Memory, sleep, and dreaming: experiencing consolidation

“Compatible with this observation is the proposal that sleep functions to transformmemory traces in part by slowly interleaving neural representations of recent experience into existing remote and semantic cortical networks.(38,69) For example, in their influential article in Psychological Review, McCelland and colleag…”

“Second, a prominent feature of memory reactivation in rodent models is that, within NREM sleep, the strength of neural-level memory replay decays quickly across time.(26,27) Similarly, it seems that sleep mentation may be most strongly related to recent memories early in the sleep phase,(24,28,29) with this associatio…”

“While research on the “default” mode of brain function has brought attention to the importance of spontaneous brain activity occurring during periods of rest and sleep [70,71], surprisingly, virtually none of this work has examined participants' own reports of what is going through their mind at rest.”

“In recent years, an accumulating body of research evidence has definitively demonstrated that post-learning sleep is beneficial for human memory performance across a variety of tasks, including verbal learning [1–4], procedural skill learning [2,5–7], emotional memory [8,9], and spatial navigation [10,11].”

“Neuronal firing sequences established during wake are reexpressed only intermittently during rodent NREM sleep, with low fidelity and on a faster timescale than the original experience.(30,31) Similarly, only intermittent fragments of recent episodicmemories appear in sleep mentation, intermingled with remote and sema…”

“In contrast, only a single study has reported similar reactivation of memory during REM sleep.(39) Our recent work examining the effects of learning tasks on sleep mentation have thus focused on periods of stage 1 and 2 NREM sleep immediately after sleep onset.”

“Yet despite widespread theoretical agreement that sleep-dependent memory processing may relate to dream experience [30,36–40,72], attempts to empirically address this hypothesis have been conspicuously absent.”

“In recent years, an accumulating body of research evidence has definitively demonstrated that post-learning sleep is beneficial for human memory performance across a variety of tasks, including verbal learning [1–4], procedural skill learning [2,5–7], emotional memory [8,9], and spatial navigation [10,11].”

“To the contrary, recent studies have shown that sleep is important for such complex processes as the integration of new information into established cortical memory networks,(15,16) the extraction of meaning,(17) and the development of insight.(18) Recent studies by Dumay and Gaskell(16) and Tamminen and colleagues(15…”

“While research on the “default” mode of brain function has brought attention to the importance of spontaneous brain activity occurring during periods of rest and sleep [70,71], surprisingly, virtually none of this work has examined participants' own reports of what is going through their mind at rest.”

“Neuronal firing sequences established during wake are reexpressed only intermittently during rodent NREM sleep, with low fidelity and on a faster timescale than the original experience.(30,31) Similarly, only intermittent fragments of recent episodicmemories appear in sleep mentation, intermingled with remote and sema…”

“This reactivation has most consistently been observed during periods of NREM just after learning, within brief hippocampal “sharp-wave ripple” burst events (SPW-Rs1 [12,13]) (Figure 1A).”

“These low levels of acetylcholine during NREM sleep have been hypothesized to facilitate the offline consolidation of hippocampus-dependent memory [34], during a time at which recent episodic memories are most likely to be appearing in concomitant dream experience [24,29].”

“In collaboration with Robert Van de Castle, Calvin Hall pioneered the use of content analysis methods to quantitatively assess the content of large sets of mentation reports [52].”

“In direct support of this hypothesis, a recent study has shown that the extent of neural pattern reactivation after learning predicts subsequent gains in memory performance.(14) Human”

“In recent years, an accumulating body of research evidence has definitively shown that postlearning sleep is beneficial for human memory performance across a variety of tasks, including verbal learning, procedural skill learning, emotional memory,(8,9) and spatial navigation.(10,11) Memories of recent experience appea…”

“Furthermore, when animals are exposed to 2 successive spatial experiences, reactivation of both patterns seems to be instantiated simultaneously during subsequent NREM sleep.(26) Compatible with this observation is the proposal that sleep functions to transformmemory traces in part by slowly interleaving neural repres…”

“In recent years, an accumulating body of research evidence has definitively demonstrated that post-learning sleep is beneficial for human memory performance across a variety of tasks, including verbal learning [1–4], procedural skill learning [2,5–7], emotional memory [8,9], and spatial navigation [10,11].”

“This reactivation has most consistently been observed during periods of NREM just after learning, within brief hippocampal “sharp-wave ripple” burst events (SPW-Rs1 [12,13]) (Figure 1A).”

“This observation that dreams do not veridically replay waking experience has led some to conclude that such mental activity is incompatible with consolidation of memory.(67,68) To the contrary, emerging evidence suggests that the fragmentary form in which waking experience appears in dreams, intermingled with other me…”

“For example, for hippocampus-dependent declarative memories, retrieval-associated activity in the hippocampal complex decreases after sleep, whereas related activation in cortical structures, particularly medial prefrontal areas, increases.(19,20) Such evidence supports models of systems-level declarative memory conso…”

“Yet despite widespread theoretical agreement that sleep-dependent memory processing may relate to dream experience [30,36–40,72], attempts to empirically address this hypothesis have been conspicuously absent.”

“To the contrary, recent studies have demonstrated, that sleep is important for such complex processes as the integration of new information into established cortical memory networks [17,18], the extraction of meaning [16], and the development of insight [15].”

“For example, the following illustrates a sleep onset dream report that clearly incorporates fragments of a waking experience, but without replicating the original context in which these fragments were embedded (data from Ref.32).”

“In recent years, an accumulating body of research evidence has definitively demonstrated that post-learning sleep is beneficial for human memory performance across a variety of tasks, including verbal learning [1–4], procedural skill learning [2,5–7], emotional memory [8,9], and spatial navigation [10,11].”

“In recent years, an accumulating body of research evidence has definitively demonstrated that post-learning sleep is beneficial for human memory performance across a variety of tasks, including verbal learning [1–4], procedural skill learning [2,5–7], emotional memory [8,9], and spatial navigation [10,11].”

“For example, for hippocampus-dependent declarative memories, retrievalassociated activity in the hippocampal complex decreases following sleep, while related activation in cortical structures, particularly medial prefrontal areas, increases [19,20].”

“Sleep preferentially benefited (false) memory for these gist words, suggesting that one function of sleep-dependent memory processing is to extract meaningful generalities from large collections of related memories.(17) These and other recent studies suggest that sleep functions not simply to strengthen memories, but…”

“Work from our own laboratory using engaging video game learning tasks has shown that incidence of direct, unambiguous incorporation of task-related imagery at sleep onset declines linearly as a function of time since the initiation of sleep.(28,29) On a broader timescale, it seems that recent life events are most like…”

“Recent work from our own laboratory has provided direct evidence that incorporation of a learning task into subsequent dream experience predicts enhanced sleep-dependent memory consolidation.(66) In this study, participants were trained on a three-dimensional style virtual maze task (Fig.”

“Other functional magnetic resonance imaging (fMRI) studies have described an analogous sleep-dependent reorganization of emotional memory, such that medial prefrontal structures becomemore engaged at delayed retrieval when participants have been allowed to sleep immediately after encoding, in concert with increased re…”

“This observation that dreams do not veridically replay waking experience has led some to conclude that such mental activity is incompatible with consolidation of memory.(67,68) To the contrary, emerging evidence suggests that the fragmentary form in which waking experience appears in dreams, intermingled with other me…”

“Reduced levels of cortisol during early night, SWSdominated sleep have also been hypothesized to both facilitate hippocampal-cortical interactions underlying memory consolidation(35,36) and to promote brain dynamics supporting NREM-type dream experience.(36) Recent papers in sleep and memory have liberally speculated…”

“Other functional magnetic resonance imaging (fMRI) studies have described an analogous sleep-dependent reorganization of emotional memory, such that medial prefrontal structures becomemore engaged at delayed retrieval when participants have been allowed to sleep immediately after encoding, in concert with increased re…”

“Other research has similarly prompted participants to connect dream reports with likely memory sources from waking experience in the previous days and weeks, showing that such memory sources are readily identified with high confidence, and correspond with the ratings of blind judges.(49) We return later to this notion…”

“Hypothesizing that REM sleep dreaming is important for emotional adaptation to stressful events, the work of Rosalind Cartwright has examined dream content as a predictor of psychological outcomes in women after divorce, finding that characteristics of spouserelated dreams predict remission from depression.(76) Other…”

“Other work also supports a role for sleep in emotional adaptation to negative experiences.(77,78) Recent work from our own laboratory has provided direct evidence that incorporation of a learning task into subsequent dream experience predicts enhanced sleep-dependent memory consolidation.”

“Work from our own laboratory using engaging video game learning tasks has shown that incidence of direct, unambiguous incorporation of task-related imagery at sleep onset declines linearly as a function of time since the initiation of sleep.(28,29) On a broader timescale, it seems that recent life events are most like…”

“Compatible with this observation is the proposal that sleep functions to transformmemory traces in part by slowly interleaving neural representations of recent experience into existing remote and semantic cortical networks.(38,69) For example, in their influential article in Psychological Review, McCelland and colleag…”

“These low levels of acetylcholineduring NREM sleep have been hypothesized to facilitate the offline consolidation of hippocampusdependentmemory,(34) duringa timeatwhich recent episodic memories are most likely to be appearing in concomitant dream experience.(24,29) Reduced levels of cortisol during early night, SWSdom…”

“Late-night NREM dreaming can be just as vivid, bizarre, and storylike as the typical dream from REM sleep.(57,60) Yet one consistent difference between dream reports from different stages of sleep seems to be the nature of participant-identified memory sources.”

“Though only a small handful of studies have examined time-of-night effects on incorporation in this manner, both the recency of subject-identified memory sources [61] and the similarity of Wamsley and Stickgold Page 6”

“Other work also supports a role for sleep in emotional adaptation to negative experiences.(77,78) Recent work from our own laboratory has provided direct evidence that incorporation of a learning task into subsequent dream experience predicts enhanced sleep-dependent memory consolidation.”

“Contrary to the entrenched popular belief that “REM sleep = dreaming”, we dream during all stages of sleep [55–58].”

“In recent years, an accumulating body of research evidence has definitively shown that postlearning sleep is beneficial for human memory performance across a variety of tasks, including verbal learning, procedural skill learning, emotional memory,(8,9) and spatial navigation.(10,11) Memories of recent experience appea…”

“[48] report that 22% of reports unambiguously incorporated either isolated elements of the laboratory situation (i.”

“memory sources (a hippocampus-dependent form of memory) than are reports from REM sleep,(24) whereas dream experiences from REM sleep are unique in the presence of particularly intense emotions.(25) Second, a prominent feature of memory reactivation in rodent models is that, within NREM sleep, the strength of neural-l…”

“Contrary to the entrenched popular belief that “REM sleep = dreaming”, we dream during all stages of sleep [55–58].”

“Yet despite widespread theoretical agreement that sleep-dependent memory processing may relate to dream experience [30,36–40,72], attempts to empirically address this hypothesis have been conspicuously absent.”

“Late-night NREM dreaming can be just as vivid, bizarre, and storylike as the typical dream from REM sleep.(57,60) Yet one consistent difference between dream reports from different stages of sleep seems to be the nature of participant-identified memory sources.”

“On a broader timescale, it seems that recent life events are most likely to appear in dream content, relative to more remote experiences from years past.(63,64) Several studies also suggest that waking experiences tend to be incorporated into dream mentation either immediately after the experience, or else about a wee…”

“sleep mentation reports to presleep thought [62] have been reported to correlate negatively with time since sleep onset.”

“On a broader timescale, it seems that recent life events are most likely to appear in dream content, relative to more remote experiences from years past.(63,64) Several studies also suggest that waking experiences tend to be incorporated into dream mentation either immediately after the experience, or else about a wee…”

“…a source of creativity, insight and problem-solving (Schredl and Erlacher, 2007), an opportunity for emotional adaptation (Cartwright et al., 1998; Lara-Carrasco et al., 2009), and an expression and potential means of memory consolidation (Nielsen and Stenstrom, 2005; Wamsley and Stickgold, 2011).”

“Some authors even speculate that REM replay may be associated with the vivid dreaming that characterises this sleep stage [67,77].”

“Dreaming could reflect the reactivation and consolidation of memories during sleep (Nielsen and Stenstrom, 2005; Wamsley and Stickgold, 2011).”

“On the neurophysiological level, dream mentation has been suggested to represent the phenomenological reflection of a neural replay of activation patterns associated with recent learning experiences (Wamsley, 2014; Wamsley Stickgold, 2011; Wilson McNaughton, 1994).”

“…the strengthening and enhanced recall of those experiences; rather, with many modern memory consolidation theories, it is suggested that emotional memories are incorporated into dreams in order to be integrated or assimilated into the wider memory system (Payne, 2010; Wamsley & Stickgold, 2011).”

“In particular, certain micro features of sleep are expressed locally within specific brain circuits supporting processes regulating systemic and synaptic neuroplasticity (McGaugh, 2000) in order to facilitate memory formation and consolidation (Buzsaki, 1998; Steriade, 2006; Walker, 2009; Diekelmann and Born, 2010; Wa…”

“In line with sleep and memory researchers (e.g., Payne, 2010; Wamsley and Stickgold, 2011), we propose that emotional waking-life memories are preferentially activated during sleep, thus appearing in dreams, in order to assimilate these memories into the wider memory system.”

“For experiment 1, participants kept a daily log for 10 days before having dream reports collected during one night in the sleep laboratory or at home.”

“Following Walker and Stickgold [25], we also predict that delayed incorporation dreams are more likely to occur later in the night than earlier.”

“…in waking life (e.g., Revonsuo, 2000; Nielsen and Levin, 2007; Cartwright, 2010; Perogamvros and Schwartz, 2012), to consolidate specific types of memories (Wamsley and Stickgold, 2011), or whether it simply reflects the individual’s waking life experiences (Domhoff, 1996, 2017; Schredl, 2003).”

“It has been proposed that mental experience in sleep, such as dreaming activity, both reflects and contributes to the off-line consolidation of recent episodic memories (e.g. Cipolli et al. 2004; De Koninck et al. 1990; Fiss et al. 1977; Wamsley & Stickgold 2011).”

“However, the question whether dreaming itself is a functional component of the consolidation of memories is highly debated (Wamsley and Stickgold, 2011; Wamsley, 2014), and this”

“In contrast, emotional memory is preferentially enhanced by REM sleep, and dream experiences from REM have uniquely intense emotions (Smith, Nixon, and Nader 2004; Wamsley and Stickgold 2011).”

“One of the proposed potential functions of dreams is that the dreaming brain extracts the gist of autobiographically salient experiences [33, 34, 85, 86].”

“Such neural processes of insight and memory consolidation during sleep are proposed by Wagner et al. (2004) and Wamsley and Stickgold (2011) to be related to the formal characteristics of dream experiences.”

“…high-density sleep EEG recordings in patients with schizophrenia found a strong reduction in sleep spindle number, amplitude and duration in comparison to healthy controls and patients diagnosed with depression (Ferrarelli et al., 2007, 2010; Wamsley and Stickgold, 2011; Wamsley et al., 2012).”

“We posit that the study of DMN in the field of sleep medicine (particularly in insomnia) will bring new translational research challenges to the field of sleep neuroscience, in particular, concerning to the conceptual link with clinical practice (Wamsley & Stickgold, 2011).”

“…a recent study has r e ported that inhibition of MCH neur ons acti v e during REM-sleep facilitates the retention of hippocampus-dependent memor y, 229 ther efor e pr oposing that REM-acti v e MCH neur ons favor hippocampal forgetting (or disrupt hippocampal consolidation 188 ) during sleep.”

“…provides increasing support for the neurocognitive theory and the contemporary emotional memory consolidation and integration theories (Malinowski & Horton, 2015; Nir & Tononi, 2010; Wamsley & Stickgold, 2011), their predictions regarding dream bizarreness have not yet been properly evaluated.”

“Based on this evidence, we have hypothesized that the consolidation of recently learned information may be reflected in the content of dreaming (56,57).”

“As argued by Wamsley and Stickgold (2011), dreaming may be the experience of memory consolidation (during sleep see also Blagrove, Ruby, & Eichenlaub, 2013; Eichenlaub, Cash, & Blagrove, 2017; for critical discussions).”

“…functional reasons, allows dream content to represent waking life matters about which we are more normally defended or even unaware when awake, because active inhibition of attending to these is suppressed during sleep (Freud, 1953; Wegner et al., 2004; Erdelyi, 2006; Bryant et al., 2011).”

“Dreams may help to process and integrate people’s daily experiences (e.g., De Monchaux 1993; Wamsley and Stickgold 2011), and it is thought that meaningful experiences, particularly those that are threatening (Revonsuo 2000), are at the forefront of dream material (Erikson 1954; Jung 1948/1974).”

“For instance, there is now robust data supporting the role of sleep in memory consolidation and learning of various types (including of motor skills, perceptual skills and declarative memory) (Wamsley and Stickgold, 2011).”

“The resulting ICs from the SogICA group level analysis, which showed high spatial similarity to RSNs [1-42], were further inspected at subject-level.”

“Dreams are widely considered to reflect the activation and recombination of memories of waking experience, where both these memories and associations to them may be altered in the process (Hartman, 2010; Nielsen & Stenstrom, 2005; Stickgold, Hobson, Fosse, & Fosse, 2001; Wamsley & Stickgold, 2011).”

“Otros1 23 (15,6) 18 (31,0) 3 (6,4) 1 (5,9) 1 (4,0)”

“…is consistent with previous findings that identify different fragments of recent waking episodes, but rarely find more elaborate replications of waking events in mentation reports from sleep (Fosse et al., 2003; Wamsley, Perry, Djonlagic, Reaven, & Stickgold, 2010; Wamsley & Stickgold, 2011).”

“There is emerging research regarding a state of ongoing dismemberment and consolidation of complex interrelated memories of all types that selectively strengthen and recombine elements of these traces and effect the network as a whole (Wamsley and Stickgold, 2011).”

“However, this activity replay is constructive, rather than passive, in nature (Cipolli et al., 2017; Graveline and Wamsley, 2015; Wamsley and Stickgold, 2011).”

“Conversely, dreaming affects daytime functioning [5,6] by enhancing memory consolidation [7,8], contributing to problem-solving [9,10] and facilitating emotional processing [11].”

“It has been proposed that dreaming reflects the reactivation and consolidation of memories during sleep (Wamsley, Perry, Djonlagic, Babkes Reaven, & Stickgold, 2010a; Wamsley & Stickgold, 2011; Wamsley, Tucker, Payne, Benavides, & Stickgold, 2010b).”

“One interesting feature of MCH neurons is that they are highly active during REM sleep [15,16] and it therefore seems plausible that this activity contributes to the proposed memory role of REM sleep (reviewed in [17]).”

“In line with sleep and memory research (e.g., Payne and Kensinger, 2010; Wamsley and Stickgold, 2011), Malinowski and Horton (2014) propose that emotional memories are preferentially activated during sleep, thus appearing in dreams, in order to assimilate these memories into the wider memory system.”

“…the brain is sifting memories for consolidation during sleep on the basis of their emotional relevance (van Rijn et al., 2017), and dreaming may reflect or be part of this filtering process (Eichenlaub et al., 2018; Malinowski & Horton, 2014; Wamsley & Stickgold, 2011; Zadra & Stickgold, 2021).”

“…that MCH neurons augment synaptic potentiation and learning, and an entirely different body of literature which suggests that REM sleep is important for memory (reviewed in Wamsley and Stickgold, 2011), it would be sensible to guess that MCH neurons contribute to this night-time consolidation.”

“Contemporary theories often relate dreaming to memory consolidation (e.g., see [3,13,14]) or emotional processing (e.g., see [15–17]).”

“Dream research has suggested that the purposes of dreaming include consolidating memory (Wamsley & Stickgold, 2010, 2011) and emotional regulation (e.g. Cartwright, 2010; Kramer, 1991), and that this takes place apart from any therapeutic intervention.”

“However, few studies have considered the subjective experience of dreaming and its relationship to emotional memory consolidation (Wamsley and Stickgold, 2011).”

“…en développement, notons l’émergence de l’idée selon laquelle le rêve pourrait avoir un rôle dans la consolidation de la mémoire (Stickgold, 2005; Wamsley & Stickgold, 2011), et plus spécifiquement, dans la mémoire émotionnelle (Diekelmann, Wilhelm, & Born, 2009; Wagner, Gais, & Born, 2001),…”

“It has beenproposed thatmental experience in sleep, such as dreaming activity, both reflects and contributes to the off-line consolidation of recent episodic memories (e.g. Cipolli et al. 2004; De Koninck et al. 1990; Fiss et al. 1977; Wamsley & Stickgold 2011).”