RSS 2009
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Michael Dickinson

Visually-Mediated Behaviors of the Fruit Fly
Michael Dickinson

Abstract

The fruit fly, Drosophila melanogaster, suffers a rather poor reputation as a pesky lab rat, better known for its rapid breeding chromosome number than for its behavioral repertoire. Independent of their utility as model genetic organisms, however, fruit flies are also noted as the result of an extraordinary evolutionary radiation. The genus Drosophila is one of the most species-rich genera in the animal kingdom. Fruit flies would be better termed fungus flies, as they make a living on fungus that grows on rotting plant and animal matter. As larvae, these animals grow quickly within yeast- and bacteria-rich rots; as adults, they navigate through their habitat guided by the sensory cues that signal the location of suitable sites for feeding, shelter, mating, and oviposition.

The research in my laboratory focuses on the sensory ethology of fruit flies, treating these tiny insects not simply as convenient laboratory models, but as real animals that have evolved a successful life history pattern. The goal of this work is to try to deconstruct the animal's behavior into a sequence of sensory-motor modules. Although these insects make use of many sensory modalities as they explore their environment, vision plays an essential role in nearly all aspects of their life history. My talk will focus on several visually-mediated components of behavior including take-off, navigation, predator avoidance, landing, and local exploration, as well as components of social behavior that ensue whenever two or more flies alight on the same piece of rotting fruit.

Long distance search starts with take-off, a behavior that is less stereotyped than previously supposed. Hungry flies launch themselves smoothly in the presence of an attractive odor, and do so by carefully coordinating a gentle leg jump with the start of wing flapping. Flies escaping a looming threat, in contrast, jump with greater force - often before they have finished raising their wings. Although the escape takes place within tens of milliseconds, the animal computes the azimuthal position of the visual threat and jumps in the opposite direction. This directionality is achieved by careful placement of the legs prior to the jump - a rudimentary form of pre-motor planning.

Once in the air, flies use a variety of visuomotor reflexes to navigate, including object fixation, velocity control, expansion avoidance, and rotatory optomotor equilibrium. My laboratory has attempted to characterize these different behaviors through a combination of free- and tethered-flight experiments. The results suggest that the gross flight behavior of flies - sequences of straight flight interspersed with rapid turns called body saccades - arises from the combination of these concurrently-running visuomotor modules.

Fruit flies do not exhibit the complex mating chases exhibited by other species, but they still must fly toward safe landmarks while avoiding small targets that represent predators or other potentially harmful objects. Flies appear to make this behavioral choice - whether to fly toward an object or steer away from it - using a relatively simple visually-mediated algorithm. Fruit flies are attracted to long vertically-oriented objects (i.e. stripes), whereas they actively avoid objects that subtend a narrow vertical angle (i.e. spots).

Once a fly lands - another behavior mediated in large part by visual reflexes - it uses an array of visuomotor behaviors to explore its local environs. Because fruit fly social behavior takes place on the ground, the visually-mediated behaviors that operate while walking and standing are even more varied and complicated than those that take place in the air. Using new technology to track the trajectories of individual flies as they explore and interact within large controlled arenas, my lab is beginning to identify and quantify these new suites of visuomotor behaviors.

In summary, by systematically dissecting the entire life history of Drosophila, we hope to provide a richer view of the visual system's role in behavior.