A data-driven biophysical network model reproduces C. elegans premotor neural dynamics

Abstract: C. elegans locomotion is composed of switches between forward and reversal states punctuated by turns. This locomotory capability is necessary for the nematode to move towards attractive stimuli, escape noxious chemicals, and explore its environment. Although experimentalists have identified a number of premotor neurons as drivers of forward and reverse motion, how these neurons work together to produce the behaviors observed remains to be understood. Towards a better understanding of C. elegans neurodynamics, we present in this paper a minimally parameterized, biophysical dynamical systems model of the premotor network. Our model consists of a recurrently connected collection of premotor neurons (the core group) driven by over a hundred sensory and interneurons that provide diverse feedforward inputs to the core group. It is data-driven in the sense that the choice of neurons in the core group follows experimental guidance, anatomical structures are dictated by the connectome, and physiological parameters are deduced from whole-brain imaging and voltage clamps data. When simulated with realistic input signals, our model produces premotor activity that closely resembles experimental data: from the seemingly random switching between forward and reversal behaviors to the synchronization of subnetworks to various higher-order statistics. We posit that different roles are played by gap junctions and synaptic connections in switching dynamics. The model correctly predicts behavior such as dwelling versus roaming as a result of the synaptic inputs received, and we demonstrate that it can be used to study how the activity level of certain individual neurons impacts behavior.