Behavioral motifs and neural pathways coordinating O2 responses and aggregation in C. elegans

Abstract

Background: Simple stimuli can evoke complex behavioral responses coordinated by multiple neural circuits. O(2) is an important environmental variable for most animals. The nematode C. elegans avoids high O(2), and O(2) levels regulate its foraging and aggregation.

Results: Here, we dissect aggregation and responses to O(2) gradients into behavioral motifs and show how O(2) 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 O(2). The rise in O(2) levels experienced by animals leaving a group induces both reversal and turning. Conversely, the fall in O(2) 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 O(2) rises. Avoidance of high O(2) 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 O(2) responsiveness and aggregation can be modified by starvation, but this is regulated by natural variation in the npr-1 neuropeptide receptor.

Conclusions: Our work provides insights into how a complex behavior emerges from simpler behavioral motifs coordinated by a distributed circuit.