Haltere mechanosensory influence on tethered flight behavior in Drosophila

In flies, mechanosensory information from modified hindwings known as halteres is combined with visual information for wing-steering behavior. Haltere input is necessary for free flight, making it difficult to study the effects of haltere ablation under natural flight conditions. We thus used tethered Drosophila melanogaster flies to examine the relationship between halteres and the visual system, using wide-field motion or moving figures as visual stimuli. Haltere input was altered by surgically decreasing its mass, or by removing it entirely. Haltere removal does not affect the flies' ability to flap or steer their wings, but it does increase the temporal frequency at which they modify their wingbeat amplitude. Reducing the haltere mass decreases the optomotor reflex response to wide-field motion, and removing the haltere entirely does not further decrease the response. Decreasing the mass does not attenuate the response to figure motion, but removing the entire haltere does attenuate the response. When flies are allowed to control a visual stimulus in closed-loop conditions, haltereless flies fixate figures with the same acuity as intact flies, but cannot stabilize a wide-field stimulus as accurately as intact flies can. These manipulations suggest that the haltere mass is influential in wide-field stabilization, but less so in figure tracking. In both figure and wide-field experiments, we observe responses to visual motion with and without halteres, indicating that during tethered flight, intact halteres are not strictly necessary for visually guided wing-steering responses. However, the haltere feedback loop may operate in a context-dependent way to modulate responses to visual motion.