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J Exp Biol. 2013 Aug 15;216(Pt 16):2985-97. doi: 10.1242/jeb.086629.

Rules and mechanisms of punishment learning in honey bees: the aversive conditioning of the sting extension response.

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Université de Toulouse, UPS, Research Centre for Animal Cognition, Toulouse, France.


Honeybees constitute established model organisms for the study of appetitive learning and memory. In recent years, the establishment of the technique of olfactory conditioning of the sting extension response (SER) has yielded new insights into the rules and mechanisms of aversive learning in insects. In olfactory SER conditioning, a harnessed bee learns to associate an olfactory stimulus as the conditioned stimulus with the noxious stimulation of an electric shock as the unconditioned stimulus. Here, we review the multiple aspects of honeybee aversive learning that have been uncovered using Pavlovian conditioning of the SER. From its behavioral principles and sensory variants to its cellular bases and implications for understanding social organization, we present the latest advancements in the study of punishment learning in bees and discuss its perspectives in order to define future research avenues and necessary improvements. The studies presented here underline the importance of studying honeybee learning not only from an appetitive but also from an aversive perspective, in order to uncover behavioral and cellular mechanisms of individual and social plasticity.


SER; aversive conditioning; conditioning; division of labor; honeybee; insect; learning; memory; stimulus responsiveness; stimulus sensitivity; sting extension response

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