Mechanisms underlying attraction to odors in walking Drosophila

Mechanisms that control movements range from navigational mechanisms, in which the animal employs directional cues to reach a specific destination, to search movements during which there are little or no environmental cues. Even though most real-world movements result from an interplay between these mechanisms, an experimental system and theoretical framework for the study of interplay of these mechanisms is not available. Here, we rectify this deficit. We create a new method to stimulate the olfactory system in Drosophila or fruit flies. As flies explore a circular arena, their olfactory receptor neuron (ORNs) are optogenetically activated within a central region making this region attractive to the flies without emitting any clear directional signals outside this central region. In the absence of ORN activation, the fly’s locomotion can be described by a random walk model where a fly’s movement is described by its speed and turn-rate (or kinematics). Upon optogenetic stimulation, the fly’s behavior changes dramatically in two respects. First, there are large kinematic changes. Second, there are more turns at the border between light-zone and no-light-zone and these turns have an inward bias. Surprisingly, there is no increase in turn-rate, rather a large decrease in speed that makes it appear that the flies are turning at the border. Similarly, the inward bias of the turns is a result of the increase in turn angle. These two mechanisms entirely account for the change in a fly’s locomotion. No complex mechanisms such as path-integration or a careful evaluation of gradients are necessary.Author summary: The strategy an animal employs to explore the environment and to find and return to the location where it has previously found food or mates is an important part of its behavior. In nature, animals have incomplete information about their environment, and must use this incomplete information to navigate. In most laboratory experiments, there is usually clear directional information making it difficult to infer an animal’s real strategy from laboratory behavioral experiments. In this study, we devise a new behavioral task wherein we remotely activate olfactory neurons when fruit flies are in a given location. This activation makes a given location attractive to the flies without providing any directional information and allows us to assess how flies navigate under these conditions. We find that flies navigate towards the activated location using two simple mechanisms: First, its speed in the activated region and its turn rate is much lower than it is elsewhere. Second, at the boundary of the odor-zone, its speed decreases dramatically and its turns become much sharper. Essentially, these simple mechanisms appear to be extremely robust.