Abstract

Anyone who has tried to enjoy a meal while fending off flies knows how good these pesky creatures are at finding food. But how do they do it — by smell alone, or by sight? In a stunning series of behavioral experiments, Mark Frye, Michael Tarsitano and Michael Dickinson have shown that fruit flies actually need specific visual cues in their surroundings to localize an attractively smelly food source (p. 843).Previous experiments focused on fruit flies' senses of smell and vision independently. A lot was known about the fly's-eye-view of the world and about how their olfactory system works. But researchers knew almost nothing about how flies integrate these senses and how this affects their behavior. So Frye and coworkers set out to perform experiments that tested the effects of visual environments on the free-flight behavior of flies searching for food.In a cylindrical test booth equipped with stereo video cameras, Frye tracked the 3-D flight trajectories of fruit flies. First, he recorded their flight behavior in the empty booth to establish a baseline and then again after a vial of apple cider vinegar was embedded in the floor. With a background of randomly distributed black-and-white squares on the wall, the flies had no trouble finding the source of the odor. But to Frye's surprise,when he changed the background to plain white, the flies generally did not hover near the vinegar. This strongly suggested that the flies needed visual feedback — not from the food itself but from the surrounding environment!Frye then devised a series of tests to find out which features in the flies' visual field were important. He recorded their behaviors in the presence of vinegar with different patterns on the wall: three vertical stripes, more numerous vertical stripes and horizontal stripes. He compared these flight paths with data recorded without the vinegar against all three backgrounds to examine how the animals' flight altitude, approach distance to the wall, and turning behaviors changed as they searched for food in different environments.The results were compelling. With vertical-striped walls, flies had little trouble finding their food. But with horizontal stripes, the flies wandered back and forth as they had in the white-out condition. This led Frye to conclude that flies need to see vertical edges in their surroundings to localize smells.But why should this be? The answer may be related to the flight paths of these insects, says Frye. They primarily fly straight ahead, with little pitching or rolling, and make abrupt yaw turns; so vertical edges appear to move a lot, whereas horizontal edges stand still as the fly flutters about. What's more, trees and plants could provide vertical edges in the flies'natural habitats.`The big picture is figuring out how sensory fusion works,' says Frye. The next step, he explains, is to study the neural mechanisms of flight control by probing the inputs and outputs of various sensory and motor systems to test how they interact to direct the fly. Then perhaps we can get them to leave us alone during dinner.

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