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Susceptibility to auditory closed-loop stimulation of sleep slow oscillations changes with age.

ABSTRACT: Study objectives: Cortical slow oscillations (SOs) and thalamocortical sleep spindles hallmark slow wave sleep and facilitate memory consolidation, both of which are reduced with age. Experiments utilizing auditory closed-loop stimulation to enhance these oscillations showed great potential in young and older subjects. However, the magnitude of responses has yet to be compared between these age groups. We examined the possibility of enhancing SOs and performance on different memory tasks in a healthy middle-aged population using this stimulation and contrast effects to younger adults.

Methods: In a within-subject design, 17 subjects (55.7 ± 1.0 years) received auditory stimulation in synchrony with SO up-states, which was compared to a no-stimulation sham condition. Overnight memory consolidation was assessed for declarative word-pairs and procedural finger-tapping skill. Post-sleep encoding capabilities were tested with a picture recognition task. Electrophysiological effects of stimulation were compared to a previous younger cohort (n = 11, 24.2 ± 0.9 years).

Results: Overnight retention and post-sleep encoding performance of the older cohort revealed no beneficial effect of stimulation, which contrasts with the enhancing effect the same stimulation protocol had in our younger cohort. Auditory stimulation prolonged endogenous SO trains and induced sleep spindles phase-locked to SO up-states in the older population. However, responses were markedly reduced compared to younger subjects. Additionally, the temporal dynamics of stimulation effects on SOs and spindles differed between age groups.

Conclusions: Our findings suggest that the susceptibility to auditory stimulation during sleep drastically changes with age and reveal the difficulties of translating a functional protocol from younger to older populations.

SUBMITTER: Schneider J

PROVIDER: S-EPMC7734479 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Susceptibility to auditory closed-loop stimulation of sleep slow oscillations changes with age.

Schneider Jules J Lewis Penelope A PA Koester Dominik D Born Jan J Ngo Hong-Viet V HV

Sleep 20201201 12

<h4>Study objectives</h4>Cortical slow oscillations (SOs) and thalamocortical sleep spindles hallmark slow wave sleep and facilitate memory consolidation, both of which are reduced with age. Experiments utilizing auditory closed-loop stimulation to enhance these oscillations showed great potential in young and older subjects. However, the magnitude of responses has yet to be compared between these age groups. We examined the possibility of enhancing SOs and performance on different memory tasks ...[more]

PMID: 32562487

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Project description:Recent research has shown that auditory closed-loop stimulation can enhance sleep slow oscillations (SO) to improve N3 sleep quality and cognition. Previous studies have been conducted in lab environments. The present study aimed to validate and assess the performance of a novel ambulatory wireless dry-EEG device (WDD), for auditory closed-loop stimulation of SO during N3 sleep at home. The performance of the WDD to detect N3 sleep automatically and to send auditory closed-loop stimulation on SO were tested on 20 young healthy subjects who slept with both the WDD and a miniaturized polysomnography (part 1) in both stimulated and sham nights within a double blind, randomized and crossover design. The effects of auditory closed-loop stimulation on delta power increase were assessed after one and 10 nights of stimulation on an observational pilot study in the home environment including 90 middle-aged subjects (part 2).The first part, aimed at assessing the quality of the WDD as compared to a polysomnograph, showed that the sensitivity and specificity to automatically detect N3 sleep in real-time were 0.70 and 0.90, respectively. The stimulation accuracy of the SO ascending-phase targeting was 45 ± 52°. The second part of the study, conducted in the home environment, showed that the stimulation protocol induced an increase of 43.9% of delta power in the 4 s window following the first stimulation (including evoked potentials and SO entrainment effect). The increase of SO response to auditory stimulation remained at the same level after 10 consecutive nights. The WDD shows good performances to automatically detect in real-time N3 sleep and to send auditory closed-loop stimulation on SO accurately. These stimulation increased the SO amplitude during N3 sleep without any adaptation effect after 10 consecutive nights. This tool provides new perspectives to figure out novel sleep EEG biomarkers in longitudinal studies and can be interesting to conduct broad studies on the effects of auditory stimulation during sleep.

Project description:Purpose:In non-rapid eye movement (NREM) stage 3 sleep (N3), phase-locked pink noise auditory stimulation can amplify slow oscillatory activity (0.5-1 Hz). Open-loop pink noise auditory stimulation can amplify slow oscillatory and delta frequency activity (0.5-4 Hz). We assessed the ability of pink noise and other sounds to elicit delta power, slow oscillatory power, and N3 sleep. Participants and Methods:Participants (n = 8) underwent four consecutive inpatient nights in a within-participants design, starting with a habituation night. A registered polysomnographic technologist live-scored sleep stage and administered stimuli on randomized counterbalanced Enhancing and Disruptive nights, with a preceding Habituation night (night 1) and an intervening Sham night (night 3). A variety of non-phase-locked pink noise stimuli were used on Enhancing night during NREM; on Disruptive night, environmental sounds were used throughout sleep to induce frequent auditory-evoked arousals. Results:Total sleep time did not differ between conditions. Percentage of N3 was higher in the Enhancing condition, and lower in the Disruptive condition, versus Sham. Standard 0.8 Hz pink noise elicited low-frequency power more effectively than other pink noise, but was not the most effective stimulus. Both pink noise on the "Enhancing" night and sounds intended to Disrupt sleep administered on the "Disruptive" night increased momentary delta and slow-wave activity (ie, during stimulation versus the immediate pre-stimulation period). Disruptive auditory stimulation degraded sleep with frequent arousals and increased next-day vigilance lapses versus Sham despite preserved sleep duration and momentary increases in delta and slow-wave activity. Conclusion:These findings emphasize sound features of interest in ecologically valid, translational auditory intervention to increase restorative sleep. Preserving sleep continuity should be a primary consideration if auditory stimulation is used to enhance slow-wave activity.

Project description:OBJECTIVE:Optogenetics provides a means to probe functional connections between brain areas. By activating a set of presynaptic neurons and recording the activity from a downstream brain area, one can establish the sign and strength of a feedforward connection. One challenge is that there are virtually limitless patterns that can be used to stimulate a presynaptic brain area. Functional influences on downstream brain areas can depend not just on whether presynaptic neurons were activated, but how they were activated. Corticofugal axons from the auditory cortex (ACtx) heavily innervate the auditory tectum, the inferior colliculus (IC). Here, we sought to determine whether different modes of corticocollicular activation could titrate the strength of feedforward modulation of sound processing in IC neurons. APPROACH:We used multi-channel electrophysiology and optogenetics to record from multiple regions of the IC in awake head-fixed mice while optogenetically stimulating ACtx neurons expressing Chronos, an ultra-fast channelrhodopsin. To identify cortical activation patterns associated with the strongest effects on IC firing rates, we employed a closed-loop evolutionary optimization procedure that tailored the voltage command signal sent to the laser based on spike feedback from single IC neurons. MAIN RESULTS:Within minutes, our evolutionary search procedure converged on ACtx stimulation configurations that produced more effective and widespread enhancement of IC unit activity than generic activation parameters. Cortical modulation of midbrain spiking was bi-directional, as the evolutionary search procedure could be programmed to converge on activation patterns that either suppressed or enhanced sound-evoked IC firing rate. SIGNIFICANCE:This study introduces a closed-loop optimization procedure to probe functional connections between brain areas. Our findings demonstrate that the influence of descending feedback projections on subcortical sensory processing can vary both in sign and degree depending on how cortical neurons are activated in time.

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Susceptibility to auditory closed-loop stimulation of sleep slow oscillations changes with age.

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Susceptibility to auditory closed-loop stimulation of sleep slow oscillations changes with age.

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