Mutual interaction between visual homeostatic plasticity and sleep in adult humans

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Abstract

Sleep and plasticity are highly interrelated, as sleep slow oscillations and sleep spindles are associated with consolidation of Hebbian-based processes. However, in adult humans, visual cortical plasticity is mainly sustained by homeostatic mechanisms, for which the role of sleep is still largely unknown. Here we demonstrate that non-REM sleep stabilizes homeostatic plasticity of ocular dominance induced in adult humans by short-term monocular deprivation: the counter-intuitive and otherwise transient boost of the deprived eye was preserved at the morning awakening (>6 hours after deprivation). Subjects exhibiting a stronger boost of the deprived eye after sleep had increased sleep spindle density in frontopolar electrodes, suggesting the involvement of distributed processes. Crucially, the individual susceptibility to visual homeostatic plasticity soon after deprivation correlated with the changes in sleep slow oscillations and spindle power in occipital sites, consistent with a modulation in early occipital visual cortex.

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Danilo Menicucci

Department of Surgical, Medical and Molecular Pathology and Critical Care Medicine, University of Pisa, Pisa, Italy

For correspondence
danilo.menicucci@unipi.it

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5521-4108
Claudia Lunghi

Département d'études Cognitives, École Normale Supérieure, UMR 8248 CNRS, Paris, France

Competing interests
The authors declare that no competing interests exist.
Andrea Zaccaro

Department of Surgical, Medical and Molecular Pathology and Critical Care Medicine, University of Pisa, Pisa, Italy

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-0409-7132
Maria Concetta Morrone

Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-1025-0316
Angelo Gemignani

Department of Surgical, Medical and Molecular and Critical Area Pathology, University of Pisa, Pisa, Italy

Competing interests
The authors declare that no competing interests exist.

Funding

FP7 (338866 - Ecsplain)

Maria Concetta Morrone

ERC (948366 - HOPLA)

Claudia Lunghi

FP7 (832813 - GenPercept)

Maria Concetta Morrone

MIUR and the French National Research Agency (ANR: AAPG 2019 JCJC,grant agreement ANR-19-CE28-0008,PlaStiC,and FrontCog grant ANR-17-EURE-0017)

Claudia Lunghi

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

Ethics

Human subjects: All eligible volunteers signed an informed written consent. The study was approved by the Local Ethical Committee (Comitato Etico Pediatrico Regionale-Azienda Ospedaliero-Universitaria Meyer-Firenze), under the protocol "Plasticità del sistema visivo" (3/2011) and complied the tenets of the Declaration of Helsinki.

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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.