journal article Open Access Dec 01, 2023

Acoustic stimulation during sleep predicts long-lasting increases in memory performance and beneficial amyloid response in older adults

View at Publisher Save 10.1093/ageing/afad228
Abstract
Abstract

Background
Sleep and neurodegeneration are assumed to be locked in a bi-directional vicious cycle. Improving sleep could break this cycle and help to prevent neurodegeneration. We tested multi-night phase-locked acoustic stimulation (PLAS) during slow wave sleep (SWS) as a non-invasive method to improve SWS, memory performance and plasma amyloid levels.


Methods
32 healthy older adults (agemean: 68.9) completed a between-subject sham-controlled three-night intervention, preceded by a sham-PLAS baseline night.


Results
PLAS induced increases in sleep-associated spectral-power bands as well as a 24% increase in slow wave-coupled spindles, known to support memory consolidation. There was no significant group-difference in memory performance or amyloid-beta between the intervention and control group. However, the magnitude of PLAS-induced physiological responses were associated with memory performance up to 3 months post intervention and beneficial changes in plasma amyloid. Results were exclusive to the intervention group.


Discussion
Multi-night PLAS is associated with long-lasting benefits in memory and metabolite clearance in older adults, rendering PLAS a promising tool to build upon and develop long-term protocols for the prevention of cognitive decline.
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References
45
[1]
Rasch "About sleep’s role in memory" Physiol Rev (2013) 10.1152/physrev.00032.2012
[2]
Sleep Drives Metabolite Clearance from the Adult Brain

Lulu Xie, Hongyi Kang, Qiwu Xu et al.

Science 2013 10.1126/science.1241224
[3]
Coupled electrophysiological, hemodynamic, and cerebrospinal fluid oscillations in human sleep

Nina E. Fultz, Giorgio Bonmassar, Kawin Setsompop et al.

Science 2019 10.1126/science.aax5440
[4]
Chylinski "Timely coupling of sleep spindles and slow waves linked to early amyloid-β burden and predicts memory decline" Elife (2022) 10.7554/elife.78191
[5]
Feinberg "Kinetics of non-rapid eye movement delta production across sleep and waking in young and elderly normal subjects: theoretical implications" Sleep (2003) 10.1093/sleep/26.2.192
[6]
Carrier "Sleep slow wave changes during the middle years of life: changes in slow waves with age" Eur J Neurosci (2011) 10.1111/j.1460-9568.2010.07543.x
[7]
Rauchs "Is there a link between sleep changes and memory in Alzheimer’s disease?" Neuroreport (2008) 10.1097/wnr.0b013e32830867c4
[8]
Westerberg "Concurrent impairments in sleep and memory in amnestic mild cognitive impairment" J Int Neuropsychol Soc (2012) 10.1017/s135561771200001x
[9]
Wunderlin "The role of slow wave sleep in the development of dementia and its potential for preventative interventions" Psychiatry Res Neuroimaging (2020) 10.1016/j.pscychresns.2020.111178
[10]
Mander "Sleep: a novel mechanistic pathway, biomarker, and treatment target in the pathology of Alzheimer’s disease?" Trends Neurosci (2016) 10.1016/j.tins.2016.05.002
[11]
Slow wave sleep disruption increases cerebrospinal fluid amyloid-β levels

Yo-El S Ju, Sharon J Ooms, Courtney Sutphen et al.

Brain 2017 10.1093/brain/awx148
[12]
Eide "Sleep deprivation impairs molecular clearance from the human brain" Brain (2021) 10.1093/brain/awaa443
[13]
β-amyloid disrupts human NREM slow waves and related hippocampus-dependent memory consolidation

Bryce A Mander, Shawn M Marks, Jacob W Vogel et al.

Nature Neuroscience 2015 10.1038/nn.4035
[14]
Fehér "Shaping the slow waves of sleep: A systematic and integrative review of sleep slow wave modulation in humans using non-invasive brain stimulation" Sleep Med Rev (2021) 10.1016/j.smrv.2021.101438
[15]
Geiser "Targeting arousal and sleep through noninvasive brain stimulation to improve mental health" Neuropsychobiology (2020) 10.1159/000507372
[16]
Auditory Closed-Loop Stimulation of the Sleep Slow Oscillation Enhances Memory

Hong-Viet V. Ngo, Thomas Martinetz, Jan Born et al.

Neuron 2013 10.1016/j.neuron.2013.03.006
[17]
Ngo "Driving sleep slow oscillations by auditory closed-loop stimulation-a self-limiting process" J Neurosci (2015) 10.1523/jneurosci.3133-14.2015
[18]
Besedovsky "Auditory closed-loop stimulation of EEG slow oscillations strengthens sleep and signs of its immune-supportive function" Nat Commun (2017) 10.1038/s41467-017-02170-3
[19]
Henin "Closed-loop acoustic stimulation enhances sleep oscillations but not memory performance" eNeuro (2019) 10.1523/eneuro.0306-19.2019
[20]
Effects of phase-locked acoustic stimulation during a nap on EEG spectra and declarative memory consolidation

Ju Lynn Ong, June C. Lo, Nicholas I.Y.N. Chee et al.

Sleep Medicine 2016 10.1016/j.sleep.2015.10.016
[21]
Schneider "Susceptibility to auditory closed-loop stimulation of sleep slow oscillations changes with age" Sleep (2020) 10.1093/sleep/zsaa111
[22]
Papalambros "Acoustic enhancement of sleep slow oscillations and concomitant memory improvement in older adults" Front Hum Neurosci (2017) 10.3389/fnhum.2017.00109
[23]
Harrington "No benefit of auditory closed-loop stimulation on memory for semantically-incongruent associations" Neurobiol Learn Mem (2021) 10.1016/j.nlm.2021.107482
[24]
Enhanced Memory Consolidation Via Automatic Sound Stimulation During Non-REM Sleep

Miika M. Leminen, Jussi Virkkala, Emma Saure et al.

SLEEPJ 2017 10.1093/sleep/zsx003
[25]
Modulating overnight memory consolidation by acoustic stimulation during slow-wave sleep: a systematic review and meta-analysis

Marina Wunderlin, Marc A. Züst, Elisabeth Hertenstein et al.

SLEEPJ 2021 10.1093/sleep/zsaa296
[27]
The Montreal Cognitive Assessment, MoCA: A Brief Screening Tool For Mild Cognitive Impairment

Ziad S. Nasreddine, Natalie A. Phillips, Valérie Bédirian et al.

Journal of the American Geriatrics Society 2005 10.1111/j.1532-5415.2005.53221.x
[28]
The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research

Daniel J. Buysse, Charles F. Reynolds, Timothy H. Monk et al.

Psychiatry Research 1989 10.1016/0165-1781(89)90047-4
[29]
Highly specific and ultrasensitive plasma test detects Abeta(1–42) and Abeta(1–40) in Alzheimer’s disease

Elisabeth H. Thijssen, Inge M. W. Verberk, Jeroen Vanbrabant et al.

Scientific Reports 2021 10.1038/s41598-021-89004-x
[30]
Combination of plasma amyloid beta(1-42/1-40) and glial fibrillary acidic protein strongly associates with cerebral amyloid pathology

Inge M.W. Verberk, Elisabeth Thijssen, Jannet Koelewijn et al.

Alzheimer's Research & Therapy 2020 10.1186/s13195-020-00682-7
[31]
Graff-Radford "Association of low plasma Aβ42/Aβ40 ratios with increased imminent risk for mild cognitive impairment and Alzheimer disease" Arch Neurol (2007) 10.1001/archneur.64.3.354
[32]
Iber (2007)
[33]
Closed-loop modulation of local slow oscillations in human NREM sleep

Simon Ruch, Flavio Jean Schmidig, Leona Knüsel et al.

NeuroImage 2022 10.1016/j.neuroimage.2022.119682
[34]
Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep

Bernhard P Staresina, Til Ole Bergmann, Mathilde Bonnefond et al.

Nature Neuroscience 2015 10.1038/nn.4119
[35]
The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats

MATTHIAS MÖLLE, Oxana Eschenko, Steffen Gais et al.

European Journal of Neuroscience 2009 10.1111/j.1460-9568.2009.06654.x
[36]
Old Brains Come Uncoupled in Sleep: Slow Wave-Spindle Synchrony, Brain Atrophy, and Forgetting

Randolph F. Helfrich, Bryce A. Mander, William J. Jagust et al.

Neuron 2018 10.1016/j.neuron.2017.11.020
[37]
Stanyer "The impact of acoustic stimulation during sleep on memory and sleep architecture: a meta-analysis" J Sleep Res (2022) 10.1111/jsr.13385
[38]
Precise Slow Oscillation–Spindle Coupling Promotes Memory Consolidation in Younger and Older Adults

Beate E. Muehlroth, Myriam C. Sander, Yana Fandakova et al.

Scientific Reports 2019 10.1038/s41598-018-36557-z
[39]
Lustenberger "Auditory deep sleep stimulation in older adults at home: a randomized crossover trial" Commun Med (2022) 10.1038/s43856-022-00096-6
[40]
Diep "Acoustic slow wave sleep enhancement via a novel, automated device improves executive function in middle-aged men" Sleep (2020)
[41]
Navarrete "Ongoing neural oscillations predict the post-stimulus outcome of closed loop auditory stimulation during slow-wave sleep" Neuroimage (2022) 10.1016/j.neuroimage.2022.119055
[42]
Huwiler "Effects of auditory sleep modulation approaches on brain oscillatory and cardiovascular dynamics" Sleep (2022) 10.1093/sleep/zsac155
[43]
Sleep as a Potential Biomarker of Tau and β-Amyloid Burden in the Human Brain

Joseph R. Winer, Bryce A. Mander, Randolph F. Helfrich et al.

The Journal of Neuroscience 2019 10.1523/jneurosci.0503-19.2019
[44]
The Hierarchy of Coupled Sleep Oscillations Reverses with Aging in Humans

Marc Alain Züst, Christian Mikutta, Ximena Omlin et al.

The Journal of Neuroscience 2023 10.1523/jneurosci.0586-23.2023
[45]
Blood-based biomarkers for Alzheimer's disease: towards clinical implementation

Charlotte E Teunissen, Inge M W Verberk, Elisabeth H Thijssen et al.

The Lancet Neurology 2022 10.1016/s1474-4422(21)00361-6
Metrics
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Citations
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References
Details
Published
Dec 01, 2023
Vol/Issue
52(12)
License
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Authors
Funding
Peter Bockhoff Foundation
Dementia Research Switzerland—Synapsis Foundation
Dr. med. Kurt Fries-Foundation Award: 2021-CDA03
Cite This Article
Marina Wunderlin, Céline Jacqueline Zeller, Samira Rafaela Senti, et al. (2023). Acoustic stimulation during sleep predicts long-lasting increases in memory performance and beneficial amyloid response in older adults. Age and Ageing, 52(12). https://doi.org/10.1093/ageing/afad228
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