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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.

All animals use olfactory information to perform tasks essential to their survival. Odors typically activate multiple olfactory receptor neuron (ORN) classes and are therefore represented by the patterns of active ORNs. How the patterns of active ORN classes are decoded to drive behavior is under intense investigation. In this study, using Drosophila as a model system, we investigate the logic by which odors modulate locomotion. We designed a novel behavioral arena in which we could examine a fly’s locomotion under precisely controlled stimulus condition. In this arena, in response to similarly attractive odors, flies modulate their locomotion differently implying that odors have a more diverse effect on locomotion than was anticipated. Three features underlie odor-guided locomotion: First, in response to odors, flies modulate a surprisingly large number of motor parameters. Second, similarly attractive odors elicit changes in different motor programs. Third, different ORN classes modulate different subset of motor parameters. DOI: http://dx.doi.org/10.7554/eLife.11092.001, eLife digest Humans rely chiefly on vision to understand and navigate the world around them. But for many organisms, the world is dominated by their sense of smell. For these animals, everyday activities, like finding food, depend on being able to change behavior based on odor-based cues. To meet the challenges of detecting and discriminating between different odors, animals have many odorant receptors that bind to the odors, which are found on olfactory receptor neurons (ORNs). Each odor activates multiple ORNs, and different odors activate different combinations of ORNs. But it is not clear how activities from different classes of ORN are combined to create the perception of an odor or to guide behavior. Now, Jung et al. have investigated the logic by which odors can alter a fruit fly’s movements. The olfactory system of the fruit fly is organized along similar lines to that of a mammal, but is much simpler. Moreover, many genetic tools are available in fruit flies to allow neuroscientists to activate and inactivate specific neurons and assess the effect this has on behavior. The results suggest that odor-guided movement in fruit flies has two noteworthy features. Firstly, in the presence of odors, flies alter their walking in unexpectedly large number of ways. Therefore, one needs to consider many different factors, or “motor parameters”, to describe how odors affect a fly’s movement. For instance, instead of just walking faster or slower, a fly can change how long it stops (stop duration), how long it runs (run duration) and how fast it runs (run speed) – all of which will affect overall speed. Secondly, a single class of ORN can strongly affect some parameters (like run duration) without affecting others (like stop duration). These data indicate that the neural circuits involved have a modular organization in which each ORN class affects a subset of motor parameters, and each motor parameter is affected by a subset of ORN classes. These findings were largely unexpected. Jung et al.’s study focused on attractive odors. Future work will study repulsive odors to investigate if similar results are seen when studying repulsion versus attraction. DOI: http://dx.doi.org/10.7554/eLife.11092.002

SUMMARY Freely flying Drosophila melanogaster respond to odors by increasing their flight speed and turning upwind. Both these flight behaviors can be recapitulated in a tethered fly, which permits the odor stimulus to be precisely controlled. In this study, we investigated the relationship between these behaviors and odor-evoked activity in primary sensory neurons. First, we verified that these behaviors are abolished by mutations that silence olfactory receptor neurons (ORNs). We also found that antennal mechanosensors in Johnston's organ are required to guide upwind turns. Flight responses to an odor depend on the identity of the ORNs that are active, meaning that these behaviors involve odor discrimination and not just odor detection. Flight modulation can begin rapidly (within about 85 ms) after the onset of olfactory transduction. Moreover, just a handful of spikes in a single ORN type is sufficient to trigger these behaviors. Finally, we found that the upwind turn is triggered independently from the increase in wingbeat frequency, implying that ORN signals diverge to activate two independent and parallel motor commands. Together, our results show that odor-evoked flight modulations are rapid and sensitive responses to specific patterns of sensory neuron activity. This makes these behaviors a useful paradigm for studying the relationship between sensory neuron activity and behavioral decision-making in a simple and genetically tractable organism.

Here we describe several fundamental principles of olfactory processing in the Drosophila melanogaster antennal lobe (the analog of the vertebrate olfactory bulb), through the systematic analysis of input and output spike trains of seven identified glomeruli. Repeated presentations of the same odor elicit more reproducible responses in second-order projection neurons (PNs) than in their presynaptic olfactory receptor neurons (ORNs). PN responses rise and accommodate rapidly, emphasizing odor onset. Furthermore, weak ORN inputs are amplified in the PN layer but strong inputs are not. This nonlinear transformation broadens PN tuning and produces more uniform distances between odor representations in PN coding space. In addition, portions of the odor response profile of a PN are not systematically related to their direct ORN inputs, which probably indicates the presence of lateral connections between glomeruli. Finally, we show that a linear discriminator classifies odors more accurately using PN spike trains than using an equivalent number of ORN spike trains.

Signaling by heterotrimeric GTP-binding proteins (G proteins) drives numerous cellular processes. The number of G protein molecules activated by a single membrane receptor is a determinant of signal amplification, although in most cases this parameter remains unknown. In retinal rod photoreceptors, a long-lived photoisomerized rhodopsin molecule activates many G protein molecules (transducins), yielding substantial amplification and a large elementary (single-photon) response, before rhodopsin activity is terminated. Here we report that the elementary response in olfactory transduction is extremely small. A ligand-bound odorant receptor has a low probability of activating even one G protein molecule because the odorant dwell-time is very brief. Thus, signal amplification in olfactory transduction appears fundamentally different from that of phototransduction.