A Behavioral Switch: cGMP and PKC Signaling in Olfactory Neurons Reverses Odor Preference in C. elegans

SummaryInnate chemosensory preferences are often encoded by sensory neurons that are specialized for attractive or avoidance behaviors. Here, we show that one olfactory neuron in Caenorhabditis elegans, AWCON, has the potential to direct both attraction and repulsion. Attraction, the typical AWCON behavior, requires a receptor-like guanylate cyclase GCY-28 that acts in adults and localizes to AWCON axons. gcy-28 mutants avoid AWCON-sensed odors; they have normal odor-evoked calcium responses in AWCON but reversed turning biases in odor gradients. In addition to gcy-28, a diacylglycerol/protein kinase C pathway that regulates neurotransmission switches AWCON odor preferences. A behavioral switch in AWCON may be part of normal olfactory plasticity, as odor conditioning can induce odor avoidance in wild-type animals. Genetic interactions, acute rescue, and calcium imaging suggest that the behavioral reversal results from presynaptic changes in AWCON. These results suggest that alternative modes of neurotransmission can couple one sensory neuron to opposite behavioral outputs.