Distinct neural circuits establish the same chemosensory behavior in C. elegans

Abstract

Animals frequently exhibit the same behavior under different environmental or physiological conditions. To what extent these behaviors are generated by similar vs. distinct mechanisms is unclear. Moreover, the circumstances under which divergent neural mechanisms establish the same behavior, and the molecular signals that regulate the same behavior across conditions, are poorly understood. We show that in C. elegans, distinct neural mechanisms mediate the same chemosensory behavior at two different life stages. Both dauer larvae and starved adults are attracted to carbon dioxide (CO2), but CO2 attraction is mediated by distinct sets of interneurons at the two life stages. Some interneurons mediate CO2 response only in dauers, some show CO2-evoked activity in adults and dauers but contribute to CO2 response only in adults, and some show CO2-evoked activity that opposes CO2 attraction in adults but promotes CO2 attraction in dauers. We also identify a novel role for insulin signaling in establishing life stage-specific CO2 responses by modulating interneuron activity. Further, we show that a combinatorial code of both shared and life-stage-specific molecular signals regulate CO2 attraction. Our results identify a mechanism by which the same chemosensory behavior can be generated by distinct neural circuits, revealing an unexpected complexity to chemosensory processing.

Mind of a dauer: Comparative connectomics reveals developmental plasticity

“…One example is CO 2 sensing in different developmental stages. Consistent with a previous report that AIY is not required for CO 2 response in dauers unlike adults [23], we easily identified that the connection from BAG [24], which is responsible for CO 2 detection to AIY does not exist in the dauer connectome while it exists in the adult (Supplementary Data 1). Now, it is possible to focus on additional specific connections and check how the neuronal functions differ in terms of CO 2 sensing using optogenetics and calcium imaging like the IL2-RIG experiments we have conducted.…”

Carbon dioxide shapes parasite-host interactions in a human-infective nematode

“…In contrast, S. stercoralis freeliving adults are neutral to CO2 (Figure 1). In addition, C. elegans dauer larvae and S. stercoralis iL3s, which are homologous life stages [54][55][56], show opposite responses to CO2; C. elegans dauers are attracted to CO2 [39,57,58], whereas S. stercoralis iL3s are repelled by CO2 (Figure 1) [25,42]. C. elegans dauers form when environmental conditions are unfavorable, and CO2 attraction likely enables dauers to migrate toward potential food sources [39,58,59].…”

“…In addition, C. elegans dauer larvae and S. stercoralis iL3s, which are homologous life stages [54][55][56], show opposite responses to CO2; C. elegans dauers are attracted to CO2 [39,57,58], whereas S. stercoralis iL3s are repelled by CO2 (Figure 1) [25,42]. C. elegans dauers form when environmental conditions are unfavorable, and CO2 attraction likely enables dauers to migrate toward potential food sources [39,58,59]. Thus, CO2 preferences of homologous life stages are not conserved across nematode species but instead reflect the ethological requirements of each species and life stage.…”

“…The extent to which interneuron function is conserved across species remains to be determined. In C. elegans, we previously showed that the CO2-evoked activity patterns of interneurons vary depending on the life stage of the animal [39,58]. Thus, it is possible that the CO2 microcircuit that operates downstream of BAG to mediate CO2 response in S. stercoralis differs in iL3s vs. iL3as.…”