Neuronal morphologies built for reliable physiology in a rhythmic motor circuit

Abstract

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in eLife 8 (2019): e41728. doi: 10.7554/eLife.41728.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.We thank Jennifer Bestman for assistance in spinning disk and confocal microscopy; the Marine Resources Center at the Marine Biological Laboratories for acquiring and maintaining animals; Louie Kerr at the Central Microscopy Facility; Dana Mock-Munoz de Luna for administrative support; Kam-ran Kodhakhah, Heather Rhodes, and the 2017 Grass Fellows for their support and feedback; and lastly, Edward Dougherty at the Brandeis University Confocal Imaging Lab for support and microscope maintenance. This study was funded by the Grass Foundation and NINDS awards to F31NS092126 to AO and R35NS097343 to EM