Aversive memory and extinction learning for noxious stimuli and aversive tastants in bumblebees

Rapid learning of aversive stimuli is adaptive, but the persistence of the avoidance response in the absence of further reinforcement might depend on the severity of the adverse experience. For example, an experience involving injury would be expected to lead to more durable memory than the mere exposure to an unpleasant tastant, especially when new experiences indicate that the aversive stimulus is no longer present. We investigated how bumblebees (Bombus terrestris) learn and retain associations between flower colours and two types of aversive stimuli: electric shock and saturated salt (NaCl) solution. Using a conditioning paradigm, we examined how these stimuli influence avoidance learning across foraging bouts and tracked the process of extinction learning, the formation of new memory in response to the absence of the reinforcement, over two weeks. Our results show that bees rapidly learn to avoid both stimuli, and reach >90% accuracy of avoidance after six foraging bouts. We then examined how bees modified their avoidance behaviour in the absence of further aversive stimulation. Testing extinction learning on days 1, 3, 5, 7 and 14, we found that electric shock as a nociceptive stimulus induces a more persistent avoidance response, whereas exposure to the salt by engaging gustatory aversion pathways leads to a three times faster extinction rate. This suggests that although the initial training leads to equal levels of avoidance for both stimuli, bumblebees might display greater behavioural flexibility when updating the association between a colour and an unpleasant taste in comparison to a potentially injurious stimulus.