Brain rhythms of sleep reflect neuronal activity underlying sleep‐associated memory consolidation. The modulation of brain rhythms, such as the sleep slow oscillation (SO), is used both to investigate neurophysiological mechanisms as well as to measure the impact of sleep on presumed functional correlates. Previously, closed‐loop acoustic stimulation in humans targeted to the SO Up‐state successfully enhanced the slow oscillation rhythm and phase‐dependent spindle activity, although effects on memory retention have varied. Here, we aim to disclose relations between stimulation‐induced hippocampo‐thalamo‐cortical activity and retention performance on a hippocampus‐dependent object‐place recognition task in mice by applying acoustic stimulation at four estimated SO phases compared to sham condition. Across the 3‐h retention interval at the beginning of the light phase closed‐loop stimulation failed to improve retention significantly over sham. However, retention during SO Up‐state stimulation was significantly higher than for another SO phase. At all SO phases, acoustic stimulation was accompanied by a sharp increase in ripple activity followed by about a second‐long suppression of hippocampal sharp wave ripple and longer maintained suppression of thalamo‐cortical spindle activity. Importantly, dynamics of SO‐coupled hippocampal ripple activity distinguished SOUp‐state stimulation. Non‐rapid eye movement (NREM) sleep was not impacted by stimulation, yet preREM sleep duration was effected. Results reveal the complex effect of stimulation on the brain dynamics and support the use of closed‐loop acoustic stimulation in mice to investigate the inter‐regional mechanisms underlying memory consolidation.
- Award ID(s):
- 1724405
- NSF-PAR ID:
- 10352316
- Date Published:
- Journal Name:
- Sleep
- Volume:
- 44
- Issue:
- 10
- ISSN:
- 0161-8105
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary Sleep is able to contribute not only to memory consolidation, but also to post‐sleep learning. The notion exists that either synaptic downscaling or another process during sleep increase post‐sleep learning capacity. A correlation between augmentation of the sleep slow oscillation and hippocampal activation at encoding support the contribution of sleep to encoding of declarative memories. In the present study, the effect of closed‐loop acoustic stimulation during an afternoon nap on post‐sleep encoding of two verbal (word pairs, verbal learning and memory test) and non‐verbal (figural pairs) tasks and on electroencephalogram during sleep and learning were investigated in young healthy adults (
N = 16). Closed‐loop acoustic stimulation enhanced slow oscillatory and spindle activity, but did not affect encoding at the group level. Subgroup analyses and comparisons with similar studies lead us to the tentative conclusion that further parameters such as time of day and subjects' cognitive ability influenced responses to closed‐loop acoustic stimulation. -
Sleep following learning facilitates the consolidation of memories. This effect has often been attributed to sleep-specific factors, such as the presence of sleep spindles or slow waves in the electroencephalogram (EEG). However, recent studies suggest that simply resting quietly while awake could confer a similar memory benefit. In the current study, we examined the effects of sleep, quiet rest, and active wakefulness on the consolidation of declarative and procedural memory. We hypothesized that sleep and eyes-closed quiet rest would both benefit memory compared with a period of active wakefulness. After completing a declarative and a procedural memory task, participants began a 30-min retention period with PSG (polysomnographic) monitoring, in which they either slept ( n = 24), quietly rested with their eyes closed ( n = 22), or completed a distractor task ( n = 29). Following the retention period, participants were again tested on their memory for the two learning tasks. As hypothesized, sleep and quiet rest both led to better performance on the declarative and procedural memory tasks than did the distractor task. Moreover, the performance advantages conferred by rest were indistinguishable from those of sleep. These data suggest that neurobiology specific to sleep might not be necessary to induce the consolidation of memory, at least across very short retention intervals. Instead, offline memory consolidation may function opportunistically, occurring during either sleep or stimulus-free rest, provided a favorable neurobiological milieu and sufficient reduction of new encoding.more » « less
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Differential thalamocortical interactions in slow and fast spindle generation: A computational modelCymbalyuk, Gennady S. (Ed.)more » « less
Cortical slow oscillations (SOs) and thalamocortical sleep spindles are two prominent EEG rhythms of slow wave sleep. These EEG rhythms play an essential role in memory consolidation. In humans, sleep spindles are categorized into slow spindles (8–12 Hz) and fast spindles (12–16 Hz), with different properties. Slow spindles that couple with the up-to-down phase of the SO require more experimental and computational investigation to disclose their origin, functional relevance and most importantly their relation with SOs regarding memory consolidation. To examine slow spindles, we propose a biophysical thalamocortical model with two independent thalamic networks (one for slow and the other for fast spindles). Our modeling results show that fast spindles lead to faster cortical cell firing, and subsequently increase the amplitude of the cortical local field potential (LFP) during the SO down-to-up phase. Slow spindles also facilitate cortical cell firing, but the response is slower, thereby increasing the cortical LFP amplitude later, at the SO up-to-down phase of the SO cycle. Neither the SO rhythm nor the duration of the SO down state is affected by slow spindle activity. Furthermore, at a more hyperpolarized membrane potential level of fast thalamic subnetwork cells, the activity of fast spindles decreases, while the slow spindles activity increases. Together, our model results suggest that slow spindles may facilitate the initiation of the following SO cycle, without however affecting expression of the SO Up and Down states.
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Abstract Objective Slow‐wave activity (
SWA ) during sleep is reduced in people with amnestic mild cognitive impairment (aMCI ) and is related to sleep‐dependent memory consolidation. Acoustic stimulation of slow oscillations has proven effective in enhancingSWA and memory in younger and older adults. In this study we aimed to determine whether acoustic stimulation during sleep boostsSWA and improves memory performance in people withaMCI .Methods Nine adults with
aMCI (72 ± 8.7 years) completed one night of acoustic stimulation (stim) and one night of sham stimulation (sham) in a blinded, randomized crossover study. Acoustic stimuli were delivered phase‐locked to the upstate of the endogenous sleep slow‐waves. Participants completed a declarative recall task with 44 word‐pairs before and after sleep.Results During intervals of acoustic stimulation,
SWA increased by >10% over sham intervals (P < 0.01), but memory recall increased in only five of the nine patients. The increase inSWA with stimulation was associated with improved morning word recall (r = 0.78,P = 0.012).Interpretation Acoustic stimulation delivered during slow‐wave sleep over one night was effective for enhancing
SWA in individuals withaMCI . Given established relationships betweenSWA and memory, a larger or more prolonged enhancement may be needed to consistently improve memory inaMCI .
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/sleep/zsab127
