Environmental enrichment enhances patterning and remodeling of synaptic nanoarchitecture as revealed by STED nanoscopy

  1. Waja Wegner
  2. Heinz Steffens
  3. Carola Gregor
  4. Fred Wolf
  5. Katrin I Willig  Is a corresponding author
  1. University Medical Center Göttingen, Germany
  2. Max Planck Institute for Biophysical Chemistry, Germany
  3. Max Planck Institute for Dynamics and Self-Organization, Germany

Abstract

Synaptic plasticity underlies long-lasting structural and functional changes to brain circuitry and its experience-dependent remodeling can be fundamentally enhanced by environmental enrichment. It is however unknown, whether and how the environmental enrichment alters the morphology and dynamics of individual synapses. Here, we present a virtually crosstalk-free two-color in vivo STED microscope to simultaneously superresolve the dynamics of endogenous PSD95 of the post-synaptic density and spine geometry in the mouse cortex. In general, the spine head geometry and PSD95 assemblies were highly dynamic, their changes depended linearly on their original size but correlated only mildly. With environmental enrichment, the size distributions of PSD95 and spine head sizes were sharper than in controls, indicating that synaptic strength is set more uniformly. The topography of the PSD95 nanoorganization was more dynamic after environmental enrichment; changes in size were smaller but more correlated than in mice housed in standard cages. Thus, two-color in vivo time-lapse imaging of synaptic nanoorganization uncovers a unique synaptic nanoplasticity associated with the enhanced learning capabilities under environmental enrichment.

Data availability

Source data files of all analysed data are included in the submission.

Article and author information

Author details

  1. Waja Wegner

    Center for Nanoscale Microscopy and Molecular Physiology of the Brain, University Medical Center Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Heinz Steffens

    Center for Nanoscale Microscopy and Molecular Physiology of the Brain, University Medical Center Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Carola Gregor

    Department of NanoBiophotonics, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Fred Wolf

    Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Katrin I Willig

    Center for Nanoscale Microscopy and Molecular Physiology of the Brain, University Medical Center Göttingen, Göttingen, Germany
    For correspondence
    kwillig@em.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1860-334X

Funding

Deutsche Forschungsgemeinschaft (EXC171)

  • Waja Wegner
  • Heinz Steffens
  • Katrin I Willig

Deutsche Forschungsgemeinschaft (EXC 2067/1- 390729940)

  • Carola Gregor
  • Katrin I Willig

Max Planck Institute for Multidisciplinary Sciences (Open Access Funding)

  • Waja Wegner
  • Heinz Steffens
  • Carola Gregor
  • Katrin I Willig

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

Ethics

Animal experimentation: Experiments were performed according to the guidelines of the national law regarding animal protection procedures and were approved by the responsible authorities, the Niedersächsisches Landesamt für Verbraucherschutz (LAVES, identification number 33.9-42502-04-14/1463). All surgery and imaging was performed under anesthesia, and all efforts were made to minimize animal suffering and the number of animals used.

Reviewing Editor

  1. Yukiko Goda, RIKEN, Japan

Publication history

  1. Preprint posted: October 23, 2020 (view preprint)
  2. Received: September 3, 2021
  3. Accepted: February 22, 2022
  4. Accepted Manuscript published: February 23, 2022 (version 1)
  5. Version of Record published: March 8, 2022 (version 2)

Copyright

© 2022, Wegner 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.

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  1. Waja Wegner
  2. Heinz Steffens
  3. Carola Gregor
  4. Fred Wolf
  5. Katrin I Willig
(2022)
Environmental enrichment enhances patterning and remodeling of synaptic nanoarchitecture as revealed by STED nanoscopy
eLife 11:e73603.
https://doi.org/10.7554/eLife.73603

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