A Priming Circuit Controls the Olfactory Response and Memory in Drosophila

Abstract

In implicit memory priming, exposure to one stimulus influences the subsequent experience of other stimuli. Here we found that in Drosophila melanogaster, a prior encounter with an aversive stimulus produces long lasting changes in the animal’s neural and behavioral response to a novel odor. The encounter of a novel odor moreover activates the reward circuitry and establishes an approach memory. We identified a pair of Priming Neurons that mediate this priming effect. By recording the activity of these neurons in the priming circuit in real time, we show that Priming Neurons act as the interface of the conditioned and unconditioned pathways to collate the mushroom body output signals and distribute them selectively to the reward and punishment aversive pathways during the presentation of a novel odor. Beyond direct exposure to unconditioned stimuli, this complex memory priming system provides an animal with a larger time window to assess more sensory inputs for valence relationships during a salient learning experience.