Thalamic reticular control of local sleep in mouse sensory cortex

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Abstract

Sleep affects brain activity globally, but many cortical sleep waves are spatially confined. Local rhythms serve cortical area-specific sleep needs and functions, however, mechanisms controlling locality are unclear. We identify the thalamic reticular nucleus (TRN) as a source for local, sensory-cortex-specific non-rapid-eye-movement sleep (NREMS) in mouse. Neurons in optogenetically identified sensory TRN sectors showed stronger repetitive burst discharge compared to non-sensory TRN cells due to higher activity of the low-threshold Ca²⁺ channel Ca_V3.3. Major NREMS rhythms in sensory but not non-sensory cortical areas were regulated in a Ca_V3.3-dependent manner. In particular, NREMS in somatosensory cortex was enriched in fast spindles, but switched to delta wave-dominated sleep when Ca_V3.3 channels were genetically eliminated or somatosensory TRN cells chemogenetically hyperpolarized. Our data indicate a previously unrecognized heterogeneity in a powerful forebrain oscillator that contributes to sensory-cortex-specific and dually regulated NREMS, enabling local sleep regulation according to use- and experience-dependence.

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All data generated or analysed during this study are included in the manuscript and supporting files.

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Laura MJ Fernandez

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-7942-3369
Gil Vantomme

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-7441-0737
Alejandro Osorio-Forero

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4341-4206
Romain Cardis

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.
Elidie Béard

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.
Anita Lüthi

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland

For correspondence
anita.luthi@unil.ch

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4954-4143

Funding

Swiss National Science Foundation (31003A_166318)

Laura MJ Fernandez
Gil Vantomme
Alejandro Osorio-Forero
Romain Cardis
Elidie Béard
Anita Lüthi

Etat de Vaud

Laura MJ Fernandez
Gil Vantomme
Alejandro Osorio-Forero
Romain Cardis
Elidie Béard
Anita Lüthi

FBM Poste de soutien à un congé parental

Laura MJ Fernandez
Elidie Béard

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

Ethics

Animal experimentation: All experimental procedures complied with the Swiss National Institutional Guidelines on Animal Experimentation (Swiss Federal Act on Animal Protection, LPA 2005) and were approved by the Swiss Cantonal Veterinary Office Committee for Animal Experimentation. All experiments were carried out in accordance with approved protocols by the Swiss Cantonal Veterinary Office Committee for in vitro experimentation on mice (reference VD2062) and for in vivo experimentation on mice (references VD2387 and VD2401).

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.