Elementary sensory-motor transformations underlying olfactory navigation in walking fruit-flies

Álvarez-Salvado, Efrén; Licata, Angela M.; Connor, Erin; McHugh, Margaret K.; King, Benjamin M.N.; Stavropoulos, Nicholas; Victor, Jonathan D.; Crimaldi, John P.; Nagel, Katherine I.

doi:10.7554/elife.37815

Cited by 116 publications

(180 citation statements)

References 82 publications

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“…This decrease is consistent with recent work in flying Drosophila that analyzed changes in a fly's behavior when odors were presented in the context of visual objects [31]. In other experiments, there is an increase in speed upon odor encounter [26,[43][44][45]. An elegant explanation for this difference is that flies slow down if they expect to encounter an odor object, and move faster if they expect the object to be far away [31].…”

Section: Discussionsupporting

confidence: 88%

“…This consistency is not just a matter of detail; it reflects a fundamental feature of search movements because it implies that the fly's behavior unfolds in chunks of tens of steps during which the fly uses the same speed and curvature. This chunking implies that flies would make fewer decisions per unit time than implied in continuous-time models employed by others [26]. Because the flies are making fewer decisions per unit time, there will be greater variability between different instances of tracks generated from the same underlying model, and this contributes to the observed inter-individual variability [37].…”

Section: Discussionmentioning

confidence: 99%

“…One mechanism suggested by Kennedy for odor-tracking in moths [46], and subsequently also considered to be important in other insects [47,48], is the automatic internally stored counter-turning which is released when the odor concentration decreases and brings the insect back into the odor plume. Another mechanism, in contrast to counter-turning, is a direct increase in turning in response to decrease in odor concentration [26]. Both mechanisms depend on increased turn rate.…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, even animals with simple brains such as C. elegans and Drosophila larvae respond to odors with strategies that are orienting [24,25]. Adult Drosophila responding to odors show both non oriented changes in behavior [26,27], and are also capable of using orienting sensory cues such as wind [26,28] to navigate to an odor source. Flies can also employ path integration to return to the location of food [29,30].…”

Section: Introductionmentioning

confidence: 99%

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Mechanisms underlying attraction to odors in walking Drosophila

2020

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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.

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Section: Discussionsupporting

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Mechanisms underlying attraction to odors in walking Drosophila

2020

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“…An alternative strategy would be to make an odor intensity judgement that gates a response to positional information from non-olfactory cues, such as wind direction, visual landmarks, or self-motion. This computation would be reminiscent of the odor-gated visual and mechanosensory behaviors observed in insects (Álvarez Salvado et al 2018;van Breugel and Dickinson 2014;Kennedy and Marsh 1974). To distinguish between these possible strategies, we tested mice in sessions interleaving the air dilution ratios 90:30 and 30:10.…”

Section: Mice Can Use Gradient Cues In Turbulent Flowmentioning

confidence: 99%

Sniff-synchronized, gradient-guided olfactory search by freely moving mice

Findley

Wyrick

Cramer

et al. 2020

Preprint

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For many organisms, searching for relevant targets such as food or mates entails active, strategic sampling of the environment. Finding odorous targets may be the most ancient search problem that motile organisms evolved to solve. While chemosensory navigation has been well characterized in micro-organisms and invertebrates, spatial olfaction in vertebrates is poorly understood. We have established an olfactory search assay in which freely-moving mice navigate noisy concentration gradients of airborne odor. Mice solve this task using concentration gradient cues and do not require stereo olfaction for performance. During task performance, respiration and nose movement are synchronized with tens of milliseconds precision. This synchrony is present during trials and largely absent during inter-trial intervals, suggesting that sniff-synchronized nose movement is a strategic behavioral state rather than simply a constant accompaniment to fast breathing. To investigate the spatiotemporal structure of these active sensing movements, we used machine learning methods to parse motion trajectories into elementary movement motifs. Motifs fall into two clusters, which correspond to investigation and approach states. Investigation motifs lock precisely to sniffing, such that the individual motifs preferentially occur at specific phases of the sniff cycle. This work clarifies sensorimotor strategies for mouse olfactory search and guides ongoing work into the underlying neural mechanisms. Bhattacharyya U, Singh Bhalla U. Robust and rapid air borne odor tracking without casting. eNeuro. 2015 11; 2(6):Eneuro.0102-15. doi: 10.1523/ENEURO.0102-15.2015. Bi S, Sourjik V. Stimulus sensing and signal processing in bacterial chemotaxis.

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Design of Polymer Carriers for Optimized Pheromone Release in Sustainable Insect Control Strategies

Hellmann,

Greiner,

Vilcinskas

2023

Advanced Science

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Semiochemicals such as pheromones play a major role in communication between insects, influencing their spatial orientation, aggregation, defense, and mating. The rational chemical design of precision pheromone‐releasing materials are increased the efficiency of pheromone‐based plant protection agents. Decades of research is begun to unravel the complex communication structures regulated by semiochemicals, from the neuronal perception of specific chemical substances to the behavioral responses in hundreds of species, including many devastating pest insects. This article summarizes the most effective uses of semiochemicals in agriculture, the behavioral responses of selected target species, and controlled‐release strategies based on formulations such as novel fibrous polymer carriers. This study helps scientists, decision‐makers, farmers, and the public understand the importance of appropriate mating disruption techniques that reduce the need for broad‐spectrum insecticides and limit their impact on non‐target and beneficial insects.

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Elementary sensory-motor transformations underlying olfactory navigation in walking fruit-flies

Cited by 116 publications

References 82 publications

Mechanisms underlying attraction to odors in walking Drosophila

Mechanisms underlying attraction to odors in walking Drosophila

Sniff-synchronized, gradient-guided olfactory search by freely moving mice

Design of Polymer Carriers for Optimized Pheromone Release in Sustainable Insect Control Strategies

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