An RFamide signaling system balances turning and forward locomotion to optimize global food search in Caenorhabditis elegans.

Abstract

Neuromodulators such as neuropeptides activate specific G-protein-coupled receptors to reconfigure activity patterns of neural circuits and alter animal behavior. However, we have an incomplete understanding of the context-dependent mechanisms through which neuromodulators alter in vivo behavioral states. Here, we report a novel off-food behavioral requirement of the Caenorhabditis elegans RFamide receptor npr-1. Removal from food initiates a unique motor program where wild-type worms increase their turning frequency during local search for food. Upon longer exposure to starvation, the turns are suppressed and replaced by forward locomotion that favors efficient dispersal during global food search to locate new resources. Animals with loss of mutation in the npr-1 locus or the NPR-1(215F) variant exhibit strikingly reduced turning ability during global search. Moreover, in contrast to their high-speed on-food locomotion, mutations in NPR-1 or its ligands FLP-18 and FLP-21 produce dramatic reduction in locomotion rate and dispersal efficiency during global search. Interestingly, npr-1 mutants are still capable of resuming high-speed locomotion when re-introduced into food after starvation. Thus, our results probably suggest alternate circuit mechanisms underlying the contradictory NPR-1-mediated modulation of locomotion in the presence and absence of food.