scholarly journals Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Carlos G Moreira ◽  
Christian R Baumann ◽  
Maurizio Scandella ◽  
Sergio I Nemirovsky ◽  
Sven Leach ◽  
...  

Slow waves and cognitive output have been modulated in humans by phase-targeted auditory stimulation. However, to advance its technical development and further our understanding, implementation of the method in animal models is indispensable. Here, we report the successful employment of slow waves' phase-targeted closed-loop auditory stimulation (CLAS) in rats. To validate this new tool both conceptually and functionally, we tested the effects of up- and down‑phase CLAS on proportions and spectral characteristics of sleep, and on learning performance in the single-pellet reaching task, respectively. Without affecting 24-h sleep-wake behavior, CLAS specifically altered delta (slow waves) and sigma (sleep spindles) power persistently over chronic periods of stimulation. While up-phase CLAS does not elicit a significant change in behavioral performance, down-phase CLAS exerted a detrimental effect on overall engagement and success rate in the behavioral test. Overall CLAS-dependent spectral changes were positively correlated with learning performance. Altogether, our results provide proof-of-principle evidence that phase-targeted CLAS of slow waves in rodents is efficient, safe and stable over chronic experimental periods, enabling the use of this high‑specificity tool for basic and preclinical translational sleep research.

2021 ◽  
Author(s):  
Carlos G. Moreira ◽  
Christian R. Baumann ◽  
Maurizio Scandella ◽  
Sergio I. Nemirovsky ◽  
Sven Leach ◽  
...  

AbstractSlow waves and cognitive output have been modulated in humans by phase-targeted auditory stimulation. However, to advance its technical development and further our understanding, implementation of the method in animal models is indispensable. Here, we report the successful employment of slow waves’ phase-targeted closed-loop auditory stimulation (CLAS) in rats. To validate this new tool both conceptually and functionally, we tested the effects of up- and down-phase CLAS on proportions and spectral characteristics of sleep, and on learning performance in the single pellet-reaching task, respectively. Without affecting 24-h sleep-wake behavior, CLAS specifically altered delta (slow waves) and sigma (sleep spindles) power persistently over chronic periods of stimulation. Down-phase CLAS exerted a detrimental effect on overall engagement and success rate in the behavioral test, and overall CLAS-dependent spectral changes were positively correlated with learning performance. Altogether, our results provide proof-of-principle evidence that phase-targeted CLAS of slow waves in rodents is efficient, safe and stable over chronic experimental periods, enabling the use of this high-specificity tool for basic and preclinical translational sleep research.


2019 ◽  
Author(s):  
Krugliakova Elena ◽  
Volk Carina ◽  
Jaramillo Valeria ◽  
Sousouri Georgia ◽  
Huber Reto

AbstractThe activity of different brain networks in non-rapid eye movement (NREM) sleep is regulated locally in an experience-dependent manner, reflecting the extent of the network load during wakefulness. In particular, improved task performance after sleep correlates with the local post-learning power increase of neocortical slow waves and faster oscillations such as sleep spindles and their temporal coupling. Recently, it was demonstrated that by targeting slow waves in a particular region at a particular phase with closed-loop auditory stimulation it is possible to locally manipulate slow-wave activity and interact with training-induced neuroplastic changes. Based on this finding, we tested whether closed-loop auditory stimulation targeting the up-phase of slow-waves over the right sensorimotor area might affect power in delta, theta and sigma bands and coupling between these oscillations within the circumscribed region. We demonstrate that while closed-loop auditory stimulation globally enhances power in delta, theta and sigma bands, changes in cross-frequency coupling of these oscillations were more spatially restricted. In particular, stimulation induced a significant decrease of delta-theta coupling in frontal channels, within the area of the strongest baseline coupling between these frequency bands. In contrast, a significant increase in delta-sigma coupling was observed over the right parietal area, located directly posterior to the target electrode. These findings suggest that closed-loop auditory stimulation locally modulates coupling between delta phase and sigma power in a targeted region, which could be used to manipulate sleep-dependent memory formation within the brain network of interest.


SLEEP ◽  
2019 ◽  
Vol 43 (6) ◽  
Author(s):  
Miguel Navarrete ◽  
Jules Schneider ◽  
Hong-Viet V Ngo ◽  
Mario Valderrama ◽  
Alexander J Casson ◽  
...  

Abstract Study Objectives Closed-loop auditory stimulation (CLAS) is a method for enhancing slow oscillations (SOs) through the presentation of auditory clicks during sleep. CLAS boosts SOs amplitude and sleep spindle power, but the optimal timing for click delivery remains unclear. Here, we determine the optimal time to present auditory clicks to maximize the enhancement of SO amplitude and spindle likelihood. Methods We examined the main factors predicting SO amplitude and sleep spindles in a dataset of 21 young and 17 older subjects. The participants received CLAS during slow-wave-sleep in two experimental conditions: sham and auditory stimulation. Post-stimulus SOs and spindles were evaluated according to the click phase on the SOs and compared between and within conditions. Results We revealed that auditory clicks applied anywhere on the positive portion of the SO increased SO amplitudes and spindle likelihood, although the interval of opportunity was shorter in the older group. For both groups, analyses showed that the optimal timing for click delivery is close to the SO peak phase. Click phase on the SO wave was the main factor determining the impact of auditory stimulation on spindle likelihood for young subjects, whereas for older participants, the temporal lag since the last spindle was a better predictor of spindle likelihood. Conclusions Our data suggest that CLAS can more effectively boost SOs during specific phase windows, and these differ between young and older participants. It is possible that this is due to the fluctuation of sensory inputs modulated by the thalamocortical networks during the SO.


SLEEP ◽  
2020 ◽  
Vol 43 (12) ◽  
Author(s):  
Jules Schneider ◽  
Penelope A Lewis ◽  
Dominik Koester ◽  
Jan Born ◽  
Hong-Viet V Ngo

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.


2020 ◽  
Vol 87 (9) ◽  
pp. S283-S284
Author(s):  
Bryan Baxter ◽  
Kristi Kwok ◽  
Christine Talbot ◽  
Lin Zhu ◽  
Dimitrios Mylonas ◽  
...  

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