Decoding a neural circuit controlling global animal state in C. Elegans

Abstract

Brains organize behavior and physiology to optimize the response to threats or opportunities. We dissect how 21%2, an indicator of surface exposure, reprograms C. elegans’ global state, inducing sustained locomotory arousal and altering expression of neuropeptides, metabolic enzymes, and other non-neural genes. The URX 02-sensing neurons drive arousal at 21% 02 by tonically activating the RMG intemeurons. Stimulating RMG is sufficient to switch behavioral state. Ablating the ASH, ADL or ASK sensory neurons connected to RMG by gap junctions does not disrupt arousal. However, disrupting cation currents in these neurons curtails RMG neurosecretion and arousal. RMG signals high 02 by peptidergic secretion. Neuropeptide reporters reveal neural circuit state, as neurosecretion stimulates neuropeptide expression. Neural imaging in unrestrained animals shows that URX and RMG encode 02 concentration rather than behavior, while the activity of downstream intemeurons such as AVB and AIY reflect both 02 levels and the behavior being executed.