Parallel Reinforcement Pathways for Conditioned Food Aversions in the Honeybee

Avoiding toxins in food is as important as obtaining nutrition. Conditioned food aversions have been studied in animals as diverse as nematodes and humans [1, 2], but the neural signaling mechanisms underlying this form of learning have been difficult to pinpoint. Honeybees quickly learn to associate floral cues with food [3], a trait that makes them an excellent model organism for studying the neural mechanisms of learning and memory. Here we show that honeybees not only detect toxins but can also learn to associate odors with both the taste of toxins and the postingestive consequences of consuming them. We found that two distinct monoaminergic pathways mediate learned food aversions in the honeybee. As for other insect species conditioned with salt or electric shock reinforcers [4–7], learned avoidances of odors paired with bad-tasting toxins are mediated by dopamine. Our experiments are the first to identify a second, postingestive pathway for learned olfactory aversions that involves serotonin. This second pathway may represent an ancient mechanism for food aversion learning conserved across animal lineages. ► Learned food avoidances arise from two independent reinforcement pathways ► Detection of toxins requires the responses of multiple gustatory neurons ► Learned avoidance of odors associated with aversive taste involves dopamine ► Learned avoidance of odors associated with toxin ingestion involves serotonin