Neuronal morphologies built for reliable physiology in a rhythmic motor circuit

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.

Robust emergence of sharply tuned place cell responses in hippocampal neurons with structural and biophysical heterogeneities

“…However, studies employing multicompartmental neuronal models have also demonstrated a remarkable degree of flexibility in a neuron's ion channel distributions that can combine to elicit similar physiological outcomes Basak and Narayanan 2018b;Otopalik et al 2017b;Otopalik et al 2017a;Otopalik et al 2019;Migliore et al 2018;Beining et al 2017;Taylor et al 2009).…”

“…A second class of studies have assessed pathology-induced or behaviorally relevant dendritic remodeling (atrophy or hypertrophy) in neuronal structures (van Elburg and van Ooyen 2010; van Ooyen et al 2002; Narayanan and Chattarji 2010; Narayanan et al 2005; Dhupia et al 2014). A third class of studies explored the implications for intrinsic morphological heterogeneities within a neuronal subtype(Krichmar et al 2002;Ferrante et al 2013;Beining et al 2017;Weaver and Wearne 2008;Otopalik et al 2017b;Otopalik et al 2019;Otopalik et al 2017a;Schaefer et al 2003).…”

Motor circuit function is stabilized during postembryonic growth by anterograde trans-synaptic Jelly Belly - Anaplastic Lymphoma Kinase signaling

“…Thus dendritic shape and synapse placement can have a strong influence on neuronal computational performance (reviewed in 62, 63 ). However, recent studies in the stomatogastric ganglion of crabs showed that the specific tapering of dendritic branches can effectively compact elaborate dendritic structures to a uniform electrotonic compartment, thus strongly reducing the impact of synapse positioning along a dendritic arbor on signal integration and ultimately spike output 64–66 . Conversely, experimentally reduced dendritic arbor complexity of Drosophila flight motorneurons still supports astonishingly normal neuronal performance, and only behaviors requiring fine precision appear to be negatively affected 67 .…”

Periodicity Pitch Perception Part III: Sensibility and Pachinko Volatility

“…Active conductance in dendrites can normalize the efficacy of distal synapses and democratize dendrites by making distal and proximal synapses equally efficient in influencing somatic firing. Strong dendritic tapering attenuates electrotonic attenuation to such an extent that the dendritic tree becomes approximately isopotential (Otopalik et al, 2019 ). Therefore, dendritic structures may avoid attenuation.…”