Abstract

Slow-wave sleep (SWS) has been shown to promote long-term consolidation of episodic memories in hippocampo–neocortical networks. Previous research has aimed to modulate cortical sleep slow-waves and spindles to facilitate episodic memory consolidation. Here, we instead aimed to modulate hippocampal activity during slow-wave sleep using transcranial direct current stimulation in 18 healthy humans. A pair-associate episodic memory task was used to evaluate sleep-dependent memory consolidation with face–occupation stimuli. Pre- and post-nap retrieval was assessed as a measure of memory performance. Anodal stimulation with 2 mA was applied bilaterally over the lateral temporal cortex, motivated by its particularly extensive connections to the hippocampus. The participants slept in a magnetic resonance (MR)-simulator during the recordings to test the feasibility for a future MR-study. We used a sham-controlled, double-blind, counterbalanced randomized, within-subject crossover design. We show that stimulation vs. sham significantly increased slow-wave density and the temporal coupling of fast spindles and slow-waves. While retention of episodic memories across sleep was not affected across the entire sample of participants, it was impaired in participants with below-average pre-sleep memory performance. Hence, bi-temporal anodal direct current stimulation applied during sleep enhanced sleep parameters that are typically involved in memory consolidation, but it failed to improve memory consolidation and even tended to impair consolidation in poor learners. These findings suggest that artificially enhancing memory-related sleep parameters to improve memory consolidation can actually backfire in those participants who are in most need of memory improvement.

Highlights

  • The memory system most vulnerable to neurodegenerative disturbances is the episodic memory system, which stores and retrieves idiosyncratic experiences including spatiotemporal context [1]

  • We identified discrete spindle events over centro–parietal electrodes as in Helfrich et al [75] for all artifact-free EEG segments that contained NREM 2 (N2) and slow-wave sleep (SWS) and that followed the onset of transcranial direct-current stimulation (tDCS)/sham stimulation

  • We focused on centro– parietal fast spindle activity [76] because fast spindles seem to be involved in memory consolidation, e.g., [37,77]

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Summary

Introduction

The memory system most vulnerable to neurodegenerative disturbances is the episodic memory system, which stores and retrieves idiosyncratic experiences including spatiotemporal context [1]. Episodic memory is one of the most prominent cognitive abilities to steadily decline with healthy aging [2,3], accelerated in mild cognitive impairment and Alzheimer’s disease [4,5]. A deterioration of episodic memory is associated with several neuropsychiatric disorders including schizophrenia, bipolar disorder, and depression [6,7,8]. There is ample evidence that sleep plays a vital role in the normal functioning of episodic memory consolidation [9]. Reduced and altered slow-wave sleep (SWS) in patients with neuropsychiatric disorders may, at least in part, explain the patients’ memory deficits [10,11,12,13]. The modulation of memory-related processes during SWS is of interest as a treatment avenue to counter the deterioration of memory functions in neuropsychiatric disorders and aging

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