Similar synapse elimination motifs at successive relays in the same efferent pathway during development in mice

  1. Shu-Hsien Sheu
  2. Juan Carlos Tapia  Is a corresponding author
  3. Shlomo Tsuriel
  4. Jeff W Lichtman  Is a corresponding author
  1. Boston Children's Hospital, United States
  2. Harvard University, United States

Abstract

In many parts of the nervous system, signals pass across multiple synaptic relays on their way to a destination, but little is known about how these relays form and the function they serve. To get some insight we ask how the connectivity patterns are organized at two successive synaptic relays in a simple, cholinergic efferent pathway. We found that the organization at successive relays in the parasympathetic nervous system strongly resemble each other despite the different embryological origin and physiological properties of the pre- and postsynaptic cells. Additionally, we found a similar developmental synaptic pruning and elaboration strategy is used at both sites to generate their adult organizations. The striking parallels in adult innervation and developmental mechanisms at the relays argue that a general strategy is in operation. We discuss why from a functional standpoint this structural organization may amplify central signals while at the same time maintaining positional targeting.

Article and author information

Author details

  1. Shu-Hsien Sheu

    Department of Pathology and Cardiology, Boston Children's Hospital, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0758-4654
  2. Juan Carlos Tapia

    Center for Brain Science, Harvard University, Cambridge, United States
    For correspondence
    juantapia@utalca.cl
    Competing interests
    The authors declare that no competing interests exist.
  3. Shlomo Tsuriel

    Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jeff W Lichtman

    Center for Brain Science, Harvard University, Cambridge, United States
    For correspondence
    jeff@mcb.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0208-3212

Funding

National Institute of Neurological Disorders and Stroke (5R01NS020364-28)

  • Shu-Hsien Sheu
  • Juan Carlos Tapia
  • Shlomo Tsuriel
  • Jeff W Lichtman

Gatsby Charitable Foundation (FONDECYT #1160888)

  • Shu-Hsien Sheu
  • Juan Carlos Tapia
  • Shlomo Tsuriel
  • Jeff W Lichtman

National Institute of Mental Health

  • Shu-Hsien Sheu
  • Juan Carlos Tapia
  • Shlomo Tsuriel
  • Jeff W Lichtman

Conte Center, Harvard University (1P50MH094271-01)

  • Shu-Hsien Sheu
  • Juan Carlos Tapia
  • Shlomo Tsuriel
  • Jeff W Lichtman

National Heart, Lung, and Blood Institute (5T32HL110852-03)

  • Shu-Hsien Sheu

Fondo Nacional de Desarrollo Científico y Tecnológico (1160888)

  • Juan Carlos Tapia

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional Animal Care and Use Committee (IACUC) protocol of Harvard University (AEP # 24-08) and Columbia University (AAAF4659 and AAAA9658).

Reviewing Editor

  1. Moses V Chao, New York University Langone Medical Center, United States

Publication history

  1. Received: November 12, 2016
  2. Accepted: February 1, 2017
  3. Accepted Manuscript published: February 3, 2017 (version 1)
  4. Version of Record published: February 17, 2017 (version 2)

Copyright

© 2017, Sheu 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. Shu-Hsien Sheu
  2. Juan Carlos Tapia
  3. Shlomo Tsuriel
  4. Jeff W Lichtman
(2017)
Similar synapse elimination motifs at successive relays in the same efferent pathway during development in mice
eLife 6:e23193.
https://doi.org/10.7554/eLife.23193

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