Roles of ionic currents and synaptic transmission in shaping the pyloric and gastric mill dynamics in lobsters, Homarus americanus

Abstract

The dynamics and coordination of neurons are essential in forming a functional neural network. The great complexity of mammalian circuits imposes significant barriers to investigating the connectivity and function of neural circuits in detail. Only recently have major advances in genome editing and optogenetics enable significant progresses in mammalian neural circuit research. Because of the similarities between vertebrate and invertebrate systems, especially with regards to basic principles of neuronal function, invertebrate model systems such as the crustacean stomatogastric nervous system (STNS) have been intensively studied for a half-century. These studies have contributed significantly to our understanding of the mechanism underlying the generation of functional motor rhythms and coordination of neurons and networks at the single cell level. The STNS is a powerful model for investigating the contribution of cell-to-cell synaptic connections and individual ionic currents in generating a specific motor rhythmic pattern. Research on small invertebrate circuits such as STNS provide key insights into how neural circuits operate in the numerically larger and less accessible mammalian nervous system. In the STNS, the stomatogastric ganglion (STG) receives modulatory synaptic inputs from a pair of commissural ganglia (CoGs) and a single esophageal ganglion (OG). The STG is composed of the pyloric and gastric mill CPGs that produce distinctive motor patterns. The gastric mill CPG produces slow oscillations often with 8 [nil] 20 second (s) burst period and pyloric CPG produces fast oscillations ranging from 0.5 [nil] 2s period. Besides the burst period, the oscillatory trajectories of the pyloric and gastric mill neurons are different--the gastric mill bursts feature a long plateau phase while the pyloric bursts are sinusoidal-like. In our work, we investigate the role of ionic currents and synapses in shaping the distinctive rhythmic patterns between the fast oscillating pyloric neurons and slow oscillating gastric mill neurons in the STG of the American lobster, Homarus americanus. We have found that both the hyperpolarization activated cationic current (I_h) and transient outward current (I_A) show different modulatory effects on the oscillations and phase between the pyloric and gastric mill neurons, which contribute to the bifurcation of their dynamics. The persistent sodium current (I_Nap) and calcium activated non-specific cationic current (I_CAN) show strong inhibitory effects on both the pyloric and gastric mill neurons, suggesting that they are essential in generating and maintaining the pyloric and gastric mill rhythms. Besides ionic currents, synapses also contribute to shaping the distinct dynamics of the pyloric and gastric mill CPGs. Our results show that both glutamatergic and cholinergic synapses are essential in maintaining the phase and stable oscillations of pyloric neurons. As for the gastric mill CPG, cholinergic synapses are necessary to maintain an active network; in contrast, glutamatergic/GABA synapses have inhibitory effects on the network activity. Our work offers valuable perspective and insights for research on oscillatory dynamics of neurons and CPGs in both the STNS and other model systems.