Behavioral Motifs and Neural Pathways Coordinating O2 Responses and Aggregation in C. elegans

SummaryBackgroundSimple stimuli can evoke complex behavioral responses coordinated by multiple neural circuits. O2 is an important environmental variable for most animals. The nematode C. elegans avoids high O2, and O2 levels regulate its foraging and aggregation.ResultsHere, we dissect aggregation and responses to O2 gradients into behavioral motifs and show how O2 responses can promote aggregation. To remain in a group, C. elegans continually modify their movement. Animals whose heads emerge from a group will reverse or turn, thereby returning to the group. Re-entry inhibits further reversal, aiding retention in the group. If an animal's tail exits a group during a reversal, it switches to forward movement, returning to the group. Aggregating C. elegans locally deplete O2. The rise in O2 levels experienced by animals leaving a group induces both reversal and turning. Conversely, the fall in O2 encountered when entering a clump suppresses reversal, turning, and high locomotory activity. The soluble guanylate cyclases GCY-35 and GCY-36, which are expressed in head and tail neurons, promote reversal and turning when O2 rises. Avoidance of high O2 is also promoted by the TRP-related channel subunits OCR-2 and OSM-9, and the transmembrane protein ODR-4, acting in the nociceptive neurons ASH and ADL. Both O2 responsiveness and aggregation can be modified by starvation, but this is regulated by natural variation in the npr-1 neuropeptide receptor.ConclusionsOur work provides insights into how a complex behavior emerges from simpler behavioral motifs coordinated by a distributed circuit.