Stability of neocortical synapses across sleep and wake states during the critical period in rats

Abstract
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Abstract

Sleep is important for brain plasticity, but its exact function remains mysterious. An influential but controversial idea is that a crucial function of sleep is to drive widespread downscaling of excitatory synaptic strengths. Here we used real-time sleep classification, ex vivo measurements of postsynaptic strength, and in vivo optogenetic monitoring of thalamocortical synaptic efficacy to ask whether sleep and wake states can constitutively drive changes in synaptic strength within the neocortex of juvenile rats. We found that miniature EPSC amplitudes onto L4 and L2/3 pyramidal neurons were stable across sleep and wake dense epochs in both primary visual (V1) and prefrontal cortex (PFC). Further, chronic monitoring of thalamocortical synaptic efficacy in V1 of freely behaving animals revealed stable responses across even prolonged periods of natural sleep and wake. Together these data demonstrate that sleep does not drive widespread downscaling of synaptic strengths during the highly plastic critical period in juvenile animals. Whether this remarkable stability across sleep and wake generalizes to the fully mature nervous system remains to be seen.

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Processed datasets and all figure data have been uploaded to Figshare (https://figshare.com/projects/Cary_et_al_2021_Elife_Submission/95867)

Article and author information

Author details

Brian A Cary

Department of Biology, Brandeis University, Waltham, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-1759-164X
Gina G Turrigiano

Department of Biology, Brandeis University, Waltham, United States

For correspondence
turrigiano@brandeis.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4476-4059

Funding

National Eye Institute (EY025613)

Gina G Turrigiano

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All animals were housed, cared for, surgerized, and sacrificed in accordance with Brandeis IBC and IACAUC protocols (#15005 and #18002). All surgery was performed under isoflurane anesthesia. All surgerized animals received two days of post-operative care including daily injection of Meloxicam and Penicillin to reduce discomfort/inflammation and risk of infection. Rats were always housed and recorded with at least one littermate.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.