When complex neuronal structures may not matter

  1. Adriane G Otopalik  Is a corresponding author
  2. Alexander C Sutton
  3. Matthew Ryan Banghart
  4. Eve Marder  Is a corresponding author
  1. Brandeis University, United States
  2. Harvard Medical School, United States

Abstract

Much work has explored animal-to-animal variability and compensation in ion channel expression. Yet, little is known regarding the physiological consequences of morphological variability. We quantify animal-to-animal variability in cable lengths (CV = 0.4) and branching patterns in the Gastric Mill (GM) neuron, an identified neuron type with highly-conserved physiological properties in the crustacean stomatogastric ganglion (STG) of Cancer borealis. We examined passive GM electrotonic structure by measuring the amplitudes and apparent reversal potentials (Erevs) of inhibitory responses evoked with focal glutamate photo-uncaging in the presence of TTX. Apparent Erevs were relatively invariant across sites (mean CV + SD =0.04 + 0.01; 7-20 sites in each of 10 neurons), which ranged between 100-800 µm from the somatic recording site. Thus, GM neurons are remarkably electrotonically compact (estimated λ > 1.5 mm). Electrotonically compact structures, in consort with graded transmission, provide an elegant solution to observed morphological variability in the STG.

Article and author information

Author details

  1. Adriane G Otopalik

    Volen Center, Brandeis University, Waltham, United States
    For correspondence
    aotopali@brandeis.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3224-6502
  2. Alexander C Sutton

    Volen Center, Brandeis University, Waltham, United States
    Competing interests
    No competing interests declared.
  3. Matthew Ryan Banghart

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    No competing interests declared.
  4. Eve Marder

    Volen Center, Brandeis University, Waltham, United States
    For correspondence
    marder@brandeis.edu
    Competing interests
    Eve Marder, Senior 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 (R37NS017813)

  • Eve Marder

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

Copyright

© 2017, 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.

Metrics

  • 3,679
    views
  • 595
    downloads
  • 39
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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)

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

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

  1. Adriane G Otopalik
  2. Alexander C Sutton
  3. Matthew Ryan Banghart
  4. Eve Marder
(2017)
When complex neuronal structures may not matter
eLife 6:e23508.
https://doi.org/10.7554/eLife.23508

Share this article

https://doi.org/10.7554/eLife.23508

Further reading

    1. Neuroscience
    Adriane G Otopalik, Marie L Goeritz ... Eve Marder
    Research Article Updated

    Neuronal physiology depends on a neuron’s ion channel composition and unique morphology. Variable ion channel compositions can produce similar neuronal physiologies across animals. Less is known regarding the morphological precision required to produce reliable neuronal physiology. Theoretical studies suggest that moraphology is tightly tuned to minimize wiring and conduction delay of synaptic events. We utilize high-resolution confocal microscopy and custom computational tools to characterize the morphologies of four neuron types in the stomatogastric ganglion (STG) of the crab Cancer borealis. Macroscopic branching patterns and fine cable properties are variable within and across neuron types. We compare these neuronal structures to synthetic minimal spanning neurite trees constrained by a wiring cost equation and find that STG neurons do not adhere to prevailing hypotheses regarding wiring optimization principles. In this highly modulated and oscillating circuit, neuronal structures appear to be governed by a space-filling mechanism that outweighs the cost of inefficient wiring.

    1. Cell Biology
    2. Neuroscience
    Victor C Wong, Patrick R Houlihan ... Erin K O'Shea
    Research Article

    AMPA-type receptors (AMPARs) are rapidly inserted into synapses undergoing plasticity to increase synaptic transmission, but it is not fully understood if and how AMPAR-containing vesicles are selectively trafficked to these synapses. Here, we developed a strategy to label AMPAR GluA1 subunits expressed from their endogenous loci in cultured rat hippocampal neurons and characterized the motion of GluA1-containing vesicles using single-particle tracking and mathematical modeling. We find that GluA1-containing vesicles are confined and concentrated near sites of stimulation-induced structural plasticity. We show that confinement is mediated by actin polymerization, which hinders the active transport of GluA1-containing vesicles along the length of the dendritic shaft by modulating the rheological properties of the cytoplasm. Actin polymerization also facilitates myosin-mediated transport of GluA1-containing vesicles to exocytic sites. We conclude that neurons utilize F-actin to increase vesicular GluA1 reservoirs and promote exocytosis proximal to the sites of synaptic activity.