Structural plasticity of dendritic secretory compartments during LTP-induced synaptogenesis

  1. Yelena D Kulik
  2. Deborah J Watson
  3. Guan Cao
  4. Masaaki Kuwajima
  5. Kristen M Harris  Is a corresponding author
  1. The University of Texas at Austin, United States

Abstract

Long-term potentiation (LTP), an increase in synaptic efficacy following high-frequency stimulation, is widely considered a mechanism of learning. LTP involves local remodeling of dendritic spines and synapses. Smooth endoplasmic reticulum (SER) and endosomal compartments could provide local stores of membrane and proteins, bypassing the distant Golgi apparatus. To test this hypothesis, effects of LTP were compared to control stimulation in rat hippocampal area CA1 at postnatal day 15 (P15). By two hours, small spines lacking SER increased after LTP, whereas large spines did not change in frequency, size, or SER content. Total SER volume decreased after LTP consistent with transfer of membrane to the added spines. Shaft SER remained more abundant in spiny than aspiny dendritic regions, apparently supporting the added spines. Recycling endosomes were elevated specifically in small spines after LTP. These findings suggest local secretory trafficking contributes to LTP-induced synaptogenesis and primes the new spines for future plasticity.

Data availability

The relevant image series files and numerical data have been provided. In addition, the program Reconstruct, is freely available from synapses.clm.utexas.edu, and can be used to image and visualize the raw trace files. We have provided the raw images, Reconstruct trace files, and analytical tables in the public domain at Texas Data Repository: DOI: https://doi.org/10.18738/T8/5TX9YA.

The following data sets were generated

Article and author information

Author details

  1. Yelena D Kulik

    Center for Learning and Memory, Department of Neuroscience, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Deborah J Watson

    Center for Learning and Memory, Department of Neuroscience, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Guan Cao

    Center for Learning and Memory, Department of Neuroscience, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6211-5872
  4. Masaaki Kuwajima

    Center for Learning and Memory, Department of Neuroscience, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1478-3726
  5. Kristen M Harris

    Center for Learning and Memory, Department of Neuroscience, The University of Texas at Austin, Austin, United States
    For correspondence
    kmh2249@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1943-4744

Funding

National Institutes of Health (NS21184)

  • Kristen M Harris

National Institutes of Health (R01NS074644)

  • Kristen M Harris

National Institutes of Health (R01MH095980)

  • Kristen M Harris

National Institutes of Health (R01MH104319)

  • Kristen M Harris

National Science Foundation (NeuroNex 1707356)

  • Kristen M Harris

National Institutes of Health (F32 MH096459)

  • Deborah J Watson

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

Ethics

Animal experimentation: All procedures were approved by the University of Texas at Austin Institutional Animal Care and Use Committee and were in compliance with NIH requirements for humane animal care and use. Protocol number (06062801). All rats were of comparable features indicative of health at the time they were taken for experimentation.

Reviewing Editor

  1. Moritz Helmstaedter, Max Planck Institute for Brain Research, Germany

Publication history

  1. Received: February 24, 2019
  2. Accepted: August 20, 2019
  3. Accepted Manuscript published: August 21, 2019 (version 1)
  4. Version of Record published: September 5, 2019 (version 2)

Copyright

© 2019, Kulik 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. Yelena D Kulik
  2. Deborah J Watson
  3. Guan Cao
  4. Masaaki Kuwajima
  5. Kristen M Harris
(2019)
Structural plasticity of dendritic secretory compartments during LTP-induced synaptogenesis
eLife 8:e46356.
https://doi.org/10.7554/eLife.46356
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