Odor cueing during slow-wave sleep benefits memory independently of low cholinergic tone - PubMed (original) (raw)

Odor cueing during slow-wave sleep benefits memory independently of low cholinergic tone

Jens G Klinzing et al. Psychopharmacology (Berl). 2018 Jan.

Abstract

Rationale: Sleep-dependent memory consolidation depends on the concerted reactivation of memories in the hippocampo-neocortical system. The communication of reactivated information from the hippocampus to the neocortex is assumed to be enabled by low levels of acetylcholine, particularly during slow-wave sleep (SWS). Recent studies suggest that the reactivation of memories does not only occur spontaneously but can also be externally triggered by re-presenting learning-associated cues during sleep.

Objectives: Here we investigated whether the beneficial effect of cued memory reactivation during sleep depends on similar mechanisms as spontaneous reactivation, and specifically on low cholinergic tone.

Methods: In two experimental nights, healthy volunteers learned a visuo-spatial memory task in the presence of an odor before going to sleep for 40 min. In one night, subjects were presented with the odor again during SWS, whereas in the other night they received an odorless vehicle. In half of the subjects, the availability of acetylcholine during sleep was increased by administering the acetylcholine-esterase inhibitor physostigmine.

Results: Contrary to our hypothesis, increased cholinergic tone during sleep did not abolish the beneficial effect of odor cueing: memory performance was better after odor cueing compared to odorless vehicle, independent of physostigmine or placebo administration.

Conclusions: This finding challenges the assumption that odor-cued and spontaneous memory reactivation rely on the same neuropharmacological mechanisms.

Keywords: Acetylcholine; Memory consolidation; Odor reactivation; Physostigmine; Sleep.

PubMed Disclaimer

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1

Fig. 1

Experimental design. In the evening, all subjects learned a 2D object-location task under the presence of an odor. Starting at subsequent sleep onset, subjects received either an acetylcholine-esterase inhibitor (physostigmine group) or saline solution (placebo group) intravenously for 40 min. During the first 20 min of SWS, the learning-associated odor was presented again in one night (odor condition) and an odorless vehicle in the other night (vehicle condition). After a sleep period of ~ 40 min, subjects were woken up and watched a movie to allow for the effects of the drug to fade out. Subjects then learned an interference memory task and were finally tested on their recall of the original memory task

Fig. 2

Fig. 2

Memory performance after odor cueing under physostigmine. Odor cueing during SWS improved memory performance as compared to vehicle, independent of physostigmine administration (“odor/vehicle” main effect: p = 0.026). Top bars show the means ± s.e.m. of memory performance at final recall relative to the learning performance (with learning set to 100%) in the odor and vehicle conditions of the physostigmine and placebo groups, respectively. Small bottom bars show each participant’s performance difference between the odor and vehicle conditions, with positive values corresponding to better performance in the odor condition and negative values corresponding to better performance in the vehicle condition

Similar articles

Cited by

References

    1. Antony JW, Gobel EW, O’Hare JK, et al. Cued memory reactivation during sleep influences skill learning. Nat Neurosci. 2012;15:1114–1116. doi: 10.1038/nn.3152. - DOI - PMC - PubMed
    1. Aquilonius SM, Hartvig P. Clinical pharmacokinetics of cholinesterase inhibitors. Clin Pharmacokinet. 1986;11:236–249. doi: 10.2165/00003088-198611030-00005. - DOI - PubMed
    1. Atherton LA, Dupret D, Mellor JR (2015) Memory trace replay: the shaping of memory consolidation by neuromodulation. Trends Neurosci:1–11. 10.1016/j.tins.2015.07.004 - PMC - PubMed
    1. Bendor D, Wilson MA. Biasing the content of hippocampal replay during sleep. Nat Neurosci. 2012;15:1439–1444. doi: 10.1038/nn.3203. - DOI - PMC - PubMed
    1. Brodt S, Pöhlchen D, Flanagin VL, et al. Rapid and independent memory formation in the parietal cortex. Proc Natl Acad Sci. 2016;113:201605719. doi: 10.1073/pnas.1605719113. - DOI - PMC - PubMed

Publication types

MeSH terms

Substances

LinkOut - more resources