Sleep Facilitates Memory by Blocking Dopamine Neuron-Mediated Forgetting

Berry, Jacob A.; Cervantes-Sandoval, Isaac; Chakraborty, Molee; Davis, Ronald L.

doi:10.1016/j.cell.2015.05.027

Cited by 219 publications

(256 citation statements)

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“…If selective memory reactivation were the only important factor, then one would expect more pronounced evidence for retention of "remember" items over "forget" items. Recent models suggest that a combination of reduced interference and increased memory reactivation (and perhaps other factors) underlie the benefit of sleep on memory, 7,8 and we interpret the current results as consistent with this framework.…”

Section: Discussionsupporting

confidence: 75%

“…1 Enhanced post-sleep retention-hereafter, memory consolidation-is thought to be due to memory reactivation during slow-wave sleep 2 (or rapid eye movement [REM] sleep 3 ), the opportunity to stabilize memories from interference, [4][5][6] or possibly a combination of these processes. 7,8 Though there is a large literature on the relationship between sleep and memory in healthy young adults, it remains unclear whether sleep-dependent memory consolidation is preserved in older adults, whom are known to show fragmented sleep as well as less slow-wave sleep and REM sleep. [8][9][10][11] Several limitations of existing studies on sleep, memory, and aging are worth consideration.…”

Section: Introductionmentioning

confidence: 99%

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The Effects of an Afternoon Nap on Episodic Memory in Young and Older Adults

Scullin

Fairley

Decker

et al. 2017

Sleep

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Study Objectives: In young adults, napping is hypothesized to benefit episodic memory retention (eg, via consolidation). Whether this relationship is present in older adults has not been adequately tested but is an important question because older adults display marked changes in sleep and memory. Design: Between-subjects design. Setting: Sleep laboratory at Emory University School of Medicine. Participants: Fifty healthy young adults (18-29) and 45 community-dwelling older adults (58-83). Intervention: Participants were randomly assigned to a 90-minute nap opportunity or an equal interval of quiet wakefulness. Measurements and Results: Participants underwent an item-wise directed forgetting learning procedure in which they studied words that were individually followed by the instruction to "remember" or "forget." Following a 90-minute retention interval filled with quiet wakefulness or a nap opportunity, they were asked to free recall and recognize those words. Young adults retained significantly more words following a nap interval than a quiet wakefulness interval on both free recall and recognition tests. There was modest evidence for greater nap-related retention of "remember" items relative to "forget" items for free recall but not recognition. Older adults' memory retention did not differ across nap and quiet wakefulness conditions, although they demonstrated greater fragmentation, lower N3, and lower rapid eye movement duration than the young adults. Conclusions: In young adults, an afternoon nap benefits episodic memory retention, but such benefits decrease with advancing age.

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Section: Discussionsupporting

confidence: 75%

Section: Introductionmentioning

confidence: 99%

The Effects of an Afternoon Nap on Episodic Memory in Young and Older Adults

Scullin

Fairley

Decker

et al. 2017

Sleep

View full text Add to dashboard Cite

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“…Dopamine receptor activation in the MBs can also reduce the effects of sleep loss on learning (Seugnet et al 2008). On the other hand, a subset of MB-projecting DA neurons is specifically active during spontaneous and induced wake and this activity can stimulate forgetting, providing a circuit basis for sleep-dependent memory (Berry et al 2015). Wakepromoting effects of dopaminergic neurons are mediated by activation of glutamatergic wake-promoting MB output neurons (Sitaraman et al 2015b).…”

Section: Acetylcholinementioning

confidence: 99%

Molecular Mechanisms of Sleep Homeostasis in Flies and Mammals

Allada¹,

Cirelli

Sehgal

2017

Cold Spring Harb Perspect Biol

137

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“…Recent studies, including work in relatively simple invertebrate models, have started to reveal basic biological mechanisms underlying forgetting (5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15). In Drosophila, single-session Pavlovian conditioning by pairing an odor (conditioned stimulus, CS) with electric shock (unconditioned stimulus, US) induces aversive memories that are short-lasting (16).…”

mentioning

confidence: 99%

Dissecting neural pathways for forgetting in Drosophila olfactory aversive memory

Shuai

Hirokawa

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Recent studies have identified molecular pathways driving forgetting and supported the notion that forgetting is a biologically active process. The circuit mechanisms of forgetting, however, remain largely unknown. Here we report two sets of Drosophila neurons that account for the rapid forgetting of early olfactory aversive memory. We show that inactivating these neurons inhibits memory decay without altering learning, whereas activating them promotes forgetting. These neurons, including a cluster of dopaminergic neurons (PAM-β′1) and a pair of glutamatergic neurons (MBON-γ4>γ1γ2), terminate in distinct subdomains in the mushroom body and represent parallel neural pathways for regulating forgetting. Interestingly, although activity of these neurons is required for memory decay over time, they are not required for acute forgetting during reversal learning. Our results thus not only establish the presence of multiple neural pathways for forgetting in Drosophila but also suggest the existence of diverse circuit mechanisms of forgetting in different contexts.forgetting | Drosophila melanogaster | associative memory | mushroom body | reversal learning A lthough forgetting commonly has a negative connotation, it is a functional process that shapes memory and cognition (1-4). Recent studies, including work in relatively simple invertebrate models, have started to reveal basic biological mechanisms underlying forgetting (5-15). In Drosophila, single-session Pavlovian conditioning by pairing an odor (conditioned stimulus, CS) with electric shock (unconditioned stimulus, US) induces aversive memories that are short-lasting (16). The memory performance of fruit flies is observed to drop to a negligible level within 24 h, decaying rapidly early after training and slowing down thereafter (17). Memory decay or forgetting requires the activation of the small G protein Rac, a signaling protein involved in actin remodeling, in the mushroom body (MB) intrinsic neurons (6). These so-called Kenyon cells (KCs) are the neurons that integrate CS-US information (18,19) and support aversive memory formation and retrieval (20)(21)(22). In addition to Rac, forgetting also requires the DAMB dopamine receptor (7), which has highly enriched expression in the MB (23). Evidence suggests that the dopamine-mediated forgetting signal is conveyed to the MB by dopamine neurons (DANs) in the protocerebral posterior lateral 1 (PPL1) cluster (7,24). Therefore, forgetting of olfactory aversive memory in Drosophila depends on a particular set of intracellular molecular pathways within KCs, involving Rac, DAMB, and possibly others (25), and also receives modulation from extrinsic neurons. Although important cellular evidence supporting the hypothesis that memory traces are erased under these circumstances is still lacking, these findings lend support to the notion that forgetting is an active, biologically regulated process (17,26).Although existing studies point to the MB circuit as essential for forgetting, several questions remain to be answered. Fir...

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Sleep Facilitates Memory by Blocking Dopamine Neuron-Mediated Forgetting

Cited by 219 publications

References 50 publications

The Effects of an Afternoon Nap on Episodic Memory in Young and Older Adults

The Effects of an Afternoon Nap on Episodic Memory in Young and Older Adults

Molecular Mechanisms of Sleep Homeostasis in Flies and Mammals

Dissecting neural pathways for forgetting in Drosophila olfactory aversive memory

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