The fate of hippocampal synapses depends on the sequence of plasticity-inducing events

  1. J Simon Wiegert
  2. Mauro Pulin
  3. Christine Elizabeth Gee
  4. Thomas G. Oertner  Is a corresponding author
  1. University Medical Center Hamburg-Eppendorf, Germany

Abstract

Synapses change their strength in response to specific activity patterns. This functional plasticity is assumed to be the brain's primary mechanism for information storage. We used optogenetic stimulation of rat hippocampal slice cultures to induce long-term potentiation (LTP), long-term depression (LTD), or both forms of plasticity in sequence. Two-photon imaging of spine calcium signals allowed us to identify stimulated synapses and to follow their fate for the next 7 days. We found that plasticity-inducing protocols affected the synapse's chance for survival: LTP increased synaptic stability, LTD destabilized synapses, and the effect of the last stimulation protocol was dominant over earlier stimulations. Interestingly, most potentiated synapses were resistant to depression-inducing protocols delivered 24 hours later. Our findings suggest that activity-dependent changes in the transmission strength of individual synapses are transient, but have long-lasting consequences for synaptic lifetime.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 2, 3, 4 and 5.

Article and author information

Author details

  1. J Simon Wiegert

    Institute for Synaptic Physiology, Center for Molecular Neurobiology Hamburg, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0893-9349
  2. Mauro Pulin

    Institute for Synaptic Physiology, Center for Molecular Neurobiology Hamburg, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6255-0276
  3. Christine Elizabeth Gee

    Institute for Synaptic Physiology, Center for Molecular Neurobiology Hamburg, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0345-3665
  4. Thomas G. Oertner

    Institute for Synaptic Physiology, Center for Molecular Neurobiology Hamburg, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
    For correspondence
    thomas.oertner@zmnh.uni-hamburg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2312-7528

Funding

Deutsche Forschungsgemeinschaft (FOR 2419)

  • Thomas G. Oertner

Deutsche Forschungsgemeinschaft (SFB 936 / B7)

  • Thomas G. Oertner

Deutsche Forschungsgemeinschaft (SPP 1665)

  • Thomas G. Oertner

European Commission (ERC-2016-StG 714762)

  • J Simon Wiegert

Deutsche Forschungsgemeinschaft (SPP 1926)

  • J Simon Wiegert

Deutsche Forschungsgemeinschaft (FOR 2419)

  • J Simon Wiegert

Deutsche Forschungsgemeinschaft (FOR 2419)

  • Christine Elizabeth Gee

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

Ethics

Animal experimentation: Animal procedures were in accordance with the guidelines of local authorities and Directive 2010/63/EU.

Reviewing Editor

  1. Julie A Kauer, Brown University, United States

Publication history

  1. Received: June 12, 2018
  2. Accepted: October 11, 2018
  3. Accepted Manuscript published: October 12, 2018 (version 1)
  4. Version of Record published: October 29, 2018 (version 2)

Copyright

© 2018, Wiegert 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. J Simon Wiegert
  2. Mauro Pulin
  3. Christine Elizabeth Gee
  4. Thomas G. Oertner
(2018)
The fate of hippocampal synapses depends on the sequence of plasticity-inducing events
eLife 7:e39151.
https://doi.org/10.7554/eLife.39151

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