Aversive Training Induces Both Presynaptic and Postsynaptic Suppression in Drosophila.

The α′β′ subtype of Drosophila mushroom body neurons (MBn) is required for memory acquisition, consolidation and early memory retrieval after aversive olfactory conditioning. However, in vivo functional imaging studies have failed to detect an early forming memory trace in these neurons as reflected by an enhanced G-CaMP signal in response to presentation of the learned odor. Moreover, whether cellular memory traces form early after conditioning in the mushroom body output neurons (MBOn) downstream of the α′β′ MBn remains unknown. Here, we show that aversive olfactory conditioning suppresses the calcium responses to the learned odor in both α′3 and α′2 axon segments of α′β′ MBn and in the dendrites of α′3 MBOn immediately after conditioning using female flies. Notably, the cellular memory traces in both α′3 MBn and α′3 MBOn are short-lived and persist for <30 min. The suppressed response in α′3 MBn is accompanied by a reduction of acetylcholine (ACh) release, suggesting that the memory trace in postsynaptic α′3 MBOn may simply reflect the suppression in presynaptic α′3 MBn. Furthermore, we show that the α′3 MBn memory trace does not occur from the inhibition of GABAergic neurons via GABAA receptor activation. Because activation of the α′3 MBOn drives approach behavior of adult flies, our results demonstrate that aversive conditioning promotes avoidance behavior through suppression of the α′3 MBn–MBOn circuit. [ABSTRACT FROM AUTHOR]