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Characterization of developmental and molecular factors underlying release heterogeneity at Drosophila synapses

  1. Yulia Akbergenova  Is a corresponding author
  2. Karen L Cunningham
  3. Yao V Zhang
  4. Shirley Weiss
  5. J Troy Littleton  Is a corresponding author
  1. Massachusetts Institute of Technology, United States
Research Article
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Cite as: eLife 2018;7:e38268 doi: 10.7554/eLife.38268

Abstract

Neurons communicate through neurotransmitter release at specialized synaptic regions known as active zones (AZs). Using biosensors to visualize single synaptic vesicle fusion events at Drosophila neuromuscular junctions, we analyzed the developmental and molecular determinants of release probability (Pr) for a defined connection with ~300 AZs. Pr was heterogeneous but represented a stable feature of each AZ. Prremained stable during high frequency stimulation and retained heterogeneity in mutants lacking the Ca2+ sensor Synaptotagmin 1. Pr correlated with both presynaptic Ca2+ channel abundance and Ca2+ influx at individual release sites. Pr heterogeneity also correlated with glutamate receptor abundance, with high Pr connections developing receptor subtype segregation. Intravital imaging throughout development revealed that AZs acquire high Pr during a multi-day maturation period, with Pr heterogeneity largely reflecting AZ age. The rate of synapse maturation was activity-dependent, as both increases and decreases in neuronal activity modulated glutamate receptor field size and segregation.

Article and author information

Author details

  1. Yulia Akbergenova

    The Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    yulakb@mit.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Karen L Cunningham

    The Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Yao V Zhang

    The Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Shirley Weiss

    The Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. J Troy Littleton

    The Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    troy@mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0001-5576-2887

Funding

National Institutes of Health (MH104536)

  • J Troy Littleton

National Institutes of Health (T32GM007287)

  • Karen L Cunningham

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

Reviewing Editor

  1. Hugo J Bellen, Baylor College of Medicine, United States

Publication history

  1. Received: May 11, 2018
  2. Accepted: June 30, 2018
  3. Accepted Manuscript published: July 10, 2018 (version 1)
  4. Version of Record published: August 3, 2018 (version 2)

Copyright

© 2018, Akbergenova 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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