Flying Drosophila stabilize their vision-based velocity controller by sensing wind with their antennae

Abstract

Flies and other insects use vision to regulate their groundspeed in flight, enabling them to fly in varying wind conditions. Compared with mechanosensory modalities, however, vision requires a long processing delay (~100 ms) that might introduce instability if operated at high gain. Flies also sense air motion with their antennae, but how this is used in flight control is unknown. We manipulated the antennal function of fruit flies by ablating their aristae, forcing them to rely on vision alone to regulate groundspeed. Arista-ablated flies in flight exhibited significantly greater groundspeed variability than intact flies. We then subjected them to a series of controlled impulsive wind gusts delivered by an air piston and experimentally manipulated antennae and visual feedback. The results show that an antenna-mediated response alters wing motion to cause flies to accelerate in the same direction as the gust. This response opposes flying into a headwind, but flies regularly fly upwind. To resolve this discrepancy, we obtained a dynamic model of the fly's velocity regulator by fitting parameters of candidate models to our experimental data. The model suggests that the groundspeed variability of arista-ablated flies is the result of unstable feedback oscillations caused by the delay and high gain of visual feedback. The antenna response drives active damping with a shorter delay (~20 ms) to stabilize this regulator, in exchange for increasing the effect of rapid wind disturbances. This provides insight into flies' multimodal sensory feedback architecture and constitutes a previously unknown role for the antennae.stability | sensory fusion | feedback delay | system identification | turbulence A nimals rely on input from multiple sensory modalities to regulate their motor actions. For example, to quickly grasp an object, a human uses both vision and tactile sensing. The visual system can estimate how close the object is, but only touch can accurately determine when contact is made (1). Similarly, flying insects rely on multiple senses, including vision and mechanosensation to control their flight (2). This multimodal feedback enables them to perform aerial feats, such as chasing conspecifics (3) and rapid self-righting after takeoff (4). Our neurobiological and biomechanical understanding of these behaviors is incomplete, but physiological studies and physics-based models have helped reveal salient features (5-9).The flight paths of flies often are structured into bouts of straight segments of forward motion, punctuated by rapid changes in heading termed body saccades (3,(10)(11)(12). During the straight segments, flies tend to maintain constant groundspeed despite changes in wind speed, suggesting the presence of an active feedback regulator (13,14). Recent results provide some insight into the properties of this vision-based forward velocity controller, such as its dependence on the spatial and temporal frequency of the visual stimulus, and the magnitude of the underlying sensory-motor delay (15,16). Experiments w...

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