Mitochondrial support of persistent presynaptic vesicle mobilization with age-dependent synaptic growth after LTP

  1. Heather L Smith
  2. Jennifer N Bourne
  3. Guan Cao
  4. Michael A Chirillo
  5. Linnaea E Ostroff
  6. Deborah J Watson
  7. Kristen M Harris  Is a corresponding author
  1. University of Texas at Austin, United States
  2. University of Colorado Denver, United States
  3. New York University, United States
  4. QPS, LLC, United States
  5. The University of Texas at Austin, United States

Abstract

Mitochondria support synaptic transmission through production of ATP, sequestration of calcium, synthesis of glutamate, and other vital functions. Surprisingly, less than 50% of hippocampal CA1 presynaptic boutons contain mitochondria, raising the question of whether synapses without mitochondria can sustain changes in efficacy. To address this question, we analyzed synapses from postnatal day 15 (P15) and adult rat hippocampus that had undergone theta-burst stimulation to produce long-term potentiation (TBS-LTP) and compared them to control or no stimulation. At 30 and 120 minutes after TBS-LTP, vesicles were decreased only in presynaptic boutons that contained mitochondria at P15, and vesicle decrement was greatest in adult boutons containing mitochondria. Presynaptic mitochondrial cristae were widened, suggesting a sustained energy demand. Thus, mitochondrial proximity reflected enhanced vesicle mobilization well after potentiation reached asymptote, in parallel with the apparently silent addition of new dendritic spines at P15 or the silent enlargement of synapses in adults.

Article and author information

Author details

  1. Heather L Smith

    Department of Neuroscience, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jennifer N Bourne

    Department of Cell and Developmental Biology, University of Colorado Denver, Denver, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Guan Cao

    Department of Neuroscience, 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. Michael A Chirillo

    Department of Neuroscience, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Linnaea E Ostroff

    Center for Neural Science, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Deborah J Watson

    QPS, LLC, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Kristen M Harris

    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 (NS201184)

  • Kristen M Harris

Texas Emerging Technology Fund

  • Kristen M Harris

National Institutes of Health (MH095980)

  • Kristen M Harris

National Institutes of Health (NS074644)

  • Kristen M Harris

National Institutes of Health (MH096459)

  • Deborah J Watson

Brain Research Foundation

  • Kristen M Harris

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

Reviewing Editor

  1. Michael Häusser, University College London, United Kingdom

Publication history

  1. Received: February 22, 2016
  2. Accepted: December 16, 2016
  3. Accepted Manuscript published: December 19, 2016 (version 1)
  4. Version of Record published: January 13, 2017 (version 2)

Copyright

© 2016, Smith 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. Heather L Smith
  2. Jennifer N Bourne
  3. Guan Cao
  4. Michael A Chirillo
  5. Linnaea E Ostroff
  6. Deborah J Watson
  7. Kristen M Harris
(2016)
Mitochondrial support of persistent presynaptic vesicle mobilization with age-dependent synaptic growth after LTP
eLife 5:e15275.
https://doi.org/10.7554/eLife.15275

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