bosman, & Fries, 2018) and alpha (e.g. Herring, Esterer, Marshall, Jensen, & Bergmann, 2019;Spaak, Bonnefond, Maier, Leopold, & Jensen, 2012) oscillations have been associated with the modulation of visual processing through modulating gamma oscillations. However, alpha oscillations were associated with selective attention on a single stimulus (e.g.…”

Brain State-Dependent Brain Stimulation

“…Yet, the most important challenge will be to develop truly closed-loop BSDBS (Figure 1B ) that allows to continuously monitor the brain signals of interest, while concurrently applying NIBS to achieve and maintain the desired brain state and to control perception or behavior. The successful real-time removal of TMS/TCS stimulation artifacts (Walter et al, 2012 ; Herring et al, 2015 ; Rogasch et al, 2017 ) and EEG correlates of multisensory co-stimulation during TMS (Herring et al, 2015 ; Conde et al, in press ) and TCS (Schutter, 2016 ; Herring et al, 2018 ) is therefore a core developmental goal for the near future.…”