Closed-loop slow-wave tACS improves sleep-dependent long-term memory generalization by modulating endogenous oscillations

Abstract

Benefits in long-term memory retention and generalization have been shown to be related to sleep-dependent processes, which correlate with neural oscillations as measured by changes in electric potential. The specificity and causal role of these oscillations, however, are still poorly understood. Here, we investigated the potential for augmenting endogenous slow-wave (SW) oscillations in humans with closedloop transcranial alternating current stimulation (tACS) with an aim toward enhancing the consolidation of recent experiences into long-term memory. Sixteen (three female) participants were trained presleep on a target detection task identifying targets hidden in complex visual scenes. During post-training sleep, closed-loop SW detection and stimulation were used to deliver tACS matching the phase and frequency of the dominant oscillation in the range of 0.5–1.2 Hz. Changes in performance were assessed the following day using test images that were identical to the training (“repeated”), and images generated from training scenes but with novel viewpoints (“generalized”). Results showed that active SW tACS during sleep enhanced the postsleep versus presleep target detection accuracy for the generalized images compared with sham nights, while no significant change was found for repeated images. Using a frequencyagnostic clustering approach sensitive to stimulation-induced spectral power changes in scalp EEG, this behavioral enhancement significantly correlated with both a poststimulation increase and a subsequent decrease in measured spectral power within theSWband, which in turn showed increased coupling with spindle amplitude. These results suggest that augmenting endogenous SW oscillations can enhance consolidation by specifically improving generalization over recognition or cued recall.