Circuit Degeneracy Facilitates Robustness and Flexibility of Navigation Behavior in C. elegans

Abstract

Animal behaviors are robust and flexible. To elucidate how these two conflicting features of behavior are encoded in the nervous system, we analyzed the neural circuits generating a C. elegans thermotaxis behavior, in which animals migrate toward the past cultivation temperature (Tc). We identified multiple circuits that are highly overlapping but individually regulate distinct behavioral components to achieve thermotaxis. When the regulation of a behavioral component is disrupted following single cell ablations, the other components compensate the deficit, enabling the animals to robustly migrate toward the Tc. Depending on whether the environmental temperature surrounding the animals is above or below the Tc, different circuits regulate the same behavioral components, mediating the flexible switch between migration up or down toward the Tc. These context-dependencies within the overlapping sub-circuits reveal the implementation of degeneracy in the nervous system, providing a circuit-level basis for the robustness and flexibility of behavior.