Association of visual objects and olfactory cues in Drosophila.

Context-dependent preferences in a choice between an upper and a lower visual object of otherwise identical appearance were recorded during stationary flight of the fruitfly, Drosophila melanogaster, in a flight simulator. The test animal was held in a fixed orientation at the center of a wing-beat processor that converts attempted turns into counter-rotations of a surrounding cylindrical panorama. This allowed the fly to maneuver the preferred object into the actual direction of flight. Single flies were trained to avoid a course toward the visual object that had been associated with the aversive odor benzaldehyde (BAL). Conditioned object avoidance was investigated in different treatment groups by collective evaluation of the scores from 80 long-lasting flights (> 1 hr). In addition to a significant cross-modal association, we found a striking long-term effect of transient exposure to BAL both in the embryonic and larval states. The preimaginal experience significantly increased the indifference to BAL in the adult flies. Disturbed vision does not account for this effect: Neither the perception nor the discrimination of the visual objects was significantly impaired in the investigated flies. Disturbed olfaction could explain the present results. Recently, however, preimaginal BAL uptake has been found to interfere directly with the retention of heat-shock-conditioned object avoidance.