4.8 Review

Sleep-A brain-state serving systems memory consolidation

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Cortical-hippocampal coupling during manifold exploration in motor cortex

Jaekyung Kim et al.

Summary: This study investigates the dynamics of cross-area coupling between the hippocampus, prefrontal cortex, and primary motor cortex during sleep. The results reveal two distinct stages of processing, characterized by different patterns of interaction between these brain areas. The first stage is associated with rapid learning and variability of motor cortex activity, while the second stage is characterized by increased coupling between the prefrontal cortex and motor cortex and decreased coupling between the hippocampus and motor cortex. Additionally, manipulation of task parameters can re-engage the interaction between the hippocampus and motor cortex.

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Mental navigation and the neural mechanisms of insight

Jaan Aru et al.

Summary: This article presents a central hypothesis that suggests insights may occur during mental navigation and create rapid cellular plasticity. It emphasizes the differences between neocortical and hippocampal mechanisms in providing insight. The suddenness of insight is argued to be related to the sudden emergence of place fields in the hippocampus. The hypothesis connects research on creativity, mental navigation, and specific synaptic plasticity mechanisms in the hippocampus.

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Sleep Electroencephalogram (EEG) Oscillations and Associated Memory Processing During Childhood and Early Adolescence

Eva-Maria Kurz et al.

Summary: The architecture of sleep undergoes distinct changes during childhood and early adolescence. Slow wave sleep is involved in memory processing and may support the formation of abstracted gist memories. The coupling of slow oscillations and fast sleep spindles becomes increasingly important for memory formation in children and adolescents, while wake-associated mechanisms are also effective in forming medium-term memory in this age group.

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Fear memory in humans is consolidated over time independently of sleep

Yuri G. Pavlov et al.

Summary: This study found that fear memories can be consolidated over time after acquisition, and this effect is independent of sleep.

COGNITIVE AFFECTIVE & BEHAVIORAL NEUROSCIENCE (2023)

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Accelerating Maturation of Spatial Memory Systems by Experience: Evidence from Sleep Oscillation Signatures of Memory Processing

Maria P. Contreras et al.

Summary: Research shows that discrete spatial experience can accelerate the maturation of spatial memory systems in the brain. This maturation is driven by specific sleep oscillations, which contribute to the formation of long-term memory and knowledge. The findings suggest that experience plays a positive role in the development of memory systems.

JOURNAL OF NEUROSCIENCE (2023)

Article Biochemistry & Molecular Biology

Ripple band phase precession of place cell firing during replay

Daniel Bush et al.

Summary: This study reveals the use of phase coding during neuronal replay, similar to the theta phase precession observed during navigation. Each replay event involves the forward propagation of decoded locations along the recapitulated trajectory.

CURRENT BIOLOGY (2022)

Review Cell Biology

The why and how of sleep-dependent synaptic down-selection

Chiara Cirelli et al.

Summary: Sleep is necessary for renormalizing synaptic weights after learning, which is a smart process of synaptic down-selection, explaining the beneficial effects of sleep on cognition. While some molecular mechanisms have been identified, others are still being investigated to understand how most synapses are weakened during sleep while some are protected.

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Sleep spindles track cortical learning patterns for memory consolidation

Marit Petzka et al.

Summary: This study explores the role of sleep spindles in memory consolidation by using high-density scalp electroencephalography (EEG) and polysomnography (PSG). The results show that sleep spindles are most pronounced over learning-related cortical areas and the extent to which spindles track learning patterns predicts memory consolidation.

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Learned Motor Patterns Are Replayed in Human Motor Cortex during Sleep

Daniel B. Rubin et al.

Summary: Replay of motor cortex neural activity may occur during sleep following motor learning in humans.

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Article Behavioral Sciences

The role of sleep for episodic memory consolidation: Stabilizing or rescuing?

Jing Zhang et al.

Summary: Sleep plays an important role in memory consolidation and protection, but recent studies have failed to demonstrate sleep's superiority in preventing memory interference. This study compared the performance of a sleep group and a wake group in memory tests at different time points and found that the sleep group performed better after 12 hours, but the two groups performed similarly after 24 hours. Additionally, the wake group showed a positive correlation between memory improvement and theta and delta band power during slow wave sleep, which was not found in the sleep group.

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Paradoxical somatodendritic decoupling supports cortical plasticity during REM sleep

Mattia Aime et al.

Summary: During REM sleep, somatodendritic decoupling in pyramidal neurons of the prefrontal cortex occurs, mainly driven by neurons from the central medial thalamus. This decoupling promotes opposite synaptic plasticity mechanisms that optimize emotional responses to future behavioral stressors.

SCIENCE (2022)

Review Behavioral Sciences

Opinion Memory leaks: information shared across memory systems

Edwin M. Robertson

Summary: The brain is highly segregated in terms of memory processing, but leaks of information can occur between different memory types. These leaks can be simple, allowing or preventing further processing, or complex, enabling the sharing of abstract information. The leaks occur in memories dependent upon hippocampal circuits and likely involve cortical areas as well. Leaks between memories are important for applying knowledge, understanding learning dynamics, and solving memory-related problems.

TRENDS IN COGNITIVE SCIENCES (2022)

Article Behavioral Sciences

Sleep Facilitates Extraction of Temporal Regularities With Varying Timescales

Itamar Lerner et al.

Summary: Evidence suggests that sleep plays a crucial role in memory consolidation, including strengthening existing memories and extracting regularities embedded within them. Slow-Wave sleep (SWS) has been found to be particularly involved in the extraction of temporal regularities. This study tested the prediction that sleep would have a greater impact on the extraction of temporal regularities when the time gap between events is shorter.

FRONTIERS IN BEHAVIORAL NEUROSCIENCE (2022)

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Cortical regulation of two-stage rapid eye movement sleep

Yufan Dong et al.

Summary: This study reveals that REM sleep in mice can be divided into two distinct substages with different facial movements and autonomic activities. The retrosplenial cortex (RSC) plays a crucial role in dictating cortical dynamics and regulating the transitions between REM sleep substages.

NATURE NEUROSCIENCE (2022)

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REM sleep is associated with distinct global cortical dynamics and controlled by occipital cortex

Ziyue Wang et al.

Summary: This study used mice for cortex-wide calcium imaging and revealed the spatiotemporal patterns of global cortical activity during sleep, as well as its role in regulating sleep state switching.

NATURE COMMUNICATIONS (2022)

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Memory for nonadjacent dependencies in the first year of life and its relation to sleep

Manuela Friedrich et al.

Summary: This study investigated the memory of nonadjacent dependencies in 6-8 month old infants and examined whether sleep after learning affects this memory. The results showed that infants were able to retain memory of nonadjacent dependencies regardless of whether they napped or stayed awake. However, napping did affect a specific processing stage, suggesting that memory evolves during sleep.

NATURE COMMUNICATIONS (2022)

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No evidence for a preferential role of sleep in episodic memory abstraction

Lucia M. Talamini et al.

Summary: Substantial evidence suggests that sleep plays an important role in consolidating declarative memory, which is associated with abstraction. However, there is controversy over whether sleep has a preferential role in decontextualization and abstract knowledge formation compared to wakefulness. This study replicates and extends previous research through two experiments, and the results show that sleep does not have a preferential function in this regard.

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Enhancement of Hippocampal-Thalamocortical Temporal Coordination during Slow-Frequency Long-Duration Anterior Thalamic Spindles

Zahra Alizadeh et al.

Summary: This study analyzed the impact of thalamic spindles on hippocampal dynamics and found that the coupling between the hippocampus and thalamocortical networks was enhanced during slower and longer spindles. Additionally, spindles occurring closer to slow oscillation troughs were more strongly coupled to hippocampal ripples. The study also revealed that the temporal association between CA1 spiking/ripples and thalamic spindles was stronger after spatial exploration.

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Memory-enhancing properties of sleep depend on the oscillatory amplitude of norepinephrine

Celia Kjaerby et al.

Summary: Kjaerby and Andersen et al. demonstrate the important role of norepinephrine (NE) in shaping sleep micro-architecture. NE oscillates during sleep and its amplitude affects memory consolidation and awakenings. Micro-arousals are generated in a periodic pattern during NREM sleep, while NE oscillations drive spindles. The amplitude of NE oscillations plays a crucial role in sleep micro-architecture and memory performance.

NATURE NEUROSCIENCE (2022)

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Two distinct ways to form long-term object recognition memory during sleep and wakefulness

Anuck Sawangjit et al.

Summary: Memory consolidation is promoted by both sleep and wakefulness, but their effects on hippocampal and nonhippocampal representations differ. Sleep consolidation involves event-context binding, while wake consolidation tends to strengthen context-independent representations.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2022)

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Selective engram coreactivation in idling brain inspires implicit learning

Mohamed H. Aly et al.

Summary: The passive priming of prior knowledge to assimilate ongoing experiences is essential for advanced cognitive processing. This study investigates the neural dynamics of memory assimilation and the potential creativity of the idling brain. The findings suggest that assimilating pertinent memories through coreactivation during sleep represents the neural underpinnings of sleep-triggered implicit cortical learning.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2022)

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Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall

Charles W. Dickey et al.

Summary: Declarative memory encoding, consolidation, and retrieval require the integration of elements encoded in widespread cortical locations. The mechanism whereby such binding of different components of mental events into unified representations occurs is unknown. This study found that brief high-frequency oscillations, known as ripples, occur in different brain areas and play a crucial role in memory recall and consolidation. These ripples phase-lock, co-occur, and show high-frequency correlations between widely distributed cortical locations, even between hemispheres. The findings suggest that cortical ripple co-occurrence and phase synchrony are essential for memory retrieval and potentially cognitive processes in general.

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Sigma oscillations protect or reinstate motor memory depending on their temporal coordination with slow waves

Judith Nicolas et al.

Summary: Targeted memory reactivation during sleep can enhance motor memory consolidation, and the coordination between slow and sigma oscillations plays a crucial role in memory reinstatement or protection against irrelevant information.
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Sleep-dependent upscaled excitability, saturated neuroplasticity, and modulated cognition in the human brain

Mohammad Ali Salehinejad et al.

Summary: Sleep deprivation increases cortical excitability while decreasing inhibitory function, leading to impaired cognitive performance such as memory, learning, and attention. These changes may be associated with increased EEG theta oscillations caused by sleep pressure.
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Cortico-Hippocampal Oscillations Are Associated With the Developmental Onset of Hippocampal-Dependent Memory

Maria A. Garcia-Perez et al.

Summary: This study provides new evidence for the onset of hippocampal-dependent memory during the late postnatal development stage and its relationship with oscillatory phenomena during sleep.

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Effects of a brief afternoon nap on declarative and procedural memory

Liu Qian et al.

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REM sleep-active hypothalamic neurons may contribute to hippocampal social-memory consolidation

Han Qin et al.

Summary: The hippocampal CA2 region is crucial for social memory, and sleep plays a vital role in the consolidation of social memory. Research has shown that hypothalamic neurons projecting to CA2 are highly active during REM sleep and silencing these neurons disrupts social memory consolidation.

NEURON (2022)

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Perspective Sleep, plasticity, and sensory neurodevelopment

Mark S. Blumberg et al.

Summary: Early infancy is characterized by neural plasticity and sleep plays an important role in the development of sensory and sensorimotor systems. There are three conceptual frameworks regarding the role of sleep, with the third framework being the most comprehensive.

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Contributions of memory and brain development to the bioregulation of naps and nap transitions in early childhood

Rebecca M. C. Spencer et al.

Summary: Nap transition is a universal process in human development and understanding it is crucial for maximizing early learning and cognitive outcomes. This study proposes a new hypothesis on the cognitive, physiological, and neural changes that accompany nap transitions, providing new insights into a key window of change in development.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2022)

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A cognitive process occurring during sleep is revealed by rapid eye movements

Yuta Senzai et al.

Summary: The eye movements during REM sleep reveal the gaze shifts in the virtual world of dreams, providing insight into the cognitive processes of the sleeping brain.

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The human thalamus orchestrates neocortical oscillations during NREM sleep

Thomas Schreiner et al.

Summary: The anterior thalamus plays an active role in organizing sleep rhythms in the neocortex, highlighting the functional diversity of thalamic nuclei in humans.

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Investigating the effects of sleep and sleep loss on the different stages of episodic emotional memory: A narrative review and guide to the future

Tony J. Cunningham et al.

Summary: This article reviews the research on the influence of sleep on different stages of emotional memory processing, identifies problematic overlaps in traditional sleep-wake study designs, and highlights areas for future research. It aims to be a valuable resource for hypothesis generation and promote important future research in understanding the relationship between sleep and emotional memory processing.

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Noradrenergic circuit control of non-REM sleep substates

Alejandro Osorio-Forero et al.

Summary: During NREMS, fluctuation of noradrenaline levels in thalamus are associated with sleep spindle rhythms and heart-rate variations, indicating vigilance-promoting mechanism by LC neurons. Optogenetic activation or inhibition of LC neurons can modulate sleep-spindle clustering and heart-rate variations, affecting sensory arousability during NREMS. Noradrenergic modulation of thalamic circuits plays a key role in maintaining sensory arousability in mammalian NREMS.

CURRENT BIOLOGY (2021)

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Activation for newly learned words in left medial-temporal lobe during toddlers' sleep is associated with memory for words

Elliott Gray Johnson et al.

Summary: The study found that activation in the left hippocampus and left anterior MTL is associated with memory for newly learned words, specifically when they are learned as puppet names, highlighting an early developing link between memory mechanisms and word learning in the medial temporal lobe.

CURRENT BIOLOGY (2021)

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Availability of food determines the need for sleep in memory consolidation

Nitin S. Chouhan et al.

Summary: Sleep plays an important role in memory consolidation, but under specific conditions like starvation, there is a memory formation mechanism that does not rely on sleep, providing an evolutionary advantage. Fruit flies are able to form sleep-dependent and sleep-independent memories based on an adaptive circuit mechanism, which demonstrates plasticity in memory circuits in response to changing environmental conditions.

NATURE (2021)

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Coupling of hippocampal theta and ripples with pontogeniculooccipital waves

Juan F. Ramirez-Villegas et al.

Summary: Studies demonstrate that the brainstem modulates hippocampal network events through PGO waves, promoting the learning and formation of memories. Different types of PGO waves influence events at different frequencies, leading to high neural synchrony within neural populations.

NATURE (2021)

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Coupling of gamma band activity to sleep spindle oscillations - a combined EEG/MEG study

Frederik D. Weber et al.

Summary: The study found that there is a temporal relationship between spindles and gamma activity, but the phase of this coupling varies across different spindles. This suggests that spindles might help synchronize gamma activity occurring in larger cortical networks and link local memory processing between distributed networks.

NEUROIMAGE (2021)

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Memory Reactivation during Sleep Improves Execution of a Challenging Motor Skill

Larry Y. Cheng et al.

Summary: Memory reactivation during sleep contributes to faster and more efficient learning of action execution, as demonstrated in this study. This finding suggests that sleep plays a role in supporting the learning of novel actions.

JOURNAL OF NEUROSCIENCE (2021)

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Reactivation predicts the consolidation of unbiased long-term cognitive maps

Andres D. Grosmark et al.

Summary: Offline reactivation plays a crucial role in stabilizing long-lasting spatial memories and predicting future stability of place cells days in advance. While representations of reward-adjacent locations are generally stable across days, offline reactivation has a more profound effect on stability for reward-distal locations, counterbalancing overall reward bias and predicting comprehensive formation of cognitive maps.

NATURE NEUROSCIENCE (2021)

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Memories off the top of your head

Jiyun N. Shin et al.

SCIENCE (2021)

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Brain neural patterns and the memory function of sleep

Gabrielle Girardeau et al.

Summary: Sleep is crucial for healthy cognition and memory. Different sleep stages, REM and non-REM sleep, are associated with characteristic electrophysiological patterns, reflecting the activity of underlying neural circuits that play important roles in memory consolidation and maintaining homeostasis.

SCIENCE (2021)

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Causal role for sleep-dependent reactivation of learning-activated sensory ensembles for fear memory consolidation

Brittany C. Clawson et al.

Summary: Learning-activated engram neurons play a critical role in memory recall but their role in offline memory consolidation is unclear. The authors demonstrate that sleep-associated reactivation of learning-activated sensory neurons is necessary for memory consolidation.

NATURE COMMUNICATIONS (2021)

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Memory-related hippocampal activation during sleep and temporal memory in toddlers

Lindsey N. Mooney et al.

Summary: The study found that assessing hippocampal activation during sleep can more accurately reflect the functional contribution of early memory, and that assessing the temporal aspects of memory best capture this contribution.

DEVELOPMENTAL COGNITIVE NEUROSCIENCE (2021)

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Sleep Spindles Preferentially Consolidate Weakly Encoded Memories

Dan Denis et al.

Summary: This study reveals the importance of sleep in memory consolidation, with initial memory strength playing a crucial role in determining which memories are consolidated during sleep. Furthermore, sleep spindles appear to facilitate memory consolidation based on memory strength, with weak memories benefiting the most from the presence of fast sleep spindles during non-rapid eye movement sleep.

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Cell-Type-Specific Dynamics of Calcium Activity in Cortical Circuits over the Course of Slow-Wave Sleep and Rapid Eye Movement Sleep

Niels Niethard et al.

Summary: The study revealed that during slow-wave sleep, excitatory pyramidal cells showed decreased calcium activity, but the variance in activity increased, indicating a heterogeneous regulation of network activity. Some pyramidal cells exhibited increased calcium activity during slow-wave sleep, potentially involved in memory processing.

JOURNAL OF NEUROSCIENCE (2021)

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Occipital sleep spindles predict sequence learning in a visuo-motor task

Nicolas D. Lutz et al.

Summary: This study suggests that sleep plays a role in improving the prediction of visual sequences, with sleep-spindle activity over occipital cortices showing significant correlation with sleep-dependent behavioral improvements. After sleep, attention shifts from predictable to unpredictable sequences, indicating enhanced automaticity in processing predictable sequences.
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Net decrease in spine-surface GluA1-containing AMPA receptors after post-learning sleep in the adult mouse cortex

Daisuke Miyamoto et al.

Summary: The study indicates that sleep helps strengthen synapses after learning, and molecular changes in spines during sleep are related to performance after sleep. Sleep assists in enhancing the effects of learning on synapses, while also weakening remaining spines.

NATURE COMMUNICATIONS (2021)

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Sleep's short-term memory preservation and long-term affect depotentiation effect in emotional memory consolidation: behavioral and EEG evidence

Shengzi Zeng et al.

Summary: This study investigated the short- and long-term impacts of sleep and sleep deprivation on emotional memory using behavioral and electrophysiological measures. The results showed that sleep preserved negative and neutral memories in the short term, but attenuated emotional responses to negative memories in the long term. EEG analyses revealed distinct neurocognitive processing of emotional memories between the sleep and sleep-deprivation groups.
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Reward biases spontaneous neural reactivation during sleep

Virginie Sterpenich et al.

Summary: Sleep promotes memory consolidation, with neural representations of rewarded experiences undergoing privileged reactivation during sleep, favoring their consolidation.

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Endogenous memory reactivation during sleep in humans is clocked by slow oscillation-spindle complexes

Thomas Schreiner et al.

Summary: The study shows that reactivating learning material during sleep, specifically during slow oscillations and sleep spindles, predicts the strength of memory consolidation, illustrating the role of these sleep rhythms in endogenous consolidation processes.

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Hippocampus-retrosplenial cortex interaction is increased during phasic REM and contributes to memory consolidation

Daniel Gomes de Almeida-Filho et al.

Summary: This study found that the modulation of causality between HPC and RSC during REM sleep is associated with memory retrieval, and the change in causality is positively correlated with memory performance 24 hours later. Additionally, causality peaks during theta acceleration in synchrony with phasic REM sleep, suggesting a functional role of causality modulation between RSC and HPC in hippocampo-cortical memory consolidation during REM sleep.

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Tracking the relation between gist and item memory over the course of long-term memory consolidation

Tima Zeng et al.

Summary: The study found that memories can be divided into specific memories and gist memories, and over time, gist memories start to guide item memories, with the interaction between the two changing as time passes.
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Coupling between motor cortex and striatum increases during sleep over long-term skill learning

Stefan M. Lemke et al.

Summary: The strength of cortical connectivity to the striatum influences the balance between behavioral variability and stability, with plasticity in corticostriatal connectivity being essential for learning to consistently produce skilled actions. This plasticity appears to occur during non-rapid-eye-movement (NREM) sleep, shaping cross-area coupling required for skill learning.
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Does Sleep Selectively Strengthen Certain Memories Over Others Based on Emotion and Perceived Future Relevance?

Per Davidson et al.

Summary: Although sleep has been found to have a beneficial effect on memory consolidation, not all memories are equally strengthened by sleep. While some evidence suggests that sleep may be more beneficial for certain types of memories based on emotion or other cues of future relevance, the majority of studies do not support this effect. Regarding specific factors during sleep, there is currently no sleep variable that has reliably been found to be specifically associated with the consolidation of certain kinds of memories over others based on emotion or other cues of future relevance.

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Marcus O. Harrington et al.

Summary: Recent studies have shown that auditory stimulation during slow-wave sleep can enhance neural oscillations linked to memory consolidation, particularly slow oscillations (SOs) and sleep spindles. This technique shows promise for improving memory benefits of sleep, with further research needed to fully understand its impact on memory processing. Additionally, recent work has shown that auditory stimulation can also manipulate rapid eye movement (REM) sleep theta oscillations, further enhancing the potential benefits for memory enhancement.

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Sleep spectral power correlates of prospective memory maintenance

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Sanna Lokhandwala et al.

Summary: Naps have been shown to benefit visuospatial learning in early childhood, with sleep spindles during the nap playing a role. This study found that nap can also benefit other forms of declarative learning in young children. The amount of time spent in slow wave sleep during the nap is positively associated with improved post-nap performance, suggesting slow wave sleep may support episodic memory consolidation in early childhood.

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Sleep's short-term memory preservation and long-term affect depotentiation effect in emotional memory consolidation: behavioral and EEG evidence

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Summary: The study investigated the short- and long-term impacts of sleep and sleep deprivation on emotional memory using behavioral, electrophysiological, and subjective affective measures. The results showed that sleep preserved emotional memory and affective tones in the short term, while sleep deprivation led to attenuated emotional responses to negative memories over time. EEG analyses revealed different neurocognitive processing of emotional memories between the two groups.
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