Neural Control and Biomechanics of Flight Initiation in Drosophila melanogaster

In response to abrupt visual stimulation, the fruit fly, Drosophila melanogaster, quickly initiates flight. This rapid takeoff is believed to be a reflex coordinated by a pair of large descending interneurons (the "giant fibers"). However, it has been difficult to evoke escapes in wild-type flies, and thus flight initiation behavior in the unrestrained wild-type fly is poorly described. I have taken advantage of recent advances in high-speed videography to capture video sequences of Drosophila flight initiation at the temporal resolution of 6,000 frames per second. A three-dimensional kinematic analysis of takeoff sequences indicates that wing use during the jumping phase of flight initiation is essential for stabilizing flight. During voluntary takeoffs, flies raise their wings prior to leaving the ground, resulting in a stable, controlled takeoff. In contrast, during visually-elicited escapes flies pull their wings down close to their body during the takeoff jump, resulting in tumbling flights that are faster but less steady. The takeoff kinematics suggest that the power delivered by the legs is substantially greater during these escapes than during voluntary takeoffs. Thus, I show that the two types of Drosophila flight initiation result in different flight performances once the fly is airborne, and that these performances are distinguished by a trade-off between speed and stability. I also determined that flies can use visual information to plan a jump directly away from a looming threat. This is surprising, given the simple architecture of the giant fiber pathway thought to mediate escape. I found that approximately 200 ms before takeoff, flies begin a series of postural adjustments that determine the direction of their escape. These movements position their center of mass so that leg extension will push them away from the looming stimulus. These preflight movements are not the result of a simple feed-forward motor program because their magnitude and direction depend on the flies' initial postural state. Furthermore, flies plan a takeoff direction even in instances when they choose not to jump. This sophisticated motor program is evidence for a form of rapid, visually mediated motor planning in a genetically accessible model organism