Boosting Recovery During Sleep by Means of Auditory Stimulation

Krugliakova, Elena; Skorucak, Jelena; Sousouri, Georgia; Leach, Sven; Snipes, Sophia; Ferster, Maria Laura; Poian, Giulia Da; Karlen, Walter; Huber, Reto

doi:10.3389/fnins.2022.755958

Cited by 13 publications

(17 citation statements)

References 51 publications

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“…The possibility of non-invasive modulation of sleep oscillations has recently attracted significant attention (Bellesi, Riedner, Garcia-Molina, Cirelli, & Tononi, 2014; Choi, Kwon, & Jun, 2020; Fattinger et al, 2019; Frase et al, 2019; Geiser et al, 2020; Krugliakova et al, 2022; Malkani & Zee, 2020; Marshall, Helgadottir, Molle, & Born, 2006; Ngo, Martinetz, Born, & Molle, 2013; Schneider, Lewis, Koester, Born, & Ngo, 2020). Slow waves are a predominant type of sleep oscillatory activity during NREM sleep, but can also occur during REM sleep and wakefulness (Andrillon, Burns, Mackay, Windt, & Tsuchiya, 2021; Bernardi et al, 2019; Borbely, Tobler, & Hanagasioglu, 1984; Funk, Honjoh, Rodriguez, Cirelli, & Tononi, 2016; Vyazovskiy et al, 2014; Vyazovskiy et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Neuronal-spiking-based closed-loop stimulation during cortical ON and OFF states in freely moving mice

Kahn

Krone

Blanco‐Duque

et al. 2022

Preprint

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The slow oscillation (SO) is a central neuronal dynamic during sleep and is generated by alternating periods of high and low neuronal activity (ON and OFF states). Mounting evidence causally links the SO to sleep's functions, and it has recently become possible to manipulate the SO non-invasively and phase-specifically. These developments represent promising clinical avenues, but they also highlight the importance of improving our understanding of how ON/OFF states affect incoming stimuli and what role they play in neuronal plasticity. Most studies using closed-loop stimulation rely on the electroencephalogram (EEG) and local field potential (LFP) signals, which reflect neuronal ON and OFF states only indirectly. Here we develop an online detection algorithm based on spiking activity recorded from laminar arrays in mouse motor cortex. We find that online detection of ON and OFF states reflects specific phases of spontaneous LFP SO. Our neuronal-spiking-based closed-loop procedure offers a novel opportunity for testing the functional role of SO in sleep-related restorative processes and neural plasticity.

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Section: Introductionmentioning

confidence: 99%

Neuronal-spiking-based closed-loop stimulation during cortical ON and OFF states in freely moving mice

Kahn

Krone

Blanco‐Duque

et al. 2022

Preprint

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“…Assuming that different pupil levels track different arousal levels, we would expect that the cortical response to auditory stimulation differs depending on when these stimuli are played as a function of pupil size. According to previous research, we found auditory stimulation to increase delta and sigma power dynamics 35,[44][45][46][47][48][49][50] . These delta responses are believed to involve enhanced slow waves or Kcomplexes 51,52 .…”

Section: Discussionmentioning

confidence: 71%

Pupil size reveals arousal level dynamics in human sleep

Carro-Domínguez,

Huwiler,

Oberlin

et al. 2023

Preprint

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Changes in arousal level are a determining characteristic of healthy and pathological sleep in humans, but how they are conventionally measured lack sensitivity and temporal precision. Recent animal research has revealed the intricate dynamics of arousal levels that are potentially crucial for maintaining proper sleep resilience and memory consolidation. To investigate whether similar dynamics exist in humans, we measured pupil size, an established indicator of arousal levels, for the first time during overnight sleep and tested the cortical response to auditory stimulation at different levels of arousal. Here we show that pupil size dynamics correspond to sleep macrostructure and microstructural events, while exhibiting an inverse relationship with fluctuations of sleep spindles, a marker of sleep resilience and memory consolidation. Additionally, pupil size prior to auditory stimulation influences its effectiveness to enhance delta power, a marker of several restorative and regenerative functions of sleep. These pupil size dynamics provide novel insights into the interplay between arousal levels and sleep, opening avenues for future research and clinical applications in diagnosing and treating pathological sleep associated with abnormal arousal levels.

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“…It is also conceivable and would be of interest to investigate, whether specifically targeted memory activation reveals a higher efficiency with a longer time period between learning and manipulation periods. Furthermore, the effect of unspecifc stimuli in non‐invasive brain stimulation procedures on memory consolidation in humans appears to rely strongly on the brain state, as either a trait or state property (Dehnavi et al, 2021; Krugliakova et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

Single closed‐loop acoustic stimulation targeting memory consolidation suppressed hippocampal ripple and thalamo‐cortical spindle activity in mice

Aksamaz,

Mölle,

Akinola

et al. 2023

Eur J of Neuroscience

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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.

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Boosting Recovery During Sleep by Means of Auditory Stimulation

Cited by 13 publications

References 51 publications

Neuronal-spiking-based closed-loop stimulation during cortical ON and OFF states in freely moving mice

Neuronal-spiking-based closed-loop stimulation during cortical ON and OFF states in freely moving mice

Pupil size reveals arousal level dynamics in human sleep

Single closed‐loop acoustic stimulation targeting memory consolidation suppressed hippocampal ripple and thalamo‐cortical spindle activity in mice

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