Neuronal morphologies built for reliable physiology in a rhythmic motor circuit

Abstract

The neurons of the crustacean stomatogastric ganglion (STG) exhibit highly-conserved firing patterns, voltage waveforms, and circuit functions despite quantifiable animal-toanimal variability in their neuronal morphologies. In recent work, we showed that one neuron type, the Gastric Mill (GM) neuron, is electrotonically compact and operates much like a single compartment, despite having thousands of branch points and a total cable length on the order of 10 mm. Here, we explore how STG neurite morphology

Degeneracy in the nervous system: from neuronal excitability to neural coding

“…Despite their highly variable morphological features, STG neurons manifest a reliable firing pattern, suggesting that different anatomical structures can provide a degenerate space to produce similar neuronal physiology. [60][61][62]…”

The dynamic range of voltage-dependent gap junction signaling is maintained by Ih-induced membrane potential depolarization

“…The hyperpolarized activation values could thus indicate a substantial space clamp issue in this large cell, where with increasing distance of the somatic electrode from I h ’s location, current measurement degrades and, due to the electrotonic distance, more hyperpolarizing current at the recording site is necessary to cause corresponding voltage changes at the current source. This effect may be exaggerated by impedance changes within the LG neurites [25] that favor current flow from the neuropil toward the soma, but not vice versa. However, I h has never been recognized in LG before, nor does it seem necessary to create rhythmic gastric mill activity [18].…”

Neuropeptide Modulation Increases Dendritic Electrical Spread to Restore Neuronal Activity Disrupted by Temperature

“…Measurements of length constants in other STG neurons indicate that neuropils are electrotonically compact with length constants of .1000 mm. STG neuropil anatomy also seems to support the propagation of synaptic signals because of continuously decreasing axial resistance from small tertiary neurites to the larger primary neurites (Otopalik et al, 2019). However, STG neuron spike initiation sites are spatially distant from the neuropil, close to where the main motor nerve exits the ganglion (Miller and Selverston, 1979;Raper, 1979).…”

“…Our imaging data corroborates this assumption. The morphology of the STG neuropil (Otopalik et al, 2019), although advantageous for orthodromic electrical signals, antagonizes antidromic propagation because of increasingly larger axial resistances resulting from smaller diameter neurites. At 10°C, much of the calcium signal was obtained in the main neurite and was less prevalent at 13°C.…”

“…Passive electrical propagation in dendrites is necessary to support summation required for action potential (AP) initiation. Because dendrites rarely support active AP propagation, changes in biophysical membrane properties, such as ionic conductance levels, can significantly alter electrical spread (Hoffman et al, 1997;Short et al, 2017;Otopalik et al, 2019). Acute temperature changes are known to alter active and passive biophysical properties but rarely do so linearly or equally across properties, which can disrupt neuronal activity (Collins and Rojas, 1982;Hille, 2001;Cao and Oertel, 2005).…”