1. Neuroscience
Download icon

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
Research Advance
  • Cited 0
  • Views 1,545
  • Annotations
Cite this article as: eLife 2021;10:e61881 doi: 10.7554/eLife.61881

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.

Metrics

  • 1,545
    Page views
  • 196
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Neuroscience
    Charlotte Vanacker et al.
    Research Article Updated

    GnRH neurons are the final central neural output regulating fertility. Kisspeptin neurons in the hypothalamic arcuate nucleus (KNDy neurons) are considered the main regulator of GnRH output. GnRH and KNDy neurons are surrounded by astrocytes, which can modulate neuronal activity and communicate over distances. Prostaglandin E2 (PGE2), synthesized primarily by astrocytes, increases GnRH neuron activity and downstream pituitary release of luteinizing hormone (LH). We hypothesized that glial fibrillary acidic protein (GFAP)-expressing astrocytes play a role in regulating GnRH and/or KNDy neuron activity and LH release. We used adeno-associated viruses to target designer receptors exclusively activated by designer drugs (DREADDs) to GFAP-expressing cells to activate Gq- or Gi-mediated signaling. Activating Gq signaling in the preoptic area, near GnRH neurons, but not in the arcuate, increases LH release in vivo and GnRH firing in vitro via a mechanism in part dependent upon PGE2. These data suggest that astrocytes can activate GnRH/LH release in a manner independent of KNDy neurons.

    1. Neuroscience
    Sahana Sitaraman et al.
    Research Article

    Gap junctions between neurons serve as electrical synapses, in addition to conducting metabolites and signaling molecules. During development, early-appearing gap junctions are thought to prefigure chemical synapses, which appear much later. We present evidence for this idea at a central, glutamatergic synapse and provide some mechanistic insights. Loss or reduction in the levels of the gap junction protein Gjd2b decreased the frequency of glutamatergic miniature excitatory postsynaptic currents (mEPSCs) in cerebellar Purkinje neurons (PNs) in larval zebrafish. Ultrastructural analysis in the molecular layer showed decreased synapse density. Further, mEPSCs had faster kinetics and larger amplitudes in mutant PNs, consistent with their stunted dendritic arbors. Time-lapse microscopy in wild type and mutant PNs reveals that Gjd2b puncta promote the elongation of branches and that CaMKII may be a critical mediator of this process. These results demonstrate that Gjd2b-mediated gap junctions regulate glutamatergic synapse formation and dendritic elaboration in PNs.