Neuronal morphologies built for reliable physiology in a rhythmic motor circuit

  1. Adriane G Otopalik  Is a corresponding author
  2. Jason Pipkin
  3. Eve Marder  Is a corresponding author
  1. Columbia University, United States
  2. Brandeis University, United States

Abstract

It is often assumed that highly-branched neuronal structures perform compartmentalized computations. Instead, the Gastric Mill (GM) neuron in the crustacean stomatogastric ganglion (STG) operates like a single electrotonic compartment, despite having thousands of branch points and total cable length >10 mm (Otopalik et al., 2017a, b). We now show: 1) that compact electrotonic architecture is generalizable to other STG neuron types, 2) these neurons present direction-insensitive, linear voltage integration, suggesting they pool synaptic inputs across their neuronal structures. 3) Simulations of 720 cable models spanning a broad range of geometries and passive properties show that compact electrotonus, linear integration, and directional insensitivity in STG neurons arise from their neurite geometries (diameters tapering from 10-20 µm to < 2 µm at their terminal tips). A broad parameter search reveals multiple morphological and biophysical solutions for achieving different degrees of passive electrotonic decrement and computational strategies in the absence of active properties.

Data availability

All computational scripts used for: analysis, visualization, and model simulations, will be promptly posted on the Marder Lab GitHub site (https://github.com/marderlab) upon publication, where it will be freely available to the public. These tools are currently available on A. Otopalik's GitHub site (https://github.com/otopalik/Otopalik-Pipkin-Marder-2019). All source data are publicly available on Dryad (https://dx.doi.org/10.5061/dryad.48pt6jd).

The following data sets were generated

Article and author information

Author details

  1. Adriane G Otopalik

    Department of Biological Sciences, Columbia University, New York, United States
    For correspondence
    ao2656@columbia.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3224-6502
  2. Jason Pipkin

    Volen Center, Brandeis University, Waltham, United States
    Competing interests
    No competing interests declared.
  3. Eve Marder

    Volen Center, Brandeis University, Waltham, United States
    For correspondence
    marder@brandeis.edu
    Competing interests
    Eve Marder, Deputy Editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9632-5448

Funding

National Institute of Neurological Disorders and Stroke (F31NS092126)

  • Adriane G Otopalik

National Institute of Neurological Disorders and Stroke (R35NS097343)

  • Eve Marder

Grass Foundation

  • Adriane G Otopalik

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

Reviewing Editor

  1. Inna Slutsky, Tel Aviv University, Israel

Publication history

  1. Received: September 7, 2018
  2. Accepted: January 12, 2019
  3. Accepted Manuscript published: January 18, 2019 (version 1)
  4. Version of Record published: January 28, 2019 (version 2)

Copyright

© 2019, Otopalik 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. Adriane G Otopalik
  2. Jason Pipkin
  3. Eve Marder
(2019)
Neuronal morphologies built for reliable physiology in a rhythmic motor circuit
eLife 8:e41728.
https://doi.org/10.7554/eLife.41728
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