Enhancing Memory Consolidation through Slow Oscillation and Spindle Synchronization

Abstract The dialogue between cortex and hippocampus is known to be crucial for sleep-dependent memory consolidation. During slow wave sleep, memory replay depends on slow oscillation (SO) and spindles in the (neo)cortex and sharp wave-ripples (SWRs) in the hippocampus. The mechanisms underlying interaction of these rhythms are poorly understood. We examined the interaction between cortical SO and hippocampal SWRs in a model of the hippocampo–cortico–thalamic network and compared the results with human intracranial recordings during sleep. We observed that ripple occurrence peaked following the onset of an Up-state of SO and that cortical input to hippocampus was crucial to maintain this relationship. A small fraction of ripples occurred during the Down-state and controlled initiation of the next Up-state. We observed that the effect of ripple depends on its precise timing, which supports the idea that ripples occurring at different phases of SO might serve different functions, particularly in the context of encoding the new and reactivation of the old memories during memory consolidation. The study revealed complex bidirectional interaction of SWRs and SO in which early hippocampal ripples influence transitions to Up-state, while cortical Up-states control occurrence of the later ripples, which in turn influence transition to Down-state.

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Precise Slow Oscillation–Spindle Coupling Promotes Memory Consolidation in Younger and Older Adults

Scientific Reports ◽

10.1038/s41598-018-36557-z ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 29

Author(s):

Beate E. Muehlroth ◽

Myriam C. Sander ◽

Yana Fandakova ◽

Thomas H. Grandy ◽

Björn Rasch ◽

...

Keyword(s):

Older Adults ◽

Memory Consolidation ◽

Slow Oscillation

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Slow oscillation-spindle coupling impairs emotional memory consolidation following stress

10.1101/2020.06.08.140350 ◽

2020 ◽

Author(s):

Dan Denis ◽

Sara Y. Kim ◽

Sarah M. Kark ◽

Ryan T. Daley ◽

Elizabeth A. Kensinger ◽

...

Keyword(s):

Memory Consolidation ◽

Slow Wave Sleep ◽

Sleep Stage ◽

Emotional Memory ◽

Slow Oscillation ◽

Stress Group ◽

Line Drawings ◽

Comparable Control ◽

Low Cortisol ◽

And Control

AbstractSleep and stress have both been shown to enhance emotional memory consolidation. They also interact, with the largest benefit of sleep on emotional memory being seen when stress occurs either shortly before or after memory encoding. Slow wave sleep (SWS) is believed to be critical for episodic memory consolidation, facilitated by the coupling of slow oscillations and sleep spindles. However, prior work in humans has only demonstrated slow oscillation-spindle coupling to be associated with consolidation of neutral information in non-stressed participants. Whether coupling interacts with stress to facilitate emotional memory consolidation is unknown. To address this exploratory question, we reanalyzed an existing dataset of N=64 individuals. Participants underwent a psychosocial stressor (n=32) or comparable control (n=32) prior to the encoding of 150 line drawings of neutral, positive, and negative images. All participants then slept overnight with polysomnographic recordings. The next day, they were given a surprise memory test. In the stress group, percentage of time spent in SWS was positively correlated with memory for images of all valences (all r>.35, p<.043). Results were primarily driven by those who showed a high cortisol response to the stressor (all r>.65, p<.007), compared to low cortisol responders (all r<.31, all p>.25). However, the amount of slow oscillation-spindle coupling during SWS was negatively associated with neutral (r= −.45, p=.01) and emotional (r=−.66, p<.001) memory in the stress group. The negative association with emotional memory was significantly stronger than for neutral memory (Meng z=2.04, p=.04). Between stress and control groups, there were no differences in any of the sleep measures assessed. These results highlight the importance of considering sleep microarchitecture events in addition to overall sleep stage time and suggests that stress may alter the relationship between SWS and memory consolidation.

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Transcranial Slow Oscillation Stimulation During Sleep Enhances Memory Consolidation in Rats

Brain Stimulation ◽

10.1016/j.brs.2014.03.001 ◽

2014 ◽

Vol 7 (4) ◽

pp. 508-515 ◽

Cited By ~ 36

Author(s):

Sonja Binder ◽

Karolin Berg ◽

Fernando Gasca ◽

Belen Lafon ◽

Lucas C. Parra ◽

...

Keyword(s):

Memory Consolidation ◽

Slow Oscillation

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Spontaneous slow oscillation - slow spindle features predict induced overnight memory retention

SLEEP ◽

10.1093/sleep/zsab127 ◽

2021 ◽

Author(s):

Fereshteh Dehnavi ◽

Ping Chai Koo-Poeggel ◽

Maryam Ghorbani ◽

Lisa Marshall

Keyword(s):

Memory Consolidation ◽

Learning Task ◽

Brain Regions ◽

Slow Oscillation ◽

Memory Retention ◽

Retention Performance ◽

Local Networks ◽

Neural Communication ◽

Functional Relevance ◽

With Memory

Abstract Study Objectives Synchronization of neural activity within local networks and between brain regions is a major contributor to rhythmic field potentials such as the EEG. On the other hand, dynamic changes in microstructure and activity are reflected in the EEG, for instance slow oscillation (SO) slope can reflect synaptic strength. SO-spindle coupling is a measure for neural communication. It was previously associated with memory consolidation, but also shown to reveal strong inter-individual differences. In studies, weak electric current stimulation has modulated brain rhythms and memory retention. Here we investigate whether SO-spindle coupling and SO slope during baseline sleep are associated with (predictive of) stimulation efficacy on retention performance. Methods Twenty-five healthy subjects participated in three experimental sessions. Sleep-associated memory consolidation was measured in two sessions, in one anodal transcranial direct current stimulation oscillating at subjects individual SO frequency (so-tDCS) was applied during nocturnal sleep. The third session was without a learning task (baseline sleep). The dependence on SO-spindle coupling and SO-slope during baseline sleep of so-tDCS efficacy on retention performance were investigated. Results Stimulation efficacy on overnight retention of declarative memories was associated with nesting of slow spindles to SO trough in deep non-rapid eye movement baseline sleep. Steepness and direction of SO slope in baseline sleep were features indicative for stimulation efficacy. Conclusions Findings underscore a functional relevance of activity during the SO up-to-down state transition for memory consolidation and provide support for distinct consolidation mechanisms for types of declarative memories.

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Bedtime Music, Involuntary Musical Imagery, and Sleep

Psychological Science ◽

10.1177/0956797621989724 ◽

2021 ◽

pp. 095679762198972

Author(s):

Michael K. Scullin ◽

Chenlu Gao ◽

Paul Fillmore

Keyword(s):

Sleep Quality ◽

Memory Consolidation ◽

Instrumental Music ◽

Slow Oscillation ◽

Music Listening ◽

Memory Reactivation ◽

Musical Imagery ◽

Popular Songs ◽

Nighttime Sleep

Many people listen to music for hours every day, often near bedtime. We investigated whether music listening affects sleep, focusing on a rarely explored mechanism: involuntary musical imagery (earworms). In Study 1 ( N = 199, mean age = 35.9 years), individuals who frequently listen to music reported persistent nighttime earworms, which were associated with worse sleep quality. In Study 2 ( N = 50, mean age = 21.2 years), we randomly assigned each participant to listen to lyrical or instrumental-only versions of popular songs before bed in a laboratory, discovering that instrumental music increased the incidence of nighttime earworms and worsened polysomnography-measured sleep quality. In both studies, earworms were experienced during awakenings, suggesting that the sleeping brain continues to process musical melodies. Study 3 substantiated this possibility by showing a significant increase in frontal slow oscillation activity, a marker of sleep-dependent memory consolidation. Thus, some types of music can disrupt nighttime sleep by inducing long-lasting earworms that are perpetuated by spontaneous memory-reactivation processes.

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The Overnight Retention of Novel Metaphors Associates With Slow Oscillation–Spindle Coupling but Not With Respiratory Phase at Encoding

Frontiers in Behavioral Neuroscience ◽

10.3389/fnbeh.2021.712774 ◽

2021 ◽

Vol 15 ◽

Author(s):

Risto Halonen ◽

Liisa Kuula ◽

Minea Antila ◽

Anu-Katriina Pesonen

Keyword(s):

Neural Activity ◽

Memory Consolidation ◽

Memory Task ◽

Slow Oscillation ◽

Sleep Spindles ◽

Memory Retention ◽

Mixed Design ◽

Respiratory Phase ◽

Local Nature ◽

Temporal Overlap

Accumulating evidence emphasizes the relevance of oscillatory synchrony in memory consolidation during sleep. Sleep spindles promote memory retention, especially when occurring in the depolarized upstate of slow oscillation (SO). A less studied topic is the inter-spindle synchrony, i.e. the temporal overlap and phasic coherence between spindles perceived in different electroencephalography channels. In this study, we examined how synchrony between SOs and spindles, as well as between simultaneous spindles, is associated with the retention of novel verbal metaphors. Moreover, we combined the encoding of the metaphors with respiratory phase (inhalation/exhalation) with the aim of modulating the strength of memorized items, as previous studies have shown that inhalation entrains neural activity, thereby benefiting memory in a waking condition. In the current study, 27 young adults underwent a two-night mixed-design study with a 12-h delayed memory task during both sleep and waking conditions. As expected, we found better retention over the delay containing sleep, and this outcome was strongly associated with the timing of SO–spindle coupling. However, no associations were observed regarding inter-spindle synchrony or respiratory phase. These findings contribute to a better understanding of the importance of SO–spindle coupling for memory. In contrast, the observed lack of association with inter-spindle synchrony may emphasize the local nature of spindle-related plasticity.

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Theta activity during encoding interacts with NREM sleep oscillations to predict memory generalization

10.1101/2021.11.18.469190 ◽

2021 ◽

Author(s):

Tamara Gibson ◽

Zachariah Reuben Cross ◽

Alex Chatburn

Keyword(s):

Memory Consolidation ◽

Nrem Sleep ◽

Theoretical Models ◽

Theta Activity ◽

Slow Oscillation ◽

Oscillatory Activity ◽

Sleep Spindle ◽

Related Activity ◽

Theta Power ◽

Sleep Condition

Relatively little is known regarding the interaction between encoding-related neural activity and sleep-based memory consolidation. One suggestion is that a function of encoding-related theta power may be to 'tag' memories for subsequent processing during sleep. This study aimed to extend previous work on the relationships between sleep spindles, slow oscillation-spindle coupling and task-related theta activity with a combined Deese-Roediger-McDermott (DRM) and nap paradigm. This allowed us to examine the influence of task- and sleep-related oscillatory activity on the recognition of both encoded list words and associative theme words. Thirty-three participants (29 females, mean age = 23.2 years) learned and recognised DRM lists separated by either a 2hr wake or sleep period. Mixed-effects modelling revealed the sleep condition endorsed more associative theme words and fewer list words in comparison to the wake group. Encoding related theta power was also found to influence sleep spindle density, and this interaction was predictive of memory outcomes. The influence of encoding-related theta was specific to sleep spindle density, and did not appear to influence the strength of slow oscillation-spindle coupling as it relates to memory outcomes. The finding of interactions between wakeful and sleep oscillatory-related activity in promoting memory and learning has important implications for theoretical models of sleep-based memory consolidation.

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Electrophysiological Indicators of Sleep-associated Memory Consolidation in 5- to 6-year-old Children

10.1101/2020.09.04.283606 ◽

2020 ◽

Author(s):

Ann-Kathrin Joechner ◽

Sarah Wehmeier ◽

Markus Werkle-Bergner

Keyword(s):

Young Adults ◽

School Children ◽

Memory Consolidation ◽

Declarative Memory ◽

Slow Oscillation ◽

Sleep Spindles ◽

Sleep Spindle ◽

Slow Oscillations ◽

Slow Sleep ◽

Temporal Coupling

ABSTRACTIn young adults, memory consolidation during sleep is supported by a time-coordinated interplay of sleep spindles and slow oscillations. However, given tremendous developmental changes in sleep spindle and slow oscillation morphology, it remains elusive whether the same mechanisms as identified in young adults are comparably functional across childhood. Here, we characterise slow and fast sleep spindles and their temporal coupling to slow oscillations in 24 pre-school children. Further, we ask whether slow and fast sleep spindles and their modulation during slow oscillations are similarly associated with behavioural indicators of declarative memory consolidation as suggested from adult literature. Employing a development-sensitive, individualised approach, we reliably identify an inherent, development-specific fast sleep spindle type, though nested in the adult-like slow sleep spindle frequency range, along with a dominant slow sleep spindle type. Further, we provide evidence for the modulation of fast sleep spindles during slow oscillations, already in pre-school children. However, the temporal coordination between fast sleep spindles and slow oscillations is weaker and less precise than expected from adult research. While we do not find evidence for a critical contribution of the pattern of fast sleep spindle modulation during slow oscillations for memory consolidation, crucially, both inherent slow and fast sleep spindles separately are differentially related to sleep-associated consolidation of items of varying quality. While a higher number of slow sleep spindles is associated with stronger maintenance of medium-quality memories, more fast sleep spindles are linked to higher gain of low-quality items. Our results provide evidence for two functionally relevant inherent sleep spindle types in pre-school children despite not fully matured sleep spindle – slow oscillation coupling.

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Spindle - slow oscillation coupling correlates with memory performance and connectivity changes in a hippocampal network after sleep

10.1101/2021.10.27.466071 ◽

2021 ◽

Author(s):

Lisa Marie Bastian ◽

Anumita Samanta ◽

Demetrius Ribeiro de Paula ◽

Frederik Weber ◽

Robby Schoenfeld ◽

...

Keyword(s):

Functional Connectivity ◽

Spatial Memory ◽

Learning Strategies ◽

Memory Consolidation ◽

Resting State ◽

Memory Performance ◽

Slow Oscillation ◽

Long Term Memory ◽

Holistic Understanding ◽

Hippocampal Network

After experiences are encoded, post-encoding reactivations during sleep have been proposed to mediate long-term memory consolidation. Spindle-slow oscillation coupling during NREM sleep is a candidate mechanism through which a hippocampal-cortical dialogue may strengthen a newly formed memory engram. Here, we investigated the role of fast spindle- and slow spindle-slow oscillation coupling in the consolidation of spatial memory in humans with a virtual water maze task involving allocentric and egocentric learning strategies. Furthermore, we analyzed how resting-state functional connectivity evolved across learning, consolidation, and retrieval of this task using a data-driven approach. Our results show task-related connectivity changes in the executive control network, the default mode network, and the hippocampal network at post-task rest. The hippocampal network could further be divided into two subnetworks of which only one showed modulation by sleep. Decreased functional connectivity in this subnetwork was associated with higher spindle-slow oscillation coupling power, which was also related to better memory performance at test. Overall, this study contributes to a more holistic understanding of the functional resting-state networks and the mechanisms during sleep associated to spatial memory consolidation.

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