Discovering the flight autostabilizer of fruit flies by inducing aerial stumbles

Abstract

Just as the Wright brothers implemented controls to achieve stable airplane flight, flying insects have evolved behavioral strategies that ensure recovery from flight disturbances. Pioneering studies performed on tethered and dissected insects demonstrate that the sensory, neurological, and musculoskeletal systems play important roles in flight control. Such studies, however, cannot produce an integrative model of insect flight stability because they do not incorporate the interaction of these systems with free-flight aerodynamics. We directly investigate control and stability through the application of torque impulses to freely flying fruit flies (Drosophila melanogaster) and measurement of their behavioral response. High-speed video and a new motion tracking method capture the aerial "stumble," and we discover that flies respond to gentle disturbances by accurately returning to their original orientation. These insects take advantage of a stabilizing aerodynamic influence and active torque generation to recover their heading to within 2°in <60 ms. To explain this recovery behavior, we form a feedback control model that includes the fly's ability to sense body rotations, process this information, and actuate the wing motions that generate corrective aerodynamic torque. Thus, like early man-made aircraft and modern fighter jets, the fruit fly employs an automatic stabilization scheme that reacts to short time-scale disturbances.flight control | insect flight | stability | perturbation | fruit fly L ocomotion through natural environments demands mechanisms that maintain stability in the face of unpredictable disturbances. Behavioral strategies play a particularly important role in controlling the flight of insects (1-7), because even gentle air currents can cause large disruptions to the intended flight path. Insects must also contend with the intrinsic instability of flapping flight (8, 9) and the large fluctuations in aerodynamic forces caused by slight variations in wing motions (10, 11). Corrective behavior often takes advantage of vision (1, 2). For fruit flies, however, reaction time to visual stimuli is at least 10 wingbeats (12), so these insects must employ faster sensory circuits to recover from short time-scale disturbances and instabilities. To probe this fast control strategy, we devised an experimental method that imposes impulsive mechanical disturbances (6, 13) to flying insects while allowing us to measure relevant aspects of flight behavior. We first glue tiny ferromagnetic pins to fruit flies and image their free flight using three orthogonally oriented highspeed video cameras (Methods and SI Text). When a fly enters the filming volume, an optical trigger detects the insect, initiates recording, and activates a pair of Helmholtz coils that produce a magnetic field. The field and pin are both oriented horizontally, so the resulting torque on the pin reorients the yaw, or heading angle, of the insect (Fig. 1). We then use a new motion tracking technique to extract the three-dimensional body and w...

Controlling roll perturbations in fruit flies

“…Second, we find that Dr increases linearly with maximum roll velocity (figure 6d). Collectively, these data suggest that, as with yaw [39], the response to roll perturbations is well described by a reduced order model of a linear PI controller with time delay.…”

“…Although the control mechanisms for body roll and yaw [39] are mathematically equivalent, there are substantial rsif.royalsocietypublishing.org J. R. Soc. Interface 12: 20150075 differences between these two degrees of freedom and the fly's response to perturbations along these angles.…”

“…As indicated by the flight trajectory, while the fly fully corrected its roll angle with T c ¼ 6.5 wing-beats, deflections of 88 in yaw and 158 in the direction of the body velocity persisted until the end of the measurement. From previous experiments [39], we know that a yaw-only perturbation of 308 should have been corrected within 14 wing-beats to 28 accuracy. In the current experiment, however, larger residual deflections ('error') in yaw and the velocity heading persist long after 14 wing-beats (see label in figure 7a).…”

“…In each experiment, approximately 15 prepared flies were released in a transparent cubic chamber of side length 13 cm, equipped with two Helmholtz coils that are used to generate a vertical magnetic field (inner diameter 10 cm, outer diameter 12 cm, copper wire diameter 0.8 mm and 240 turns) [39,46]. Three synchronized fast cameras (Phantom v. 7.1, Vision Research) were focused on a cubic filming volume at the centre of the chamber.…”

“…More recently, free-flight experiments used vortices [1 -3] and impulsive gusts [4] to perturb insects, highlighting the sensitivity of the roll angle to perturbations. Understanding roll control, however, requires fast and accurate quantitative measurements of wing and body kinematics in response to controlled mid-air perturbation impulses-a methodology recently applied to study yaw control [39]. Crucially, these previous works typically consider only the linear response [30,39 -45].…”