Honey bees can store and retrieve independent memory traces after complex experiences that combine appetitive and aversive associations

Abstract

Real-world experiences often mix appetitive and aversive events. Understanding the ability of animals to extract, store and use this information is an important issue in neurobiology. We used honey bees as model organism to study learning and memory after a differential conditioning paradigm that combines appetitive and aversive training trials. First, we used an aversive conditioning paradigm that constitutes a clear opposite of the well-known appetitive olfactory conditioning of the proboscis extension response. A neutral odour is presented paired with the bitter substance quinine. Aversive memory is evidenced later as an odour-specific impairment in appetitive conditioning. Then, we tested the effect of mixing appetitive and aversive conditioning trials distributed along the same training session. Differential conditioning protocols like this were used previously to study the ability to discriminate odours; however, they were not focused on whether appetitive and aversive memories are formed. We found that after differential conditioning, honey bees establish independent appetitive and aversive memories that do not interfere with each other during acquisition or storage. Finally, we moved the question forward to retrieval and memory expression to evaluate what happens when appetitive and the aversive learned odours are mixed during a test. Interestingly, opposite memories compete in such a way that they do not cancel each other out. Honey bees showed the ability to switch from expressing appetitive to aversive memory depending on their satiation level.