Neuronal morphologies built for reliable physiology in a rhythmic motor circuit

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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

(2019) Data from: Neuronal morphologies built for reliable physiology in a rhythmic motor circuit
Dryad Digital Repository, doi:10.5061/dryad.48pt6jd.

http://dx.doi.org/10.5061/dryad.48pt6jd

Article and author information

Author details

Adriane G Otopalik

Department of Biological Sciences, Columbia University, New York, United States

For correspondence
ao2656@columbia.edu

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-3224-6502
Jason Pipkin

Volen Center, Brandeis University, Waltham, United States

Competing interests
No competing interests declared.
Eve Marder

Volen Center, Brandeis University, Waltham, United States

For correspondence
marder@brandeis.edu

Competing interests
Eve Marder, Deputy Editor, eLife.

"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.

Copyright

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.