Increasing Explicit Sequence Knowledge by Odor Cueing during Sleep in Men but not Women

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.

Use of targeted memory reactivation enhances skill performance during a nap and enhances declarative memory during wake in healthy young adults

“…Application of TMR during sleep, but not wake, has been shown to reactivate and strengthen connectivity among neural networks and regions associated with task performance to improve task-specific performance (Cousins, El-Deredy, Parkes, Hennies, & Lewis, 2016;Diekelmann, Büchel, Born, & Rasch, 2011). This method has been used by others to enhance declarative and motor sequence performance (Antony, Gobel, O'Hare, Reber, & Paller, 2012;Cousins, El-Deredy, Parkes, Hennies, & Lewis, 2014;Creery, Oudiette, Antony, & Paller, 2015;Diekelmann, Born, & Rasch, 2016;Laventure et al, 2016;Oudiette, Antony, Creery, & Paller, 2013;Rasch, Büchel, Gais, & Born, 2007;Schönauer, Geisler, & Gais, 2014), and more recently in our laboratory (Johnson, Scharf, & Westlake, 2018) to improve performance of a real-world sensorimotor skill with less cognitive reliance (i.e., non-dominant arm throwing).…”

Shaping memory consolidation via targeted memory reactivation during sleep

“…Moreover, cueing during SWS was associated with increased activity in the bilateral caudate nuclei and hippocampi at post‐test, suggesting an effect of cueing on hippocampal activity . Another study employed a similar SRTT task with a 12‐element sequence, but this time an odor was presented every five key responses. Participants performed several trials, some of them with random sequences and some with fixed sequences.…”

Impact of sex steroids and reproductive stage on sleep-dependent memory consolidation in women

“…Behavior and brain function are sexually dimorphic across a range of cognitive domains including memory, emotion, visual perception and spatial navigation (Voyer et al 1995, Astur et al 1998, Lewin et al 2001, Canli et al 2002, Cahill 2006, McDevitt et al 2014, Diekelmann et al 2016, Voyer et al 2016. Generally, women outperform men in verbal memory tasks including word recall and recognition, name recognition, as well as memory for emotional stimuli, while men outperform women in visual-spatial tasks and with certain mathematical abilities (Voyer et al 1995, Lewin et al 2001, Voyer et al 2016.…”