Bi-frontal transcranial alternating current stimulation in the ripple range reduced overnight forgetting

Géza Gergely Ambrus,Andrea Antal,Alberto Pisoni,Zsolt Turi,Annika Primaßin,Walter Paulus

doi:10.3389/fncel.2015.00374

Abstract

High frequency oscillations in the hippocampal structures recorded during sleep have been proved to be essential for long-term episodic memory consolidation in both animals and in humans. The aim of this study was to test if transcranial Alternating Current Stimulation (tACS) of the dorsolateral prefrontal cortex (DLPFC) in the hippocampal ripple range, applied bi-frontally during encoding, could modulate declarative memory performance, measured immediately after encoding, and after a night's sleep. An associative word-pair learning test was used. During an evening encoding phase, participants received 1 mA 140 Hz tACS or sham stimulation over both DLPFCs for 10 min while being presented twice with a list of word-pairs. Cued recall performance was investigated 10 min after training and the morning following the training session. Forgetting from evening to morning was observed in the sham condition, but not in the 140 Hz stimulation condition. 140 Hz tACS during encoding may have an effect on the consolidation of declarative material.

Highlights

Memory formation is a dynamic process, which requires continuous encoding of new pieces of information and subsequent long-term consolidation (Frankland and Bontempi, 2005; Axmacher et al, 2008; Kuhl et al, 2010; O’Neill et al, 2010)
The present study investigates the effects of transcranial Alternating Current Stimulation (tACS) on memory performance, applied in the hippocampal ripple frequency range, at 140 Hz, in awake participants during the encoding phase of a word-pair learning task
In the active stimulation condition participants performed at 71.26% (32.78 ± 8.16 words) in the evening test phase and 72.22% (33.22 ± 8.72 words) in the morning retest phase

Summary

Introduction

Memory formation is a dynamic process, which requires continuous encoding of new pieces of information and subsequent long-term consolidation (Frankland and Bontempi, 2005; Axmacher et al, 2008; Kuhl et al, 2010; O’Neill et al, 2010). The formation of a stable representation of the encoded material involves temporally-structured and precisely coordinated communication between the hippocampal structures and the neocortex (Sirota et al, 2003; Frankland and Bontempi, 2005; Logothetis et al, 2012) This dialogue is characterized by slow-frequency (0.5–4 Hz) and high-frequency oscillations (or so-called ripples; 100–200 Hz), each oscillation is believed to serve different functions within the mnemonic process (Buzsáki, 1989; O’Neill et al, 2010). Ripple-range tACS and overnight forgetting this process might reflect the transfer of memory representations from the hippocampus to various neocortical regions including the frontal and temporal lobes (Axmacher et al, 2008) This combined activity outlines a pattern of synchronized upregulations in several cortical foci, including mainly association cortices, parietal and early sensory cortices (but not the primary visual cortex). Results from animal studies suggest that the experimental alteration of these precisely orchestrated and temporally structured oscillations can lead to functionally relevant changes in the animal’s behavior (Buzsáki, 1989; Girardeau et al, 2009; Jadhav et al, 2012; Varga et al, 2012)

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