Stability Analysis of Phase-Locked Bursting in Inhibitory Neuron Networks

Networks of neurons, which form central pattern generators (CPGs), are important for controlling animal behaviors. Of special interest are configurations or CPG motifs composed of reciprocally inhibited neurons, such as half-center oscillators (HCOs). Bursting rhythms of HCOs are shown to include stable synchrony or in-phase bursting, which is a phase-locked state that has zero phase difference. This in-phase bursting can co-exist with anti-phase bursting, commonly expected as the single stable state in HCOs that are connected with fast non-delayed synapses. The finding contrasts with the classical view that reciprocal inhibition has to be slow or time-delayed to synchronize such bursting neurons. Phase-locked rhythms are analyzed via Lyapunov exponents estimated with variational equations, and through the convergence rates estimated with Poincaré return maps. A new mechanism underlying multistability is proposed that is based on the spike interactions, which confer a dual property on the fast non-delayed reciprocal inhibition; this reveals the role of spikes in generating multiple co-existing phase-locked rhythms. In particular, it demonstrates that the number and temporal characteristics of spikes determine the number and stability of the multiple phase-locked states in weakly coupled HCOs. The generality of the multistability phenomenon is demonstrated by analyzing diverse models of bursting networks with various inhibitory synapses; the individual cell models include the reduced leech heart interneuron, the Sherman model for pancreatic beta cells, the Purkinje neuron model and Fitzhugh-Rinzel phenomenological model. Finally, hypothetical and experiment-based CPGs composed of HCOs are investigated, and predictions that may be verified by electrophysiologists studying the sensory-motor systems are made. This study is relevant for various applications that use CPGs such as robotics, prosthetics, and artificial intelligence. INDEX WORDS: Bursting, Central pattern generator, Fast threshold modulation, Half-center oscillator, Inhibition, Lyapunov exponents, Multistability, Networks, Neurons, Phase-locking, Poincaré return maps, Synchrony, Variational equations STABILITY ANALYSIS OF PHASE-LOCKED BURSTING IN INHIBITORY NEURON NETWORKS