Aversive learning overcomes appetitive innate responding in honeybees

Despite their miniature brain, honeybees have emerged as a powerful model for the study of learning and memory. Yet, they also exhibit innate responses to biologically relevant social signals such as pheromones. Here, we asked whether the bees' developed learning capabilities allow them to overcome hardwired appetitive responses. Can they learn that attractant pheromones, that are not normally associated with a noxious stimulation in nature, predict the punishment of an electric shock? Immobilized honeybees were trained to discriminate two odorants, one that was paired with a shock and another that had no consequences. We measured whether they learned to produce aversive sting extension responses to the punished but not the non-punished odorant. One odorant was a neutral odor without innate value while the other was either an attractive pheromone (geraniol or citral) or an attractive floral odorant (phenylacetaldehyde). In all cases, bees developed a conditioned aversive response to the punished odorant, be it pheromone or not, and efficiently retrieved this information 1 h later. No learning asymmetries between odors were found. Thus, associative aversive learning in bees is strong enough to override preprogrammed responding, thus reflecting an impressive behavioral flexibility.