Sensory Neurons Arouse C. elegans Locomotion via Both Glutamate and Neuropeptide Release

C. elegans undergoes periods of behavioral quiescence during larval molts (termed lethargus) and as adults. Little is known about the circuit mechanisms that establish these quiescent states. Lethargus and adult locomotion quiescence is dramatically reduced in mutants lacking the neuropeptide receptor NPR-1. Here, we show that the aroused locomotion of npr-1 mutants results from the exaggerated activity in multiple classes of sensory neurons, including nociceptive (ASH), touch sensitive (ALM and PLM), and stretch sensing (DVA) neurons. These sensory neurons accelerate locomotion via both neuropeptide and glutamate release. The relative contribution of these sensory neurons to arousal differs between larval molts and adults. Our results suggest that a broad network of sensory neurons dictates transitions between aroused and quiescent behavioral states.
Author Summary Animals switch between periods of behavioral arousal and quiescence in response to environmental, developmental, and circadian cues. Little is known about the circuit mechanisms that produce these behavioral states. During larval molts, C. elegans exhibits a sleep-like state (termed lethargus) that is characterized by the absence of feeding and profound locomotion quiescence. We previously showed that mutants lacking the neuropeptide receptor NPR-1 exhibit increased arousal during larval molts, which is in part mediated by increased secretion of an arousal peptide (PDF-1). Here, we compare the circuits regulating arousal in larval molts and adults. We show that a broad network of sensory neurons arouses locomotion but that the impact of each neuron differs between lethargus and adults. We propose that this broad sensory network allows C. elegans to adapt its behavior across a broad range of developmental and physiological circumstances.