A dynamical circuit model for C. elegans chemotaxis with emergent sharp turns

Abstract

With its rigorously characterized connectome, the nematode Caenorhabditis elegans is a powerful model organism to study the fundamental roles of neuronal circuits in behavior. However, despite the breadth of research, many questions remain unanswered regarding how these organisms are able to successfully navigate their environment. Here, we present a biologically grounded dynamical circuit model for the investigation of sensory-guided behavior during C. elegans chemotaxis. Our model consists of the chemosensory neuron AWA, interneurons RIM and RIA, motor neurons, including SMDs and RMDs, and body wall muscles that provide proprioceptive feedback through stretch receptors. The connectivity prioritizes functional and dynamical correspondence with the biological circuit over one-to-one anatomical fidelity. After optimization with an evolutionary algorithm, the model locomotes toward a chemical attractant, effectively capturing nematode chemotactic behavior. A key emergent property of the model that contributes to successful chemotaxis is the ability to make sharp turns, which resemble the omega turns of living nematodes. The direction and magnitude of these turns depend on the phase of the ongoing locomotory cycle. The sharp turning behavior is triggered by decreases in the concentration of the attractant. In the model, decreases in attractant concentration levels reduce AWA activity, which in turn triggers disinhibition of RIM activity and subsequent changes in RIA oscillatory activity. The ensuing coordinated changes in downstream motor neurons' activity patterns produce sharp turns, which correct the model worm's path to head toward the attractant source and, after reaching the concentration gradient peak, allow the model worm to remain in its proximity. The proposed framework and its emergent dynamics provide new insights into how circuit-level dynamics may generate key features of C. elegans chemotactic behavior, including omega-like turns. In parallel, it generates experimentally testable hypotheses about how the participating neuronal elements contribute to chemotactic behavior.