Aversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom body

Summary In Drosophila, negatively reinforcing dopaminergic neurons also provide the inhibitory control of satiety over appetitive memory expression. Here we show that aversive learning causes a persistent depression of the conditioned odor drive to two downstream feed-forward inhibitory GABAergic interneurons of the mushroom body, called MVP2, or mushroom body output neuron (MBON)-γ1pedc>α/β. However, MVP2 neuron output is only essential for expression of short-term aversive memory. Stimulating MVP2 neurons preferentially inhibits the odor-evoked activity of avoidance-directing MBONs and odor-driven avoidance behavior, whereas their inhibition enhances odor avoidance. In contrast, odor-evoked activity of MVP2 neurons is elevated in hungry flies, and their feed-forward inhibition is required for expression of appetitive memory at all times. Moreover, imposing MVP2 activity promotes inappropriate appetitive memory expression in food-satiated flies. Aversive learning and appetitive motivation therefore toggle alternate modes of a common feed-forward inhibitory MVP2 pathway to promote conditioned odor avoidance or approach.
Highlights • Aversive learning reduces odor-specific feed-forward inhibition in mushroom body • Feed-forward inhibition selectively inhibits avoidance-directing neural pathways • Appetitive motivation increases feed-forward inhibition in the mushroom body • Imposing feed-forward inhibition favors appetitive memory expression
Fruit fly memory and its state-dependent behavioral expression involve modulation of mushroom body output synapses. Perisse et al. demonstrate aversive learning and appetitive motivation toggle alternate modes of feed-forward inhibition in mushroom body, favoring either conditioned avoidance or approach behavior.