Multiple Intrinsic Membrane Properties are Modulated in a Switch from Single to Dual-Network Activity

Abstract

Neural network flexibility extends to changes in neuronal participation between networks. This neuronal switching can include neurons moving between single- and dual-network activity. We previously identified an example in which bursting at a second frequency occurs due to modulation of intrinsic membrane properties instead of synaptic recruitment into a second network. However, the intrinsic properties that are modulated were not determined. Here, we use small networks in the Jonah crab (Cancer borealis) stomatogastric nervous system (STNS) to examine modulation of intrinsic properties underlying neuropeptide- (Gly1-SIFamide) elicited neuronal switching. The LPG neuron switches from exclusive participation in the fast pyloric ([~]1 Hz) network, due to electrical coupling, to dual-network activity which includes periodic escapes from the fast rhythm via intrinsically-generated oscillations at the slower gastric mill network frequency ([~]0.1 Hz). We isolated LPG from both networks using pharmacology and hyperpolarizing current injection. Gly1-SIFamide increased LPG intrinsic excitability and rebound from inhibition, and decreased spike frequency adaptation, which can all contribute to intrinsic bursting. Using ion substitution and channel blockers, we found that a hyperpolarization-activated current, a persistent sodium current, and a calcium or calcium-related current(s) appear to be primary contributors to Gly1-SIFamide-elicited LPG intrinsic bursting. However, this intrinsic bursting was more sensitive to blocking currents when LPG received rhythmic electrical coupling input from the fast network than in the isolated condition. Overall, a switch from single- to dual-network activity can involve modulation of multiple intrinsic properties, while synaptic input from a second network can shape the contributions of these properties. New and NoteworthyNeuropeptide-elicited intrinsic bursting was recently determined to switch a neuron from single to dual-network participation. Here we identified multiple intrinsic properties modulated in the dual-network state and candidate ion channels underlying the intrinsic bursting. Bursting at the second network frequency was more sensitive to blocking currents in the dual-network state than when neurons were synaptically isolated from their home network. Thus, synaptic input can shape the contributions of modulated intrinsic properties underlying dual-network activity.