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.

Reviewing Editor

  1. Masako Tamaki

Publication history

  1. Preprint posted: March 31, 2021 (view preprint)
  2. Received: May 24, 2021
  3. Accepted: August 15, 2022
  4. Accepted Manuscript published: August 16, 2022 (version 1)
  5. Version of Record published: August 26, 2022 (version 2)

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

  • 703
    Page views
  • 220
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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

Further reading

    1. Neuroscience
    Benjamin D Pedigo, Mike Powell ... Joshua T Vogelstein
    Research Article

    Comparing connectomes can help explain how neural connectivity is related to genetics, disease, development, learning, and behavior. However, making statistical inferences about the significance and nature of differences between two networks is an open problem, and such analysis has not been extensively applied to nanoscale connectomes. Here, we investigate this problem via a case study on the bilateral symmetry of a larval Drosophila brain connectome. We translate notions of'bilateral symmetry' to generative models of the network structure of the left and right hemispheres, allowing us to test and refine our understanding of symmetry. We find significant differences in connection probabilities both across the entire left and right networks and between specific cell types. By rescaling connection probabilities or removing certain edges based on weight, we also present adjusted definitions of bilateral symmetry exhibited by this connectome. This work shows how statistical inferences from networks can inform the study of connectomes, facilitating future comparisons of neural structures.

    1. Neuroscience
    Sinisa Pajevic, Dietmar Plenz ... R Douglas Fields
    Research Article

    Temporal synchrony of signals arriving from different neurons or brain regions is essential for proper neural processing. Nevertheless, it is not well understood how such synchrony is achieved and maintained in a complex network of time-delayed neural interactions. Myelin plasticity, accomplished by oligodendrocytes (OLs), has been suggested as an efficient mechanism for controlling timing in brain communications through adaptive changes of axonal conduction velocity and consequently conduction time delays, or latencies; however, local rules and feedback mechanisms that OLs use to achieve synchronization are not known. We propose a mathematical model of oligodendrocyte-mediated myelin plasticity (OMP) in which OLs play an active role in providing such feedback. This is achieved without using arrival times at the synapse or modulatory signaling from astrocytes; instead, it relies on the presence of global and transient OL responses to local action potentials in the axons they myelinate. While inspired by OL morphology, we provide the theoretical underpinnings that motivated the model and explore its performance for a wide range of its parameters. Our results indicate that when the characteristic time of OL’s transient intracellular responses to neural spikes is between 10 and 40 ms and the firing rates in individual axons are relatively low (⪅ 10 Hz), the OMP model efficiently synchronizes correlated and time-locked signals while latencies in axons carrying independent signals are unaffected. This suggests a novel form of selective synchronization in the CNS in which oligodendrocytes play an active role by modulating the conduction delays of correlated spike trains as they traverse to their targets.