Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits

  1. Mária Ashaber
  2. Yusuke Tomina
  3. Pegah Kassraian
  4. Eric A Bushong
  5. William B Kristan Jnr
  6. Mark H Ellisman
  7. Daniel A Wagenaar  Is a corresponding author
  1. California Institute of Technology, United States
  2. Keio University, Japan
  3. University of California, San Diego, United States

Abstract

Dorsal Excitor motor neuron DE-3 in the medicinal leech plays three very different dynamical roles in three different behaviors. Without rewiring its anatomical connectivity, how can a motor neuron dynamically switch roles to play appropriate roles in various behaviors? We previously used voltage-sensitive dye imaging to record from DE-3 and most other neurons in the leech segmental ganglion during (fictive) swimming, crawling, and local-bend escape (Tomina and Wagenaar, 2017). Here, we repeated that experiment, then re-imaged the same ganglion using serial blockface electron microscopy and traced DE-3's processes. Further, we traced back the processes of DE-3's presynaptic partners to their respective somata. This allowed us to analyze the relationship between circuit anatomy and the activity patterns it sustains. We found that input synapses important for all of the behaviors were widely distributed over DE-3's branches, yet that functional clusters were different during (fictive) swimming vs. crawling.

Data availability

The easiest way to access the raw electrophysiology and voltage-dye data as well as the tracing results used in this paper is through a series of Python modules that we made available at https://github.com/wagenadl/leechem-public. Included in the package is a file called "demo.py" that demonstrates the use of the modules. Table 4 lists the available VSD trials.The aligned EM volume may be accessed through the Neuroglancer instance at https://leechem.caltech.edu or by pointing SBEMViewer to https://leechem.caltech.edu/emdata.The code used for alignment is available at https://github.com/wagenadl/sbemalign. Our visualization tools SBEMViewer and GVox are at https://github.com/wagenadl/sbemviewer and https://github.com/wagenadl/gvox.

The following data sets were generated

Article and author information

Author details

  1. Mária Ashaber

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5586-9585
  2. Yusuke Tomina

    Faculty of Science and Technology, Keio University, Yokohama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Pegah Kassraian

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Eric A Bushong

    Center for Research in Biological Systems, National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6195-2433
  5. William B Kristan Jnr

    Division of Biological Sciences,, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Mark H Ellisman

    National Center for Microscopy and Imaging Research,, University of California, San Diego, Le Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Daniel A Wagenaar

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    For correspondence
    daw@caltech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6222-761X

Funding

National Institute of Neurological Disorders and Stroke (R01-NS094403)

  • William B Kristan Jnr
  • Mark H Ellisman
  • Daniel A Wagenaar

National Institute of General Medical Sciences (P41-GM103412)

  • Mark H Ellisman

Japan Society for the Promotion of Science (201800526)

  • Yusuke Tomina

Japan Society for the Promotion of Science (19K16191)

  • Yusuke Tomina

Swiss National Science Foundation (P2EZP3-181896)

  • Pegah Kassraian

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

Reviewing Editor

  1. Vatsala Thirumalai, National Centre for Biological Sciences, India

Publication history

  1. Received: August 7, 2020
  2. Accepted: February 12, 2021
  3. Accepted Manuscript published: February 15, 2021 (version 1)
  4. Version of Record published: March 12, 2021 (version 2)
  5. Version of Record updated: March 22, 2021 (version 3)

Copyright

© 2021, Ashaber 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. Mária Ashaber
  2. Yusuke Tomina
  3. Pegah Kassraian
  4. Eric A Bushong
  5. William B Kristan Jnr
  6. Mark H Ellisman
  7. Daniel A Wagenaar
(2021)
Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits
eLife 10:e61881.
https://doi.org/10.7554/eLife.61881

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