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  1. Evaluation Summary:

    This manuscript describes their phase-targeted closed-loop auditory stimulation protocol to alter slow wave oscillations in rodents. This manuscript provides a set of proof-of-concept data for a rodent model of closed-loop auditory stimulation during sleep as a method for augmenting NREM sleep thalamocortical oscillations and its behavioral effect on a motor task. The strongest contribution of this study to the field is that it provides a technical basis for future studies to be carried out which actually explore the neurobiological underpinnings of CLAS in detail. Applying this tool to rodent research in future studies may allow for bridging some of the putative mechanisms underlying memory consolidation (e.g., replay during NREM sleep) and behavioral changes observed with sleep (e.g., improved hippocampus-dependent memory). It's also nice to have a non-invasive way to manipulate sleep, particularly to translate rodent research to clinical work.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

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  2. Reviewer #1 (Public Review):

    This manuscript does a great job of describing their phase-targeted closed-loop auditory stimulation protocols to alter slow wave oscillations in rodents and alter behavior on a motor task. They are able to stimulate an auditory stimulus within ~5 degrees of the target, both during the ascending and descending (termed up-phase and down-phase). They showed that stimulating during the up-phase increased delta and sigma while stimulating the down-phase decreased delta and sigma. They also showed that stimulating the up-phase improved performance on a motor task while stimulating the down-phase generally decreased performance. There is translational value to this approach as this has been previously used in human subjects- altering slow wave oscillation to improve memory consolidation (a hot topic in neuroscience). Applying this tool to rodent research in future studies may allow for bridging some of the putative mechanisms underlying memory consolidation (e.g., replay during NREM sleep) and behavioral changes observed with sleep (e.g., improved hippocampus-dependent memory). It's also nice to have a non-invasive way to manipulate sleep, particularly as we want to translate rodent research to clinical work.

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  3. Reviewer #2 (Public Review):

    Numerous recent studies with human subjects have suggested that periodic auditory stimuli, delivered at a particular phase with respect to NREM thalamocortical oscillations, have the capacity to promote memory consolidation during sleep. However, the underlying neurobiological mechanisms are less well understood. In order to characterize changes occurring within the thalamocortical circuitry during such closed-loop stimulation, the authors have carried out preliminary proof of principle work here in a rat model. In the model, closed-loop auditory stimulation (CLAS) is delivered across multiple days to rats, at different phases with respect to ongoing EEG rhythms. Effects of CLAS on EEG spectral power and performance on an multi-day motor learning paradigm have been assessed. The results largely replicate what has been found previously in CLAS studies with human subjects: upstate-targeted stimulation augments NREM thalamocortical oscillations. While upstate-targeted CLAS did not have any clear effect on motor learning, downstate-targeted CLAS appeared to reduce overall engagement with the motor task. While the present study does not provide additional information regarding neurobiological underpinnings of performance improvement driven by CLAS, the developed model has potential to do so in the future.

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