Abstract
Flies achieve supreme flight maneuverability through a small set of miniscule steering muscles attached to the wing base. The fast flight maneuvers arise from precisely timed activation of the steering muscles and the resulting subtle modulation of the wing stroke. In addition, slower modulation of wing kinematics arises from changes in the activity of indirect flight muscles in the thorax. We investigated if these modulations can be described as a superposition of a limited number of elementary deformations of the wing stroke that are under independent physiological control. Using a high-speed computer vision system, we recorded the wing motion of tethered flying fruit flies for up to 12 000 consecutive wing strokes at a sampling rate of 6250 Hz. We then decomposed the joint motion pattern of both wings into components that had the minimal mutual information (a measure of statistical dependence). In 100 flight segments measured from 10 individual flies, we identified 7 distinct types of frequently occurring least-dependent components, each defining a kinematic pattern (a specific deformation of the wing stroke and the sequence of its activation from cycle to cycle). Two of these stroke deformations can be associated with the control of yaw torque and total flight force, respectively. A third deformation involves a change in the downstroke-to-upstroke duration ratio, which is expected to alter the pitch torque. A fourth kinematic pattern consists in the alteration of stroke amplitude with a period of 2 wingbeat cycles, extending for dozens of cycles. Our analysis indicates that these four elementary kinematic patterns can be activated mutually independently, and occur both in isolation and in linear superposition. The results strengthen the available evidence for independent control of yaw torque, pitch torque, and total flight force. Our computational method facilitates systematic identification of novel patterns in large kinematic datasets.
Highlights
Insect flight provides a powerful model system for neuromotor control [1,2,3]
Our results indicate that changes in yaw torque, pitch torque and total flight force can be controlled mutually independently.The computational method described here provides a novel way to analyze extensive flight recordings, taking advantage of the information inherent in spontaneous variations of the wing stroke kinematics
In the first three subsections, we present important general features of the wing motion decomposition into least-dependent kinematic patterns, illustrated with specific examples
Summary
Flight puts extreme physiological demands on the organism, which are met by specialized adaptations with sharply defined structure-function relations [4] This is apparent in flies, in which the generation of power for wing motion and the control of fast modulations of the wing stroke are mediated by two distinct types of muscles [5,6]. The quantitative correspondence between the kinematic patterns of wing motion and the resulting aerodynamic forces has been clearly established using dynamically scaled robotic models [7,8,9]. This knowledge provides a functional interpretion of observed variations in the fly’s wing kinematics. Our approach combines high-speed measurements of wing motion during extended intervals of unstimulated tethered flight with a computational analysis that extracts independently occurring components of the kinematics
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