Smelling on the fly: sensory cues and strategies for olfactory navigation in Drosophila

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Navigating toward (or away from) a remote odor source is a challenging problem that requires integrating olfactory information with visual and mechanosensory cues. Drosophila melanogaster is a useful organism for studying the neural mechanisms of these navigation behaviors. There are a wealth of genetic tools in this organism, as well as a history of inventive behavioral experiments. There is also a large and growing literature in Drosophila on the neural coding of olfactory, visual, and mechanosensory stimuli. Here we review recent progress in understanding how these stimulus modalities are encoded in the Drosophila nervous system. We also discuss what strategies a fly might use to navigate in a natural olfactory landscape while making use of all these sources of sensory information. We emphasize that Drosophila are likely to switch between multiple strategies for olfactory navigation, depending on the availability of various sensory cues. Finally, we highlight future research directions that will be important in understanding the neural circuits that underlie these behaviors.

Highlights

► Chemotaxis requires integrating olfactory, visual, and mechanosensory cues. ► Drosophila is a useful model for understanding the neural mechanisms of chemotaxis. ► The neural codes for all these sensory cues are being elucidated in Drosophila. ► The optimal strategy for integrating these cues depends on environmental context. ► A future challenge is to understand multimodal integration and strategy selection.

Introduction

Chemical cues can signal the presence of food, a mate, a competitor, a predator, or a hazard. Thus, chemotaxis  defined as movement toward (or away from) a source of chemical cues  is central to the ecology of most animals. However, chemotaxis is not a purely olfactory behavior. Because an odor may be encountered far downwind from its source, navigation may also depend on information about wind direction and the visual environment. Thus, chemotaxis involves integrating information across sensory modalities. This makes chemotaxis an interesting case study for understanding how the nervous system combines information from multiple sources.

Importantly, the optimal strategy for finding a chemical source may change as the environment changes. To take an obvious example, visual cues may be useful in the daytime but less useful at night. This makes chemotaxis an interesting behavior from the perspective of understanding how the nervous system selects a particular program of action among different alternatives.

In this review, we will focus on chemotaxis in Drosophila melanogaster (here called ‘the fly’, with apologies to other flies). D. melanogaster is an attractive model system for linking neural coding to behavior. Most notably, it is possible to make in vivo physiological recordings in this organism from single neurons within genetically identified populations [1, 2].

We will begin by describing the strategies that flies and other insects use for chemotaxis. Next, we will discuss how the fly nervous system encodes olfactory information important for chemotaxis. Then, we will briefly discuss the roles of visual and mechanosensory cues in chemotaxis. Finally, we will discuss situations in which flies are likely to switch between chemotaxis strategies. We will neglect the topic of chemotaxis in Drosophila larvae, which is reviewed elsewhere in this issue [3]. Some of the topics we discuss have been previously reviewed with a different focus [4, 5].

Section snippets

Chemotaxis strategies and the olfactory landscape

Insects have been shown to use multiple strategies to navigate toward odors. One strategy depends on measuring instantaneous concentration differences between two spatially separated odor sensors, and turning toward the side of the higher concentration (‘osmotropotaxis’). This behavior can be observed in tethered Drosophila walking on a spherical treadmill. The fly is exposed to two air streams having different odor concentrations, each directed at one antenna. Under these conditions, flies

Neural encoding of odor cues

Thanks to recent advances in genetics and physiology, much is now known about how odor stimuli are encoded in the Drosophila brain. A key problem in odor encoding is maintaining sensitivity over a wide range of concentrations. Near an odor source, the instantaneous concentration of an odor can approach saturated vapor, especially at low air speeds. At the same time, the fly olfactory system can also detect very low odor concentrations: peripheral and central neurons have been identified that

Visual contributions to chemotaxis

Insects often rely heavily on visual cues for chemotaxis, particularly in flight. An important visual cue is large-scale optic flow, produced when the fly moves relative to the ground  either under its own power, or when displaced by wind. Optic flow provides the most reliable information about groundspeed [4, 46, 47]. Optic flow can also provide information about wind direction. If an insect is flying straight upwind, it perceives optic flow purely along its longitudinal axis, but if the fly

Mechanosensory contributions to chemotaxis

Although flying flies are thought to rely mainly on vision for determining wind direction, wind can also be sensed using the antennae. Each antenna contains a mechanosensitive structure known as Johnston's organ (JO) [59]. A feather-like structure on the antenna (called the arista) acts as a sail which makes the antenna sensitive to small air velocities. The arista also confers direction-selectivity on JO, because air velocity vectors that are perpendicular to the arista are most effective at

Switching between navigation strategies

Because natural olfactory environments are complex and constantly changing, flies are likely to use multiple sensory cues to navigate toward attractive odors. Which strategy is most useful depends on which cues are available. For instance, if spatial concentration gradients of an odor are not sufficiently steep to support osmotropotaxis, flies may rely more on the statistics of temporal fluctuations or on wind direction. Conversely, if temporal fluctuations are minimal (near the ground, for

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

Acknowledgements

We are grateful to Allison E. Baker, Elizabeth J. Hong, and Brendan P. Lehnert for useful comments on the manuscript. R.I.W. is supported by a research project grant from the NIH (R01 DC008174) and an HHMI Early Career Scientist Award.

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