Dose-Dependent Effects of Closed-Loop tACS Delivered During Slow-Wave Oscillations on Memory Consolidation

Abstract

Sleep is critically important to consolidate information learned throughout the day. Slow-wave sleep (SWS) serves to consolidate declarative memories, a process previously modulated with open-loop non-invasive electrical stimulation, though not always effectively. These failures to replicate could be explained by the fact that stimulation has only been performed in open-loop, as opposed to closed-loop where phase and frequency of the endogenous slow-wave oscillations (SWOs) are matched for optimal timing. The current study investigated the effects of closed-loop transcranial Alternating Current Stimulation (tACS) targeting SWOs during sleep on memory consolidation. 21 participants took part in a three-night, counterbalanced, randomized, single-blind, within-subjects study, investigating performance changes (correct rate and F1 score) on images in a target detection task over 24 h. During sleep, 1.5 mA closed-loop tACS was delivered in phase over electrodes at F3 and F4 and 180° out of phase over electrodes at bilateral mastoids at the frequency (range 0.5–1.2 Hz) and phase of ongoing SWOs for a duration of 5 cycles in each discrete event throughout the night. Data were analyzed in a repeated measures ANOVA framework, and results show that verum stimulation improved post-sleep performance specifically on generalized versions of images used in training at both morning and afternoon tests compared to sham, suggesting the facilitation of schematization of information, but not of rote, veridical recall. We also found a surprising inverted U-shaped dose effect of sleep tACS, which is interpreted in terms of tACS-induced faciliatory and subsequent refractory dynamics of SWO power in scalp EEG. This is the first study showing a selective modulation of long-term memory generalization using a novel closed-loop tACS approach, which holds great potential for both healthy and neuropsychiatric populations.

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“…98; reviewed in Refs. 137,138), recent studies indicate that, due to the subthreshold character of the stimulation, covert interactions between the applied stimulation, inter-individual confounds and content can play a decisive role in the efficiency of oscillatory weak electric stimulation (57,62). In rodents, reinforcing the temporal coordination of cortical delta waves and spindles using SPWR-triggered electrical stimulation resulted in a reorganization of spatio-temporal spiking patterns of prefrontal pyramidal neurons, along with subsequent increased recall performance relative to controls (72).…”

One-Shot Tagging During Wake and Cueing During Sleep With Spatiotemporal Patterns of Transcranial Electrical Stimulation Can Boost Long-Term Metamemory of Individual Episodes in Humans

“…Seventh, the application of STAMPs was limited to the presence of SWOs during sleep, and so the optimal dose may not be deliverable to a subject due to impoverished SW activity. A potential strategy is to employ SW tACS to boost SWOs (Jones et al, 2018;Ketz et al, 2018) in alternating blocks with STAMPs. However, our recent attempt at this strategy failed to boost the consolidation of individual sequential experiences (Lerner et al, 2019).…”

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“…13,137,146 Some attempts of open-loop tACS or closed-loop protocols went around the artifact issue by using short durations of stimulation (a few tACS cycles) and then recorded the immediate EEG aftereffects. 147,148…”