Side-specificity of olfactory learning in the honeybee: US input side

In honeybees, Apis mellifera L., the proboscis extension reflex (PER) can be conditioned by associating an odor stimulus (CS) with a sucrose reward (US). As the neural structures involved in the detection and integration of CS and US are bilaterally symmetrical in the bee brain, we ask what respective role each brain side plays in the conditioning process. More specifically, the US normally used in conditioning experiments is the compound stimulation of the antennae (which triggers the PER) and of the proboscis (where bees lick the sucrose solution). Anatomically, the brain receives unilateral US input through each antenna, but bilateral input from the proboscis. By controlling each US component, we show that an antenna–US produces unilateral sensitization, whereas a proboscis–US or a compound–US induces bilateral sensitization. Bees can learn a unilateral odor CS with all three USs, but when a proboscis–US is used, new learning is inhibited on the contralateral side, owing to a possible US-preexposure effect. Furthermore, we show that the antenna–US induces both unilateral and bilateral reinforcement processes, whereas the proboscis–US produces only bilateral effects. Based on these data, we propose a functional model of the role of each brain side in processing lateralized CSs and USs in olfactory learning in honeybees.