The role of slow-wave sleep rhythms in the cortical-hippocampal loop for memory consolidation

AbstractNewly acquired memory traces are spontaneously reactivated during slow-wave sleep (SWS), leading to the consolidation of recent memories. Empirical studies found that sensory stimulation during SWS selectively enhances memory consolidation and the effect depends on the phase of stimulation. In this new study, we aimed to understand the mechanisms behind the role of sensory stimulation on memory consolidation using computational models implementing effects of neuromodulators to simulate transitions between awake and SWS sleep, and synaptic plasticity to allow the change of synaptic connections due to the training in awake or replay during sleep. We found that when closed-loop stimulation was applied during the Down states (900-2700) of sleep slow oscillation, particularly right before transition from Down to Up state, it significantly affected the spatio-temporal pattern of the slow-waves and maximized memory replay. In contrast, when the stimulation was presented during the Up states (2700-3600 and 00-900), it did not have a significant impact on the slow-waves or memory performance after sleep. For multiple memories trained in awake, presenting stimulation cues associated with specific memory trace could selectively augment replay and enhance consolidation of that memory and interfere with consolidation of the others (particularly weak) memories. Our study proposes a synaptic level mechanism of how memory consolidation is affected by sensory stimulation during sleep.Significance statementStimulation, such as training-associated cues or auditory stimulation, during sleep can augment consolidation of the newly encoded memories. In this study, we used a computational model of the thalamocortical system to describe the mechanisms behind the role of stimulation in memory consolidation during slow-wave sleep. Our study suggested that stimulation preferentially strengthens the memory traces when delivered at specific phase of slow oscillations just before Down to Up state transition when it makes the largest impact on the spatio-temporal pattern of sleep slow waves. In the presence of multiple memories, presenting sensory cues during sleep could selectively strengthen selected memories. Our study proposes a synaptic level mechanism of how memory consolidation is affected by sensory stimulation during sleep.

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Faculty Opinions recommendation of Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1020901.240539 ◽

2004 ◽

Author(s):

Michael E Hasselmo

Keyword(s):

Slow Wave ◽

Memory Consolidation ◽

Slow Wave Sleep ◽

Declarative Memory

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Faculty Opinions recommendation of Odor cues during slow-wave sleep prompt declarative memory consolidation.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1069824.524599 ◽

2007 ◽

Author(s):

Edvard I Moser

Keyword(s):

Slow Wave ◽

Memory Consolidation ◽

Slow Wave Sleep ◽

Declarative Memory ◽

Odor Cues

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Faculty Opinions recommendation of Learning-dependent, transient increase of activity in noradrenergic neurons of locus coeruleus during slow wave sleep in the rat: brain stem-cortex interplay for memory consolidation?

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1103341.559379 ◽

2008 ◽

Author(s):

Mark Mayford

Keyword(s):

Locus Coeruleus ◽

Brain Stem ◽

Rat Brain ◽

Slow Wave ◽

Memory Consolidation ◽

Slow Wave Sleep ◽

Transient Increase ◽

Noradrenergic Neurons

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Bi-Temporal Anodal Transcranial Direct Current Stimulation during Slow-Wave Sleep Boosts Slow-Wave Density but Not Memory Consolidation

Brain Sciences ◽

10.3390/brainsci11040410 ◽

2021 ◽

Vol 11 (4) ◽

pp. 410

Author(s):

Simon Ruch ◽

Kristoffer Fehér ◽

Stephanie Homan ◽

Yosuke Morishima ◽

Sarah Maria Mueller ◽

...

Keyword(s):

Episodic Memory ◽

Slow Wave ◽

Direct Current ◽

Memory Consolidation ◽

Transcranial Direct Current Stimulation ◽

Slow Wave Sleep ◽

Memory Performance ◽

Direct Current Stimulation ◽

Sleep Parameters ◽

Episodic Memories

Slow-wave sleep (SWS) has been shown to promote long-term consolidation of episodic memories in hippocampo–neocortical networks. Previous research has aimed to modulate cortical sleep slow-waves and spindles to facilitate episodic memory consolidation. Here, we instead aimed to modulate hippocampal activity during slow-wave sleep using transcranial direct current stimulation in 18 healthy humans. A pair-associate episodic memory task was used to evaluate sleep-dependent memory consolidation with face–occupation stimuli. Pre- and post-nap retrieval was assessed as a measure of memory performance. Anodal stimulation with 2 mA was applied bilaterally over the lateral temporal cortex, motivated by its particularly extensive connections to the hippocampus. The participants slept in a magnetic resonance (MR)-simulator during the recordings to test the feasibility for a future MR-study. We used a sham-controlled, double-blind, counterbalanced randomized, within-subject crossover design. We show that stimulation vs. sham significantly increased slow-wave density and the temporal coupling of fast spindles and slow-waves. While retention of episodic memories across sleep was not affected across the entire sample of participants, it was impaired in participants with below-average pre-sleep memory performance. Hence, bi-temporal anodal direct current stimulation applied during sleep enhanced sleep parameters that are typically involved in memory consolidation, but it failed to improve memory consolidation and even tended to impair consolidation in poor learners. These findings suggest that artificially enhancing memory-related sleep parameters to improve memory consolidation can actually backfire in those participants who are in most need of memory improvement.

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Selection of stimulus parameters for enhancing slow wave sleep events with a Neural-field theory thalamocortical computational model

10.1101/2021.02.03.429528 ◽

2021 ◽

Author(s):

Felipe A. Torres ◽

Patricio Orio ◽

María-José Escobar

Keyword(s):

Computational Model ◽

Slow Wave ◽

Memory Consolidation ◽

Closed Loop ◽

Slow Wave Sleep ◽

Brain Activity ◽

Sensory Stimulation ◽

Sleep Spindles ◽

Slow Oscillations ◽

Closed Loop Stimulation

AbstractSlow-wave sleep cortical brain activity, conformed by slow-oscillations and sleep spindles, plays a key role in memory consolidation. The increase of the power of the slow-wave events, obtained by auditory sensory stimulation, positively correlates to memory consolidation performance. However, little is known about the experimental protocol maximizing this effect, which could be induced by the power of slow-oscillation, the number of sleep spindles, or the timing of both events’ co-occurrence. Using a mean-field model of thalamocortical activity, we studied the effect of several stimulation protocols, varying the pulse shape, duration, amplitude, and frequency, as well as a target-phase using a closed-loop approach. We evaluated the effect of these parameters on slow-oscillations (SO) and sleep-spindles (SP), considering: (i) the power at the frequency bands of interest, (ii) the number of SO and SP, (iii) co-occurrences between SO and SP, and (iv) synchronization of SP with the up-peak of the SO. The first three targets are maximized using a decreasing ramp pulse with a pulse duration of 50 ms. Also, we observed a reduction in the number of SO when increasing the stimulus energy by rising its amplitude. To assess the target-phase parameter, we applied closed-loop stimulation at 0º, 45º, and 90º of the phase of the narrow-band filtered ongoing activity, at 0.85 Hz as central frequency. The 0º stimulation produces better results in the power and number of SO and SP than the rhythmic or aleatory stimulation. On the other hand, stimulating at 45º or 90º change the timing distribution of spindles centers but with fewer co-occurrences than rhythmic and 0º phase. Finally, we propose the application of closed-loop stimulation at the rising zero-cross point using pulses with a decreasing ramp shape and 50 ms of duration for future experimental work.Author summaryDuring the non-REM (NREM) phase of sleep, events that are known as slow oscillations (SO) and spindles (SP) can be detected by EEG. These events have been associated with the consolidation of declarative memories and learning. Thus, there is an ongoing interest in promoting them during sleep by non-invasive manipulations such as sensory stimulation. In this paper, we used a computational model of brain activity that generates SO and SP, to investigate which type of sensory stimulus –shape, amplitude, duration, periodicity– would be optimal for increasing the events’ frequency and their co-occurrence. We found that a decreasing ramp of 50 ms duration is the most effective. The effectiveness increases when the stimulus pulse is delivered in a closed-loop configuration triggering the pulse at a target phase of the ongoing SO activity. A desirable secondary effect is to promote SPs at the rising phase of the SO oscillation.

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036 The Effect of Exercise on Sleep Architecture and Memory Consolidation during a Daytime Nap

SLEEP ◽

10.1093/sleep/zsab072.035 ◽

2021 ◽

Vol 44 (Supplement_2) ◽

pp. A16-A16

Author(s):

Megan Collins ◽

Erin Wamsley ◽

Hailey Napier ◽

Madeline Ray

Keyword(s):

Slow Wave ◽

Memory Consolidation ◽

Slow Wave Sleep ◽

Declarative Memory ◽

Sleep Stage ◽

Sleep Time ◽

Learning Task ◽

Memory Retention ◽

Verbal Information ◽

Significant Difference

Abstract Introduction Slow wave sleep (SWS) is thought to especially benefit declarative memory (i.e., memory for facts and events). As such, recent studies have used various methods to experimentally increase the amount of slow wave sleep that participants obtain, with the goal of assessing how SWS affects declarative memory consolidation. Studies dating back decades have reported that exercising before sleep may increase time spent in SWS. Thus, the aim of the current project was to determine whether exercising after learning verbal information enhances slow wave sleep during a subsequent nap and/or enhances memory for verbal information. Methods Participants who exercised regularly were recruited to attend two 2.5hr laboratory sessions. During each session, they trained on a paired associates learning task and then completed either a 20min cardiovascular exercise routine or a 20min stretching routine. Following a 1hr nap opportunity, participants were tested on their memory. PSG was recorded during the nap, and scored following AASM criteria. Participants were excluded from analysis if they failed to sleep for at least 10 min. Following exclusions, n=30 participants were included in analysis. Results Contrary to our hypotheses, there was no significant difference between the exercise and stretching conditions for minutes spent in slow wave sleep (p=.16), % time spent in slow wave sleep (p=.22), or raw improvement in paired associated performance (p=.23). The amount of SWS obtained during the nap did not correlate with performance in either condition (SWS min vs. memory in exercise condition: r28=.10, p=.60; sleep condition: r28=-.06, p=.74). Exercise did not affect time spent in any other sleep stage, nor did it affect total sleep time. Conclusion Contrary to our hypotheses and the results of prior research, we were unable to detect a significant effect of exercise on slow wave sleep. Also contrary to our hypotheses, exercise did not affect memory retention across the nap interval. These null results could indicate that there is no effect of exercise on nap sleep and/or associated memory retention. However, it could also be that we lacked sufficient power to detect effects that were smaller than expected. Support (if any):

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Bidirectional Interaction of Hippocampal Ripples and Cortical Slow Waves Leads to Coordinated Spiking Activity During NREM Sleep

Cerebral Cortex ◽

10.1093/cercor/bhaa228 ◽

2020 ◽

Vol 31 (1) ◽

pp. 324-340

Author(s):

Pavel Sanda ◽

Paola Malerba ◽

Xi Jiang ◽

Giri P Krishnan ◽

Jorge Gonzalez-Martinez ◽

...

Keyword(s):

Slow Wave ◽

Memory Consolidation ◽

Slow Wave Sleep ◽

Nrem Sleep ◽

Slow Waves ◽

Slow Oscillation ◽

Cortical Input ◽

Sharp Wave ◽

Up States ◽

Intracranial Recordings

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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