Distinct neurogenetic mechanisms establish the same chemosensory valence state at different life stages in Caenorhabditis elegans.

An animal's preference for many chemosensory cues remains constant despite dramatic changes in the animal's internal state. The mechanisms that maintain chemosensory preference across different physiological contexts remain poorly understood. We previously showed that distinct patterns of neural activity and motor output are evoked by carbon dioxide (CO2) in starved adults vs dauers of Caenorhabditis elegans, despite the two life stages displaying the same preference (attraction) for CO2. However, how the distinct CO2-evoked neural dynamics and motor patterns contribute to CO2 attraction at the two life stages remained unclear. Here, using a CO2 chemotaxis assay, we show that different interneurons are employed to drive CO2 attraction at the two life stages. We also investigate the molecular mechanisms that mediate CO2 attraction in dauers vs adults. We show that insulin signaling promotes CO2 attraction in dauers but not starved adults and that different combinations of neurotransmitters and neuropeptides are used for CO2 attraction at the two life stages. Our findings provide new insight into the distinct molecular and cellular mechanisms used by C. elegans at two different life stages to generate attractive behavioral responses to CO2.

Differential processing of a chemosensory cue across life stages sharing the same valence state in Caenorhabditis elegans.

Many chemosensory cues evoke responses of the same valence under widely varying physiological conditions. It remains unclear whether similar or distinct neural mechanisms are involved in the detection and processing of such chemosensory cues across contexts. We show that in Caenorhabditis elegans, a chemosensory cue is processed by distinct neural mechanisms at two different life stages that share the same valence state. Both starved adults and dauer larvae are attracted to carbon dioxide (CO2), but CO2 evokes different patterns of neural activity and different motor outputs at the two life stages. Moreover, the same interneuron within the CO2 microcircuit plays a different role in driving CO2-evoked motor output at the two life stages. The dauer-specific patterns of CO2-evoked activity in this interneuron require a dauer-specific gap junction complex and insulin signaling. Our results demonstrate that functionally distinct microcircuits are engaged in response to a chemosensory cue that triggers the same valence state at different life stages, revealing an unexpected complexity to chemosensory processing.