Intentions matter for benefits from sleep

Consolidation of Prospective Memory: Effects of Sleep on Completed and Reinstated Intentions
Barner C, Seibold M, Born J, Diekelmann S.
Front. Psychol., 06 January 2017 

Sleep has been shown to facilitate the consolidation of prospective memory, which is the ability to execute intended actions at the appropriate time in the future. In a previous study, the sleep benefit for prospective memory was mainly expressed as a preservation of prospective memory performance under divided attention as compared to full attention. Based on evidence that intentions are only remembered as long as they have not been executed yet (cf. 'Zeigarnik effect'), here we asked whether the enhancement of prospective memory by sleep vanishes if the intention is completed before sleep and whether completed intentions can be reinstated to benefit from sleep again. In Experiment 1, subjects learned cue-associate word pairs in the evening and were prospectively instructed to detect the cue words and to type in the associates in a lexical decision task (serving as ongoing task) 2 h later before a night of sleep or wakefulness. At a second surprise test 2 days later, sleep and wake subjects did not differ in prospective memory performance. Specifically, both sleep and wake groups detected fewer cue words under divided compared to full attention, indicating that sleep does not facilitate the consolidation of completed intentions. Unexpectedly, in Experiment 2, reinstating the intention, by instructing subjects about the second test after completion of the first test, was not sufficient to restore the sleep benefit. However, in Experiment 3, where subjects were instructed about both test sessions immediately after learning, sleep facilitated prospective memory performance at the second test after 2 days, evidenced by comparable cue word detection under divided attention and full attention in sleep participants, whereas wake participants detected fewer cue words under divided relative to full attention. Together, these findings show that for prospective memory to benefit from sleep, (i) the intention has to be active across the sleep period, and (ii) the intention should be induced in temporal proximity to the initial learning session.

Sleep after learning facilitates memory retention

Sleep Facilitates Memory by Blocking Dopamine Neuron-Mediated Forgetting
Jacob A. Berry, Isaac Cervantes-Sandoval, Molee Chakraborty, Ronald L. Davis
Cell, Volume 161, Issue 7, 18 June 2015, Pages 1656–1667

Early studies from psychology suggest that sleep facilitates memory retention by stopping ongoing retroactive interference caused by mental activity or external sensory stimuli. Neuroscience research with animal models, on the other hand, suggests that sleep facilitates retention by enhancing memory consolidation. Recently, in Drosophila, the ongoing activity of specific dopamine neurons was shown to regulate the forgetting of olfactory memories. Here, we show this ongoing dopaminergic activity is modulated with behavioral state, increasing robustly with locomotor activity and decreasing with rest. Increasing sleep-drive, with either the sleep-promoting agent Gaboxadol or by genetic stimulation of the neural circuit for sleep, decreases ongoing dopaminergic activity, while enhancing memory retention. Conversely, increasing arousal stimulates ongoing dopaminergic activity and accelerates dopaminergic-based forgetting. Therefore, forgetting is regulated by the behavioral state modulation of dopaminergic-based plasticity. Our findings integrate psychological and neuroscience research on sleep and forgetting.

Sleep, cognition and aging

Sleep, Cognition, and Normal Aging: Integrating a Half-Century of Multidisciplinary Research.
Scullin MK, Bliwise DL.
Perspect Psychol Sci. 2015 Jan;10(1):97-137. 

Sleep is implicated in cognitive functioning in young adults. With increasing age there are substantial changes to sleep quantity and quality including changes to slow wave sleep, spindle density, and sleep continuity/fragmentation. A provocative question for the field of cognitive aging is whether such changes in sleep physiology affect cognition (e.g., memory consolidation). We review nearly a half-century of research studies across 7 diverse correlational and experimental literature domains, which historically have had little crosstalk. Broadly speaking, sleep and cognitive functions are often related in advancing age, though the prevalence of null effects (including correlations in the unexpected, negative direction) in healthy older adults indicates that age may be an effect modifier of these associations. We interpret the literature as suggesting that maintaining good sleep quality, at least in young adulthood and middle age, promotes better cognitive functioning and serves to protect against age-related cognitive declines.

Emotionally salient information and memory performance

Prospection and emotional memory: how expectation affects emotional memory formation following sleep and wake.
Tony J. Cunningham, Alexis M. Chambers, and Jessica D. Payne
Front Psychol. 2014 Aug 4;5:862. 

Successful prospective memory is necessarily driven by an expectation that encoded information will be relevant in the future, leading to its preferential placement in memory storage. Like expectation, emotional salience is another type of cue that benefits human memory formation. Although separate lines of research suggest that both emotional information and information explicitly expected to be important in the future benefit memory consolidation, it is unknown how expectation affects the processing of emotional information and whether sleep, which is known to maximize memory consolidation, plays a critical role. The purpose of this study was to investigate how expectation would impact the consolidation of emotionally salient content, and whether this impact would differ across delays of sleep and wake. Participants encoded scenes containing an emotionally charged negative or neutral foreground object placed on a plausible neutral background. After encoding, half of the participants were informed they would later be tested on the scenes (expected condition), while the other half received no information about the test (unexpected condition). At recognition, following a 12-h delay of sleep or wakefulness, the scene components (objects and backgrounds) were presented separately and one at a time, and participants were asked to determine if each component was old or new. Results revealed a greater disparity for memory of negative objects over their paired neutral backgrounds for both the sleep and wake groups when the memory test was expected compared to when it was unexpected, while neutral memory remained unchanged. Analyzing each group separately, the wake group showed a threefold increase in the magnitude of this object/background trade-off for emotional scenes when the memory test was expected compared to when it was unexpected, while those who slept performed similarly across conditions. These results suggest that emotional salience and expectation cues interact to benefit emotional memory consolidation during a delay of wakefulness. The sleeping brain, however, may automatically tag emotionally salient information as important, such that explicit instruction of an upcoming memory test does not further improve memory performance.

Sleep to Remember

Sleep consolidates memories for competing tasks

Sleep Consolidation of Interfering Auditory Memories in Starlings
Brawn TP, Nusbaum HC, Margoliash D.
Psychological Science 2013, published on Feb 22

Memory consolidation has been described as a process to strengthen newly formed memories and to stabilize them against interference from similar learning experiences. Sleep facilitates memory consolidation in humans, improving memory performance and protecting against interference encountered after sleep. The European starling, a songbird, has also manifested sleep-dependent memory consolidation when trained on an auditory-classification task. Here, we examined how memory for two similar classification tasks is consolidated across waking and sleep in starlings. We demonstrated for the first time that the learning of each classification reliably interferes with the retention of the other classification across waking retention but that sleep enhances and stabilizes the memory of both classifications even after performance is impaired by interference. These observations demonstrate that sleep consolidation enhances retention of interfering experiences, facilitating opportunistic daytime learning and the subsequent formation of stable long-term memories

REM sleep necessary for emotional memory consolidation

The role of REM sleep in the processing of emotional memories: Evidence from behavior and event-related potentials
S. Groch, I. Wilhelm, S. Diekelmann, J. Born
Neurobiology of Learning and Memory, Volume 99, January 2013, Pages 1–9

Emotional memories are vividly remembered for the long-term. Rapid eye movement (REM) sleep has been repeatedly proposed to support the superior retention of emotional memories. However, its exact contribution and, specifically, whether its effect is mainly on the consolidation of the contents or the processing of the affective component of emotional memories is not clear. Here, we investigated the effects of sleep rich in slow wave sleep (SWS) or REM sleep on the consolidation of emotional pictures and the accompanying changes in affective tone, using event-related potentials (ERPs) together with subjective ratings of valence and arousal. Sixteen healthy, young men learned 50 negative and 50 neutral pictures before 3-h retention sleep intervals that were filled with either SWS-rich early or REM sleep-rich late nocturnal sleep. In accordance with our hypothesis, recognition was better for emotional pictures than neutral pictures after REM compared to SWS-rich sleep. This emotional enhancement after REM-rich sleep expressed itself in an increased late positive potential of the ERP over the frontal cortex 300–500 ms after stimulus onset for correctly classified old emotional pictures compared with new emotional and neutral pictures. Valence and arousal ratings of emotional pictures were not differentially affected by REM or SWS-rich sleep after learning. Our results corroborate that REM sleep contributes to the consolidation of emotional contents in memory, but suggest that the affective tone is preserved rather than reduced by the processing of emotional memories during REM sleep.

Beneficial effects of sleep for memory consolidation

Offline consolidation of memory varies with time in slow wave sleep and can be accelerated by cuing memory reactivations.
Diekelmann S, Biggel S, Rasch B, Born J.
Neurobiology of Learning and Memory Volume 98, Issue 2, September 2012, Pages 103–111

Memory representations are reactivated during slow-wave sleep (SWS) after learning, and these reactivations cause a beneficial effect of sleep for memory consolidation. Memory reactivations can also be externally triggered during sleep by associated cues which enhance the sleep-dependent memory consolidation process. Here, we compared in humans the influence of sleep periods (i) of 40min and (ii) of 90min without externally triggered reactivations and (iii) of externally triggered reactivations by an associated odor cue during a 40-min sleep period on the consolidation of previously learned hippocampus-dependent visuo-spatial memories. We show that external reactivation by an odor cue during the 40-min sleep period enhanced memory stability to the same extent as 90min of sleep without odor reactivation. In contrast, 40min of sleep without external reactivations were not sufficient to benefit memory. In the 90-min sleep condition, memory enhancements were associated with time spent in SWS and were independent of the presence or absence of REM sleep. These results suggest that the efficacy of hippocampus-dependent memory consolidation depends on the duration of sleep and particularly SWS. External reactivation cues can accelerate the consolidation process even during shorter sleep episodes.

The memory function of sleep

Nature Reviews Neuroscience 11, 114-126 (February 2010) 
Susanne Diekelmann & Jan Born

Sleep has been identified as a state that optimizes the consolidation of newly acquired information in memory, depending on the specific conditions of learning and the timing of sleep. Consolidation during sleep promotes both quantitative and qualitative changes of memory representations. Through specific patterns of neuromodulatory activity and electric field potential oscillations, slow-wave sleep (SWS) and rapid eye movement (REM) sleep support system consolidation and synaptic consolidation, respectively. During SWS, slow oscillations, spindles and ripples - at minimum cholinergic activity - coordinate the re-activation and redistribution of hippocampus-dependent memories to neocortical sites, whereas during REM sleep, local increases in plasticity-related immediate-early gene activity - at high cholinergic and theta activity - might favour the subsequent synaptic consolidation of memories in the cortex.

The Episodic-inhibition hypothesis

Consolidation of Episodic Memories During Sleep: Long-Term Effects of Retrieval Practice
Psychological Science OnlineFirst, published on November 23, 2009 as doi:10.1177/0956797609354074
Mihály Racsmány, Martin A. Conway, and Gyula Demeter

Two experiments investigated the long-term effects of retrieval practice. In the retrieval-practice procedure, selected items from a previously studied list are repeatedly recalled. The typical retrieval-practice effects are considerably enhanced memory for practiced items accompanied by low levels of recall, relative to baseline, for previously studied items that are associated with the practiced items but were not themselves practiced. The two experiments demonstrated that the former effect persisted over 12 hr; the latter effect also persisted over 12 hr, but only if a period of nocturnal sleep occurred during the retention interval. We propose that consolidation processes occurring during sleep, and possibly featuring some form of offline rehearsal, mediate these long-term effects of retrieval practice.

More faithful memories for those experiences

Awake replay of remote experiences in the hippocampus
Nature Neuroscience Volume 12, Number 7, July 2009
Published online at http://www.nature.com/natureneuroscience
Mattias P Karlsson & Loren M Frank

Hippocampal replay is thought to be essential for the consolidation of event memories in hippocampal-neocortical networks. Replay is present during both sleep and waking behavior, but although sleep replay involves the reactivation of stored representations in the absence of specific sensory inputs, awake replay is thought to depend on sensory input from the current environment. Here, we show that stored representations are reactivated during both waking and sleep replay. We found frequent awake replay of sequences of rat hippocampal place cells from a previous experience. This spatially remote replay was as common as local replay of the current environment and was more robust when the rat had recently been in motion than during extended periods of quiescence. Our results indicate that the hippocampus consistently replays past experiences during brief pauses in waking behavior, suggesting a role for waking replay in memory consolidation and retrieval.

Whats and Whens of sleep-dependent memory consolidation

The whats and whens of sleep-dependent memory consolidation
Susanne Diekelmann, Ines Wilhelm, Jan Born
Sleep Medicine Reviews (2009), doi:10.1016

Sleep benefits memory consolidation. The reviewed studies indicate that this consolidating effect is not revealed under all circumstances but is linked to specific psychological conditions. Specifically, we discuss to what extent memory consolidation during sleep depends on the type of learning materials, type of learning and retrieval test, different features of sleep and the subject population. Post-learning sleep enhances consolidation of declarative, procedural and emotional memories. The enhancement is greater for weakly than strongly encoded associations and more consistent for explicitly than implicitly encoded memories. Memories associated with expected reward gain preferentially access to sleep-dependent consolidation. For declarative memories, sleep benefits are more consistently revealed with recall than recognition procedures at retrieval testing. Slow wave sleep (SWS) particularly enhances declarative memories whereas rapid eye movement (REM) sleep preferentially supports procedural and emotional memory aspects. Declarative memory profits already from rather short sleep periods (1–2 h). Procedural memory profits seem more dose-dependent on the amount of sleep following the day after learning. Children’s sleep with high amounts of SWS distinctly enhances declarative memories whereas elderly and psychiatric patients with disturbed sleep show impaired sleep-associated consolidation often of declarative memories. Based on the constellation of psychological conditions identified we hypothesize that access to sleep-dependent consolidation requires memories to be encoded under control of prefrontal-hippocampal circuitry, with the same circuitry controlling subsequent consolidation during sleep.

Replay during sleep

Replay of rule-learning related neural patterns in the prefrontal cortex during sleep
Adrien Peyrache, Mehdi Khamassi, Karim Benchenane, Sidney I Wiener & Francesco P Battaglia
Nature Neuroscience, doi:10.1038/nn.2337

Slow-wave sleep (SWS) is important for memory consolidation. During sleep, neural patterns reflecting previously acquired information are replayed. One possible reason for this is that such replay exchanges information between hippocampus and neocortex, supporting consolidation. We recorded neuron ensembles in the rat medial prefrontal cortex (mPFC) to study memory trace reactivation during SWS following learning and execution of cross-modal strategy shifts. In general, reactivation of learning-related patterns occurred in distinct, highly synchronized transient bouts, mostly simultaneous with hippocampal sharp wave/ripple complexes (SPWRs), when hippocampal ensemble reactivation and cortico-hippocampal interaction is enhanced. During sleep following learning of a new rule, mPFC neural patterns that appeared during response selection replayed prominently, coincident with hippocampal SPWRs. This was learning dependent, as the patterns appeared only after rule acquisition. Therefore, learning, or the resulting reliable reward, influenced which patterns were most strongly encoded and successively reactivated in the hippocampal/prefrontal network.