Mutual interaction between visual homeostatic plasticity and sleep in adult humans

  1. Danilo Menicucci  Is a corresponding author
  2. Claudia Lunghi
  3. Andrea Zaccaro
  4. Maria Concetta Morrone
  5. Angelo Gemignani
  1. University of Pisa, Italy
  2. École Normale Supérieure, UMR 8248 CNRS, France

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.

Data availability

All data included in manuscript and supporting files

Article and author information

Author details

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5521-4108
  2. Claudia Lunghi

    Département d'études Cognitives, École Normale Supérieure, UMR 8248 CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0409-7132
  4. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1025-0316
  5. 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.

Copyright

© 2022, Menicucci et al.

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.

Metrics

  • 1,100
    views
  • 286
    downloads
  • 7
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Danilo Menicucci
  2. Claudia Lunghi
  3. Andrea Zaccaro
  4. Maria Concetta Morrone
  5. Angelo Gemignani
(2022)
Mutual interaction between visual homeostatic plasticity and sleep in adult humans
eLife 11:e70633.
https://doi.org/10.7554/eLife.70633

Share this article

https://doi.org/10.7554/eLife.70633

Further reading

    1. Neuroscience
    Zhujun Shao, Mengya Zhang, Qing Yu
    Research Article

    When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.

    1. Neuroscience
    Franziska Auer, Katherine Nardone ... David Schoppik
    Research Article

    Cerebellar dysfunction leads to postural instability. Recent work in freely moving rodents has transformed investigations of cerebellar contributions to posture. However, the combined complexity of terrestrial locomotion and the rodent cerebellum motivate new approaches to perturb cerebellar function in simpler vertebrates. Here, we adapted a validated chemogenetic tool (TRPV1/capsaicin) to describe the role of Purkinje cells — the output neurons of the cerebellar cortex — as larval zebrafish swam freely in depth. We achieved both bidirectional control (activation and ablation) of Purkinje cells while performing quantitative high-throughput assessment of posture and locomotion. Activation modified postural control in the pitch (nose-up/nose-down) axis. Similarly, ablations disrupted pitch-axis posture and fin-body coordination responsible for climbs. Postural disruption was more widespread in older larvae, offering a window into emergent roles for the developing cerebellum in the control of posture. Finally, we found that activity in Purkinje cells could individually and collectively encode tilt direction, a key feature of postural control neurons. Our findings delineate an expected role for the cerebellum in postural control and vestibular sensation in larval zebrafish, establishing the validity of TRPV1/capsaicin-mediated perturbations in a simple, genetically tractable vertebrate. Moreover, by comparing the contributions of Purkinje cell ablations to posture in time, we uncover signatures of emerging cerebellar control of posture across early development. This work takes a major step towards understanding an ancestral role of the cerebellum in regulating postural maturation.