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Increasing Explicit Sequence Knowledge by Odor Cueing During Sleep in Men but Not Women

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Increasing Explicit Sequence Knowledge by Odor Cueing During Sleep in Men but Not Women

Susanne Diekelmann et al. Front Behav Neurosci.

Abstract

Sleep consolidates newly acquired memories. Beyond stabilizing memories, sleep is thought to reorganize memory representations such that invariant structures, statistical regularities and even new explicit knowledge are extracted. Whereas increasing evidence suggests that the stabilization of memories during sleep can be facilitated by cueing with learning-associated stimuli, the effect of cueing on memory reorganization is less well understood. Here we asked whether olfactory cueing during sleep enhances the generation of explicit knowledge about an implicitly learned procedural memory task. Subjects were trained on a serial reaction time task (SRTT) containing a hidden 12-element sequence in the presence of an odor. During subsequent sleep, half of the subjects were re-exposed to the odor during periods of slow wave sleep (SWS), while the other half received odorless vehicle. In the next morning, subjects were tested on their explicit knowledge about the underlying sequence in a free recall test and a generation task. Although odor cueing did not significantly affect overall explicit knowledge, differential effects were evident when analyzing male and female subjects separately. Explicit sequence knowledge, both in free recall and the generation task, was enhanced by odor cueing in men, whereas women showed no cueing effect. Procedural skill in the SRTT was not affected by cueing, neither in men nor in women. These findings suggest that olfactory memory reactivation can increase explicit knowledge about implicitly learned information, but only in men. Hormonal differences due to menstrual cycle phase and/or hormonal contraceptives might explain the lacking effect in women.

Keywords: consolidation; reactivation; reorganization; serial reaction time task; slow wave sleep.

Figures

Figure 1
Figure 1
Serial reaction time task (SRTT) and experimental procedures. (A) Participants were instructed to press one of four buttons whenever a visual cue (picture of a fish) appeared in one of four corresponding squares on the screen. Unbeknownst to the participants, the appearance of the cue followed a repeating 12-element sequence. (B) During learning, participants performed on the SRTT in a 1st test block with 15 sequence (S) repetitions flanked by random (R) trials, followed by the training block containing 25 sequence repetitions with concurrent odor presentation, and the 2nd test block with 15 sequence repetitions flanked by random trials and four final sequence repetitions. During the subsequent 8-h sleep period, half of the subjects were again presented with the odor during slow wave sleep (SWS), whereas the other half received an odor-less vehicle. At retrieval testing in the morning, participants performed on a 3rd test block of the SRTT and were then tested on their explicit knowledge about the sequence in a free recall test and a generation task.
Figure 2
Figure 2
Explicit sequence knowledge after odor cueing during sleep. (A) Free recall of the sequence did not differ significantly between the odor and vehicle groups in the whole sample (left panel). Analyzing male and female participants separately showed that odor cueing during SWS increased free recall of the sequence in men but not in women (right panel). Free recall is displayed as the number of correctly recalled sequence elements (range between 0–12). (B) Whereas performance on the generation task was not significantly increased by odor stimulation in the whole sample (left panel), odor reactivation tended to improve the ability to generate the sequence in men but not in women (right panel). Generation task performance refers to percent correct predictions of the next cue position upon presentation of two successive elements of the sequence. Mean ± SEM are shown. *p < 0.05, #p < 0.08.
Figure 3
Figure 3
Performance on the SRTT after odor reactivation during sleep. Odor presentation during SWS did not affect the skill level in the SRTT, neither in the whole sample (A) nor in men and women separately (B). The skill level is presented as the difference between the last random trials and the preceding last sequence trials (in ms) at the end of learning (2nd test block) and at retrieval (3rd test block), respectively. Mean ± SEM are shown.

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