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Front. Neurosci. | doi: 10.3389/fnins.2018.00867

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

  • 1Psychology Clinical Neuroscience Center/Department of Psychology, University of New Mexico, United States
  • 2Center for Human-Machine Collaboration, Information and Systems Sciences Laboratory, HRL Laboratories (United States), United States
  • 3Mind Research Network (MRN), United States

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 hours. During sleep, 1.5 mA closed-loop tACS was delivered in phase over electrodes at F3 and F4 and 180o out of phase over electrodes at bilateral mastoids at the frequency (range 0.5 to 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 facilitatory 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.

Keywords: closed-loop, transcranial alternating current stimulation (tACS), memory consolidation, Sleep, Learning, transcranial direct current stimulation (tDCS), learning and memory

Received: 13 Aug 2018; Accepted: 06 Nov 2018.

Edited by:

Shapour Jaberzadeh, Monash University, Australia

Reviewed by:

Michele Bellesi, Università Politecnica delle Marche, Italy
Surjo R. Soekadar, Klinik für Psychiatrie und Psychotherapie, Universitätsklinikum Tübingen, Germany  

Copyright: © 2018 Jones, Choe, Bryant, Robinson, Ketz, Skorheim, Combs, Lamphere, Robert, Gill, Heinrich, Howard, Clark and Pilly. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence:
Dr. Vincent P. Clark, University of New Mexico, Psychology Clinical Neuroscience Center/Department of Psychology, Albuquerque, 87131, New Mexico, United States, vclark@unm.edu
Dr. Praveen K. Pilly, HRL Laboratories (United States), Center for Human-Machine Collaboration, Information and Systems Sciences Laboratory, Malibu, 90265, California, United States, Pkpilly@hrl.com