Avoiding pitfalls: Trace conditioning and rapid aversive learning during route navigation in desert ants

Abstract

The ability of bees and ants to learn long visually guided routes in complex environments is perhaps one of the most spectacular pieces of evidence for the impressive power of their small brains. While flying bees can visit flowers in an optimised sequence over kilometres, walking ants can precisely recapitulate routes of up to a hundred metres in complex environments. It is clear that route following depends largely on learnt visual information and we have good idea how views can guide individuals along them, however little is known about the mechanisms that control route learning and development. Here we show that ants in natural environments can actively learn a route detour to avoid a pit trap and that this depends on a process analogous to aversive trace conditioning. Views experienced before falling into the trap become associated with the ensuing negative outcome and thus trigger salutary turns on the subsequent trip. This drives the ants to orient away from the goal direction and avoid the trap. If the pit is avoided, the novel views experienced during the detour become positively reinforced and the new route crystallises. We discuss how such an interplay between appetitive and aversive memories might be implemented in insect neural circuitry.