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.
Highlights
Sleep is hypothesized to promote the consolidation of information from short-term stores to more schematized long-term representations (Fenn et al, 2003; Stickgold and Walker, 2013; Sterpenich et al, 2014; Friedrich et al, 2015)
In this study and Ketz et al (2018), we investigated the effects of combining transcranial Direct Current Stimulation (tDCS) during waking training and closed-loop transcranial Alternating Current Stimulation (tACS) during slow-wave oscillations on memory performance assessed over 24 h
To better understand the contribution of closed-loop tACS to sleep-dependent memory generalization, we analyzed dose effects of tACS event count through the night on raw performance in correct rate and F1 score at morning and afternoon tests for both generalized and repeated images separately, as well as the contrast in generalized vs. repeated overnight performance changes, across participants and between the two experimental nights
Summary
Sleep is hypothesized to promote the consolidation of information from short-term stores to more schematized long-term representations (Fenn et al, 2003; Stickgold and Walker, 2013; Sterpenich et al, 2014; Friedrich et al, 2015). Slow-wave oscillations (SWOs) are a global neural phenomenon exhibiting synchronized EEG activity at a frequency peaking at 0.7–0.8 Hz, which appear to be involved in declarative memory consolidation (Plihal and Born, 1997; Marshall and Born, 2007; Diekelmann and Born, 2010; Rasch and Born, 2013) They are thought to promote large-scale neuronal synchronization across cortical and sub-cortical regions (Timofeev et al, 2012), which is ideal for coordinated reactivations (or replays) across disparate brain regions, facilitating the transfer of information from hippocampal to neocortical areas (Squire and Alvarez, 1995). Sleep-dependent consolidation effects have been revealed in innumerable studies with various forms of information, including extraction of the hidden structure of digit strings (Wagner et al, 2004) and Serial Reaction Time Task patterns (Fischer et al, 2006), as well as incorporation of new words into an existing vocabulary (Tamminen et al, 2010)
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