Free-flight responses of<i>Drosophila melanogaster</i>to attractive odors

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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“…All experiments were performed in a 150 cm × 30 cm × 30 cm wind tunnel (27,28) equipped with a visual projection system (Fig. 1A).…”

Section: Methodsmentioning

confidence: 99%

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

Fuller

Straw

Peek

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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136

131

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“…While the biochemical and physiological bases are less well understood, chemotaxis also plays a crucial role in the navigation of multicellular organisms. The nematode worm C. elegans undergoes chemotaxis in response to a variety of external signals [67] while in insects, the fruit fly Drosophila melanogaster navigates up gradients of attractive odours during food location [10] and male moths follow pheromone gradients released by the female during mate location [47].…”

Section: Introductionmentioning

confidence: 99%

A user’s guide to PDE models for chemotaxis

2008

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Mathematical modelling of chemotaxis (the movement of biological cells or organisms in response to chemical gradients) has developed into a large and diverse discipline, whose aspects include its mechanistic basis, the modelling of specific systems and the mathematical behaviour of the underlying equations. The Keller-Segel model of chemotaxis (Keller and Segel in J Theor Biol 26:399-415, 1970; 30:225-234, 1971) has provided a cornerstone for much of this work, its success being a consequence of its intuitive simplicity, analytical tractability and capacity to replicate key behaviour of chemotactic populations. One such property, the ability to display "auto-aggregation", has led to its prominence as a mechanism for self-organisation of biological systems. This phenomenon has been shown to lead to finite-time blow-up under certain formulations of the model, and a large body of work has been devoted to determining when blow-up occurs or whether globally existing solutions exist. In this paper, we explore in detail a number of variations of the original Keller-Segel model. We review their formulation from a biological perspective, contrast their patterning properties, summarise key results on their analytical properties and classify their solution form. We conclude with a brief discussion and expand on some of the outstanding issues revealed as a result of this work.

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“…Following take-off, the odor signal mediates upwind oriented flight and guides the insect towards the source (Budick and Dickinson 2006;Chow and Frye 2008).…”

Section: Introductionmentioning

confidence: 99%

“…Wind tunnels have been employed to investigate odor-mediated upwind flight behavior in D. melanogaster (Budick and Dickinson 2006), but have, with the exception of the pheromone compound cis-vaccenyl acetate (Bartelt et al 1985), not been used to identify behavior-modifying chemicals. We have set up a wind tunnel to study long-range attraction in relation to odor quality and the internal physiological state of the flies.…”

Section: Introductionmentioning

confidence: 99%