Controlling interneuron activity in Caenorhabditis elegans to evoke chemotactic behavior

Animals locate and track chemoattractive gradients in the environment to find food. With its small nervous system, Caenorhabditis elegans is a good model system(1,2) in which to understand how the dynamics of neural activity control this search behavior. Extensive work on the nematode has identified the neurons that are necessary for the different locomotory behaviors underlying chemotaxis through laser ablation(3–7), activity recording in immobilized animals and the study of mutants(4,5). However, we do not know the neural activity patterns in C. elegans that are sufficient to control its complex chemotactic behavior. To understand how the activity in its interneurons coordinate different motor programs to lead the animal to food, we used optogenetics and new optical tools to directly manipulate neural activity in freely moving animals to evoke chemotactic behavior. By deducing the classes of activity patterns triggered during chemotaxis and exciting individual neurons with these patterns, we identified interneurons that control the essential locomotory programs for this behavior. Surprisingly, we discovered that controlling the dynamics of activity in just one interneuron pair (AIY) was sufficient to force the animal to locate, turn towards and track virtual light gradients. Two distinct activity patterns triggered in AIY as the animal moved through the gradient, controlled reversals and gradual turns to drive chemotactic behavior. Since AIY are post-synaptic to most chemosensory and thermosensory neurons(8), these activity patterns in AIY are likely to play an important role in controlling and coordinating different taxis behaviors of the animal.