Abstract
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.
Highlights
Neurons often present complex and highly-branched morphologies
We show that a subset of cable models with geometries consistent with those observed in multiple stomatogastric ganglion (STG) neuron types (Otopalik et al, 2017a), are relatively resilient to electrotonic decrement
We find that multiple STG neuron types present electrotonically compact structures and within-neurite voltage summation that is relatively linear and directionally insensitive
Summary
How synaptic voltage events propagate within and across neurite branches is determined by the structure’s geometrical and biophysical properties. Schierwagen devised a broader mathematical description of membrane voltage distributions in complex, highly-branched neurite trees with non-uniform boundary conditions and geometries (Schierwagen, 1989). These seminal theoretical studies have provided an invaluable framework for understanding passive neuronal physiology. To date, measuring voltage attenuation across the many neurite paths presented in complex neuronal structures using electrophysiological techniques has proven difficult. Electrotonus has been experimentally assessed in only a handful of neuron types (for example: Spruston and Johnston, 1992; Spruston et al, 1994; Rapp et al, 1994; Carnevale et al, 1997; Stuart and Spruston, 1998; Chitwood et al, 1999; Jaffe and Carnevale, 1999; Otopalik et al, 2017b; Medan et al, 2018), and this greatly restricts our understanding of the breadth of biophysical organizations utilized in different neuron types and circuit contexts
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