Abstract
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 hr 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.
Highlights
Non-invasive neuromodulation strategies are en vogue for their unique potential to diagnose and treat neurological and psychiatric disorders, or to rebalance the activity in dysfunctional brain networks
Regarding online precision of non-rapid eye movement (NREM) sleep staging, 70% of epochs were confirmed offline as NREM sleep, whereas 18% were later identified as wakefulness and 2% as REM sleep (Fig. 3b)
We explored the distribution of triggers across sleep stages and observed that up-phase stimulated animals received more sound triggers during NREM sleep than down-phase stimulated subjects
Summary
Non-invasive neuromodulation strategies are en vogue for their unique potential to diagnose and treat neurological and psychiatric disorders, or to rebalance the activity in dysfunctional brain networks. Innovative approaches to further comprehend and eventually enable therapeutic implementations of SWS modulation have been tested Auditory stimulation during SWS was successfully implemented in human subjects in laboratory-based settings. V. Ngo, Claussen, Born, & Mölle, 2013; Tononi, Riedner, Hulse, Ferrarelli, & Sarasso, 2010), but was later developed further to deliver auditory stimulation in synchrony with the brain’s own rhythm in a closed-loop manner Targeting ongoing slow waves in their up-phase enhanced slow oscillations during SWS, while targeting the waves’ down-phase had the opposite effect. The success of the human implementation of CLAS further encouraged the development of portable devices enabling acoustic stimulation in a home-based environment (Ferster, Lustenberger, & Karlen, 2019)
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