Neuronal morphologies built for reliable physiology in a rhythmic motor circuit

It is often assumed that highly-branched neuronal structures perform compartmentalized computations. However, previously we showed that the Gastric Mill (GM) neuron in the crustacean stomatogastric ganglion (STG) operates like a single electrotonic compartment, despite having thousands of branch poi...

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Bibliographic Details
Published in:eLife 2019-01, Vol.8
Main Authors: Otopalik, Adriane G, Pipkin, Jason, Marder, Eve
Format: Article
Language:English
Subjects:
Action Potentials - physiology
Animals
Bias
Brachyura - cytology
Brachyura - physiology
Cables
cancer borealis
electrotonus
Ganglia, Invertebrate - cytology
Ganglia, Invertebrate - physiology
Gizzard, Non-avian - cytology
Gizzard, Non-avian - physiology
Integration
Laboratories
Libraries
Models, Neurological
Morphology
Nerve Net - physiology
Neurites - physiology
Neurons
Neurons - physiology
Neuroscience
Physiology
Research Advance
Rhythms
Stomatogastric ganglion
Synaptic Potentials - physiology
variability
voltage Integration
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Summary:It is often assumed that highly-branched neuronal structures perform compartmentalized computations. However, previously we showed that 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; 2017b). Here we show that compact electrotonic architecture is generalizable to other STG neuron types, and that these neurons present direction-insensitive, linear voltage integration, suggesting they pool synaptic inputs across their neuronal structures. We also show, using simulations of 720 cable models spanning a broad range of geometries and passive properties, 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.
ISSN:2050-084X
2050-084X
DOI:10.7554/eLife.41728