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

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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.

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

Article and author information

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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.
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.
Carola Gregor

Department of NanoBiophotonics, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany

Competing interests
The authors declare that no competing interests exist.
Fred Wolf

Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany

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

"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.

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.