Sloppy morphological tuning in identified neurons of the crustacean stomatogastric ganglion

Abstract

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.DOI: http://dx.doi.org/10.7554/eLife.22352.001

Neuronal morphologies built for reliable physiology in a rhythmic motor circuit

“…In previous work, we were surprised to find that STG neurons exhibit neurites as long as 1 mm in length, and neurite diameters that often tapered from 10-20 microns at the primary neurite junction, to sub-micron diameters at the terminating tips (Otopalik et al, 2017a). Passive cable theory, first applied to the study of neurons by Wilfred Rall and colleagues, suggests that voltage signals passively propagating such long distances are likely to undergo a great deal of attenuation (Rall, 1960(Rall, , 1964(Rall, , 1969Jack et al, 1975).…”

“…In two recent studies, we characterized the morphology (Otopalik et al, 2017a) and passive physiology (Otopalik et al, 2017b) of the identified neurons of the crustacean stomatogastric ganglion (STG), a small central pattern-generating circuit mediating the rhythmic contractions of the animal's foregut. The 14 identified neurons of the STG present distinct, cell-type-specific physiological waveforms, firing patterns and circuit functions.…”

“…The 14 identified neurons of the STG present distinct, cell-type-specific physiological waveforms, firing patterns and circuit functions. We quantified numerous morphological features pertaining to the macroscopic branching patterns and fine cable properties of four neuron types (Otopalik et al, 2017a). There was quantifiable inter-animal variability in all features within neuron types, and no single metric or combination of metrics distinguished the four neuron types.…”

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).…”