Slow wave sleep during a daytime nap is necessary for protection from subsequent interference and long-term retention

Alger, Sara E.; Lau, Hiuyan; Fishbein, William

doi:10.1016/j.nlm.2012.06.003

Cited by 77 publications

(72 citation statements)

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“…3). This correlation of memory improvement with SWS echoes prior observations of the importance of this sleep stage to other forms of hippocampus-dependent memory consolidation (Plihal and Born 1997;Lau et al 2011;Alger et al 2012), which here appears to have been enhanced by feedback.…”

supporting

confidence: 86%

“…The human brain is constantly bombarded with a barrage of stimuli, and must decipher which newly encoded information is important enough to consolidate into long-term memory. It is now clear that memory consolidation is facilitated by sleep (Plihal and Born 1997;Stickgold et al 2000;Mednick et al 2002;Walker et al 2002;Tucker et al 2006;Drosopoulos et al 2007;Ellenbogen et al 2007;Alger et al 2012). However, sleep may not benefit all memories equally-emerging evidence suggests that sleepdependent memory consolidation is influenced by a variety of factors including emotion (Payne et al 2008), expected future utility (Wilhelm et al 2011a), and reward (Fischer and Born 2009;Oudiette et al 2013).…”

mentioning

confidence: 99%

“…As for other forms of hippocampal-dependent learning (Plihal and Born 1997;Lau et al 2011;Alger et al 2012), human spatial learning may be facilitated by slow wave sleep (SWS) and/or slow wave activity (SWA) (Peigneux et al 2004;Wamsley et al 2010b). Because models of the brain basis of memory consolidation draw heavily on studies of spatial navigation in rodents, studying this memory system in humans provides an important analog to the rodent sleep and memory literature.…”

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confidence: 99%

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Negative reinforcement impairs overnight memory consolidation

et al. 2014

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Post-learning sleep is beneficial for human memory. However, it may be that not all memories benefit equally from sleep. Here, we manipulated a spatial learning task using monetary reward and performance feedback, asking whether enhancing the salience of the task would augment overnight memory consolidation and alter its incorporation into dreaming. Contrary to our hypothesis, we found that the addition of reward impaired overnight consolidation of spatial memory. Our findings seemingly contradict prior reports that enhancing the reward value of learned information augments sleep-dependent memory processing. Given that the reward followed a negative reinforcement paradigm, consolidation may have been impaired via a stress-related mechanism.

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confidence: 86%

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confidence: 99%

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confidence: 99%

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Negative reinforcement impairs overnight memory consolidation

et al. 2014

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“…During slow wave sleep, thought to benefit hippocampal dependent declarative memory, reactivation of the face-object pairs may promote the beginning of the process of consolidation from short-term dependence on the hippocampus to eventual longterm neocortical storage (Buzsáki, 1989;Peigneux et al, 2004;Wilson & McNaughton, 1994). Although we did not find an explicit significant relationship between performance and SWS in this study, we cannot rule out that SWS is playing a role in the preservation of memory for the paired associates, as several studies find a general benefit of sleep for this type of memory using designs that indicate a role for NREM sleep (e.g., split night design with SWS-rich sleep, Plihal & Born, 1997;NREM only nap, Tucker et al, 2006; naps with and without SWS, Alger, Lau, & Fishbein, 2012). With regard to relational memory, Lau et al (2010), using a task similar to the current one, found a relationship between SWS and face-face memory formation.…”

Section: Discussionmentioning

confidence: 57%

The differential effects of emotional salience on direct associative and relational memory during a nap

Alger

Payne

2016

Cogn Affect Behav Neurosci

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Relational memories are formed from shared components between directly learned memory associations, flexibly linking learned information to better inform future judgments. Sleep has been found to facilitate both direct associative and relational memories. However, the impact of incorporating emotionally salient information into learned material and the interaction of emotional salience and sleep in facilitating both types of memory is unknown. Participants encoded two sets of picture pairs, with either emotionally negative or neutral objects paired with neutral faces. The same objects were present in both sets, paired with two different faces across the sets. Baseline memory for these directly paired associates was tested immediately after encoding, followed by either a 90-min nap opportunity or wakefulness. Five hours after learning, a surprise test assessed relational memory, the indirect association between two faces paired with the same object during encoding, followed by a retest of direct associative memory. Overall, negative information was remembered better than neutral for directly learned pairs. A nap facilitated both preservation of direct associative memories and formation of relational memories, compared to remaining awake. Interestingly, however, this sleep benefit was observed specifically for neutral directly paired associates, while both neutral and negative relational associations benefitted from a nap. Finally, REM sleep played opposing roles in neutral direct and relational associative memory formation, with more REM sleep leading to forgetting of direct associations but promoting relational associations, suggesting that, while not benefitting memory consolidation for directly learned details, REM sleep may foster the memory reorganization needed for relational memory.Keywords Emotion . Associative memory . Naps . Sleep . Inference . Relational memory In our encounters with the everyday stream of information, we do not encode and store all individual experiences in a veridical fashion. Rather, new information is integrated with old, and overlapping details are consolidated into schemata, or networks linked by common features of related memories, to flexibly form novel relationships (Eichenbaum, 2004;Eichenbaum & Cohen, 2001). We use these new representations derived from related memories to adaptively make inferential judgments about future experiences. However, our everyday experiences are not devoid of emotion. Emotional salience, defined by the valence (negative to positive) and arousal (calming to arousing) of an experience, is a biologically adaptive cue that can influence how an event is remembered and possibly how it is integrated in memory. In addition to the influence of emotion, sleep during the consolidation and integration period of a new memory may impact its fate. This experiment investigates the separate and interacting contributions of emotional salience and sleep to the consolidation of direct associative and relational memories, the indirect associations between two...

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“…Furthermore, whereas most studies have entailed the learning of a single novel task, real-world learning often involves the acquisition of a variety of skills or information that may interfere with other learning acquired throughout the day. A number of recent studies have explored the interaction between interference and sleep consolidation (e.g., Walker et al 2003;Ellenbogen et al 2006Ellenbogen et al , 2009Korman et al 2007;Drosopoulos et al 2007;Diekelmann et al 2011;Alger et al 2012;Sheth et al 2012). Remarkably, the memory benefit of sleep is often greater in conditions with interference compared to conditions that only learn a single task.…”

Section: A Behavioral Approach To Sleep-dependent Memory Consolidationmentioning

confidence: 99%

A Bird’s Eye View of Sleep-Dependent Memory Consolidation

Brawn

Margoliash

2014

Sleep, Neuronal Plasticity and Brain Function

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How new experiences are solidified into long-lasting memories is a central question in the study of brain and behavior. One of the most intriguing discoveries in memory research is that brain activity during sleep helps to transform newly learned information and skills into robust memories. Though the first experimental work linking sleep and memory was conducted 90 years ago by Jenkins and Dallenbach, the case for sleep-dependent memory consolidation has only garnered strong support in the last decade. Recent studies in humans provide extensive behavioral, imaging, and polysomnographic data supporting sleep consolidation of a broad range of memory tasks. Likewise, studies in a few animal model systems have elucidated potential mechanisms contributing to sleep consolidation such as neural reactivation and synaptic homeostasis. Here, we present an overview of sleep-dependent memory consolidation, focusing on how investigations of sleep and learning in birds have complemented the progress made in mammalian systems by emphasizing a strong connection between behavior and physiology. We begin by describing the behavioral approach that has been utilized to demonstrate sleep consolidation in humans. We then address neural reactivation in the rodent hippocampal system as a putative mechanism of sleep consolidation. Next, we discuss the role of sleep in the learning and maintenance of song in zebra finches. We note that while both the rodent and zebra finch systems provide evidence for sleep-dependent memory changes in physiology and behavior, neither duplicates the pattern of changes most commonly observed in humans. Finally, we present a recently developed model of sleep consolidation involving auditory classification learning in European starlings , which has the potential to connect behavioral evidence of sleep consolidation as developed in humans with underlying neural mechanisms observable in animals.

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Slow wave sleep during a daytime nap is necessary for protection from subsequent interference and long-term retention

Cited by 77 publications

References 71 publications

Negative reinforcement impairs overnight memory consolidation

Negative reinforcement impairs overnight memory consolidation

The differential effects of emotional salience on direct associative and relational memory during a nap

A Bird’s Eye View of Sleep-Dependent Memory Consolidation

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