Cued memory reactivation during sleep influences skill learning

Antony, James W.; Gobel, Eric W.; O’Hare, Justin K.; Reber, Paul J.; Paller, Ken A.

doi:10.1038/nn.3152

Cited by 296 publications

(264 citation statements)

References 24 publications

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“…This manipulation impaired trace eyeblink conditioning, a hippocampus-dependent learning task (Nokia et al 2012). Other studies in humans have shown that reactivation during SWS can enhance not only spatial memory but also procedural memories, suggesting that reintroduction of cues during sleep may reactivate other brain regions as well (Antony et al 2012;Oudiette et al 2013). These findings validate the hypothesis that NREM SWS is important for learning and memory (Girardeau et al 2009;Ego-Stengel and Wilson 2010).…”

Section: Sleep Enhances Memory Consolidationsupporting

confidence: 66%

The impact of sleep loss on hippocampal function

2013

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Hippocampal cellular and molecular processes critical for memory consolidation are affected by the amount and quality of sleep attained. Questions remain with regard to how sleep enhances memory, what parameters of sleep after learning are optimal for memory consolidation, and what underlying hippocampal molecular players are targeted by sleep deprivation to impair memory consolidation and plasticity. In this review, we address these topics with a focus on the detrimental effects of post-learning sleep deprivation on memory consolidation. Obtaining adequate sleep is challenging in a society that values "work around the clock." Therefore, the development of interventions to combat the negative cognitive effects of sleep deprivation is key. However, there are a limited number of therapeutics that are able to enhance cognition in the face of insufficient sleep. The identification of molecular pathways implicated in the deleterious effects of sleep deprivation on memory could potentially yield new targets for the development of more effective drugs.

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Section: Sleep Enhances Memory Consolidationsupporting

confidence: 66%

The impact of sleep loss on hippocampal function

2013

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“…This decision reflected a tradeoff between the increased prevalence of slow waves in SWS versus the reduced overall time of SWS that occupied in this experiment: only ϳ17% of sleep time compared with ϳ50% of sleep time in stage 2 (Table 1). Moreover, although SWS clearly plays a role in memory consolidation and reactivation (Plihal and Born, 1999;Mölle et al, 2004;Peigneux et al, 2004;Rasch et al, 2007;Aeschbach et al, 2008;Antony et al, 2012;Mascetti et al, 2013), such a role is also documented for stage 2 sleep (Gais et al, 2002;Schabus et al, 2004;Clemens et al, 2007;Nishida and Walker, 2007;Andrade et al, 2011;Arzi et al, 2012;Mednick et al, 2013;Tamminen et al, 2013 (Mednick et al, 2013). Given that the primary goal of this study was to ask whether sleep conditioning induces behavioral modifications that persist over time, and considering the increased number of events we could expect in stage 2 versus SWS, we concluded that stage 2 conditioning is a safer path for us to test.…”

Section: Discussionmentioning

confidence: 99%

Olfactory Aversive Conditioning during Sleep Reduces Cigarette-Smoking Behavior

et al. 2014

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Recent findings suggest that novel associations can be learned during sleep. However, whether associative learning during sleep can alter later waking behavior and whether such behavioral changes last for minutes, hours, or days remain unknown. We tested the hypothesis that olfactory aversive conditioning during sleep will alter cigarette-smoking behavior during ensuing wakefulness. A total of 66 human subjects wishing to quit smoking participated in the study (23 females; mean age, 28.7 Ϯ 5.2 years). Subjects completed a daily smoking diary detailing the number of cigarettes smoked during 7 d before and following a 1 d or night protocol of conditioning between cigarette odor and profoundly unpleasant odors. We observed significant reductions in the number of cigarettes smoked following olfactory aversive conditioning during stage 2 and rapid eye movement (REM) sleep but not following aversive conditioning during wakefulness (p Ͻ 0.05). Moreover, the reduction in smoking following aversive conditioning during stage 2 (34.4 Ϯ 30.1%) was greater and longer lasting compared with the reduction following aversive conditioning during REM (11.9 Ϯ 19.2%, p Ͻ 0.05). Finally, the reduction in smoking following aversive conditioning during sleep was significantly greater than in two separate control sleep experiments that tested aversive odors alone and the effects of cigarette odors and aversive odors without pairing. To conclude, a single night of olfactory aversive conditioning during sleep significantly reduced cigarette-smoking behavior in a sleep stage-dependent manner, and this effect persisted for several days.

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“…Indeed, experimentally inducing memory reactivation by reexposure to a contextual olfactory memory cue during SWS activated hippocampal areas during sleep and resulted in improved memory recall the next day Rasch et al, 2007). This concept has received further support by recent findings indicating that reactivating memories during sleep by auditory cueing leads to a strengthening of individual memory traces, suggesting a high degree of specificity of the effects of reactivation on memory consolidation during sleep (Oudiette, Antony, Creery, & Paller, 2013;Antony, Gobel, OʼHare, Reber, & Paller, 2012;Rudoy, Voss, Westerberg, & Paller, 2009). Although a first study on creativity suggests that odor effects on reactivation are absent when different odors are used before and during sleep (Ritter, Strick, Bos, van Baaren, & Dijksterhuis, 2012), the specificity of olfactory cueing for memory consolidation processes during sleep has not yet been examined in previous studies.…”

Section: Introductionmentioning

confidence: 90%

Reactivating Memories during Sleep by Odors: Odor Specificity and Associated Changes in Sleep Oscillations

Rihm

Diekelmann

Born

et al. 2014

Journal of Cognitive Neuroscience

100

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Memories are reactivated during sleep. Reexposure to olfactory cues during sleep triggers this reactivation and improves later recall performance. Here, we tested if the effects of odor-induced memory reactivations are odor specific, that is, requiring the same odor during learning and subsequent sleep. We also tested whether odor-induced memory reactivation affects oscillatory EEG activity during sleep, as a putative mechanism underlying memory processing during sleep. Participants learned a visuospatial memory task under the presence of an odor. During subsequent SWS, the same odor, a different odor, or an odorless vehicle was presented. We found that odor reexposure during sleep significantly improves memory only when the same odor was presented again, whereas exposure to a new odor or the odorless vehicle had no effect. The memory-enhancing effect of the congruent odor was accompanied by significant increases in frontal delta (1.5-4.5 Hz) and parietal fast spindle (13.0-15.0 Hz) power as well as by an increased negative-to-positive slope of the frontal slow oscillation. Our results indicate that odor-induced memory reactivations are odor specific and trigger changes in slow-wave and spindle power possibly reflecting a bottom-up influence of hippocampal memory replay on cortical slow oscillations as well as thalamo-cortical sleep spindles. Abstract ■ Memories are reactivated during sleep. Reexposure to olfactory cues during sleep triggers this reactivation and improves later recall performance. Here, we tested if the effects of odor-induced memory reactivations are odor specific, that is, requiring the same odor during learning and subsequent sleep. We also tested whether odor-induced memory reactivation affects oscillatory EEG activity during sleep, as a putative mechanism underlying memory processing during sleep. Participants learned a visuospatial memory task under the presence of an odor. During subsequent SWS, the same odor, a different odor, or an odorless vehicle was presented. We found that odor reexposure during sleep significantly improves memory only when the same odor was presented again, whereas exposure to a new odor or the odorless vehicle had no effect. The memory-enhancing effect of the congruent odor was accompanied by significant increases in frontal delta (1.5-4.5 Hz) and parietal fast spindle (13.0-15.0 Hz) power as well as by an increased negative-to-positive slope of the frontal slow oscillation. Our results indicate that odor-induced memory reactivations are odor specific and trigger changes in slow-wave and spindle power possibly reflecting a bottom-up influence of hippocampal memory replay on cortical slow oscillations as well as thalamo-cortical sleep spindles. ■

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Cued memory reactivation during sleep influences skill learning

Cited by 296 publications

References 24 publications

The impact of sleep loss on hippocampal function

The impact of sleep loss on hippocampal function

Olfactory Aversive Conditioning during Sleep Reduces Cigarette-Smoking Behavior

Reactivating Memories during Sleep by Odors: Odor Specificity and Associated Changes in Sleep Oscillations

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