Distinct neuronal circuits mediate experience-dependent, non-associative osmotactic responses in Drosophila

Osmotactic responses can be modified in an experience-dependent manner and have been used to condition animals in negative or positive associative paradigms. Experience-dependent non-associative defects in avoidance of aversive odors were reported in Drosophila learning mutants. This prompted an examination of the contribution of the mushroom bodies and inner antenoglomerular tract, the two neuronal populations implicated in processing olfactory information to experience-dependent non-associative osmotactic responses. Silencing inner antenoglomerular tract synapses results in defective osmotaxis after experiencing a different odor, but not electric shock. Conversely, structural or functional perturbation of the mushroom bodies precipitates osmotactic deficits after prior experience of electric shock but not odors. These effects on osmotaxis are specific, long lasting and independent of the aversive or attractive properties of the odors. Deficient osmotactic responses only after electric shock stimulation were exhibited by mutants with altered cAMP levels, but all other mutants in genes preferentially expressed in the mushroom bodies responded normally. Our results suggest that the mushroom bodies and inner antenoglomerular tract are essential for normal osmotactic responses after prior stimulation with electric shock or another odor respectively. Finally, these experience-dependent non-associative paradigms are excellent methods of functionally ascertaining normal activity of the mushroom bodies and inner antenoglomerular tract in putative leaning and memory mutants.