For a fruit fly, locating fermenting fruit where it can feed, find mates, and lay eggs is an essential and difficult task requiring the integration of olfactory and visual cues. Here, we develop an ...approach to correlate flies’ free-flight behavior with their olfactory experience under different wind and visual conditions, yielding new insight into plume tracking based on over 70 hr of data.
To localize an odor source, flies exhibit three iterative, independent, reflex-driven behaviors, which remain constant through repeated encounters of the same stimulus: (1) 190 ± 75 ms after encountering a plume, flies increase their flight speed and turn upwind, using visual cues to determine wind direction. Due to this substantial response delay, flies pass through the plume shortly after entering it. (2) 450 ± 165 ms after losing the plume, flies initiate a series of vertical and horizontal casts, using visual cues to maintain a crosswind heading. (3) After sensing an attractive odor, flies exhibit an enhanced attraction to small visual features, which increases their probability of finding the plume’s source.
Due to plume structure and sensory-motor delays, a fly’s olfactory experience during foraging flights consists of short bursts of odor stimulation. As a consequence, delays in the onset of crosswind casting and the increased attraction to visual features are necessary behavioral components for efficiently locating an odor source. Our results provide a quantitative behavioral background for elucidating the neural basis of plume tracking using genetic and physiological approaches.
•Flies’ odor sensation is largely determined by self-motion•Flies surge upwind using visual cues 190 ± 75 ms after encountering attractive odors•Flies cast crosswind using visual feedback 450 ± 165 ms after odor plume loss•Perception of an attractive odor increases saliency of high-contrast features
Fruit flies locate food in flight by tracking odor plumes to their source with a simple iterative, visually guided algorithm that helps them orient their heading with respect to the wind direction. After sensing an odor, flies explore visual features in order to pinpoint the source.
All moving animals, including flies 1–3, sharks 4, and humans 5, experience a dynamic sensory landscape that is a function of both their trajectory through space and the distribution of stimuli in ...the environment. This is particularly apparent for mosquitoes, which use a combination of olfactory, visual, and thermal cues to locate hosts 6–10. Mosquitoes are thought to detect suitable hosts by the presence of a sparse CO2 plume, which they track by surging upwind and casting crosswind 11. Upon approach, local cues such as heat and skin volatiles help them identify a landing site 12–15. Recent evidence suggests that thermal attraction is gated by the presence of CO2 6, although this conclusion was based experiments in which the actual flight trajectories of the animals were unknown and visual cues were not studied. Using a three-dimensional tracking system, we show that rather than gating heat sensing, the detection of CO2 actually activates a strong attraction to visual features. This visual reflex guides the mosquitoes to potential hosts where they are close enough to detect thermal cues. By experimentally decoupling the olfactory, visual, and thermal cues, we show that the motor reactions to these stimuli are independently controlled. Given that humans become visible to mosquitoes at a distance of 5–15 m 16, visual cues play a critical intermediate role in host localization by coupling long-range plume tracking to behaviors that require short-range cues. Rather than direct neural coupling, the separate sensory-motor reflexes are linked as a result of the interaction between the animal’s reactions and the spatial structure of the stimuli in the environment.
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•A mosquito’s perception of CO2 triggers a strong attraction to visual features•A mosquito’s attraction to thermal targets is independent of the presence of CO2•Olfaction, vision, and heat trigger independent host-seeking behavioral modules•Interactions among behavioral modules underlie multimodal sensory integration
To find human hosts, mosquitoes must integrate sensory cues that are separated in space and time. To solve this challenge, van Breugel et al. show that mosquitoes respond to exhaled CO2 by exploring visual features they otherwise ignore. This guides them to potential hosts, where they use cues such as heat and humidity to locate a landing site.
After discovering a small drop of food, hungry flies exhibit a peculiar behavior in which they repeatedly stray from, but then return to, the newly discovered resource. To study this behavior in more ...detail, we tracked hungry Drosophila as they explored a large arena, focusing on the question of how flies remain near the food. To determine whether flies use external stimuli, we individually eliminated visual, olfactory, and pheromonal cues. In all cases, flies still exhibited a centralized search behavior, suggesting that none of these cues are absolutely required for navigation back to the food. To simultaneously eliminate visual and olfactory cues associated with the position of the food, we constructed an apparatus in which the food could be rapidly translated from the center of the arena. Flies continued to search around the original location, even after the food was moved to a new position. A random search model based on measured locomotor statistics could not reproduce the centered nature of the animal’s trajectory. We conclude that this behavior is best explained by a form of path integration in which the flies use idiothetic cues to search near the location of the food. We argue that the use of path integration to perform a centered local search is not a specialization of Drosophila but rather represents an ancient behavioral mode that is homologous to the more elaborate foraging strategies of central place foragers such as ants.
•After finding a small drop of food, hungry fruit flies execute local search behavior•The flies’ ability to return to the food does not require vision or a sense of smell•The local search is a form of path integration that relies on internal cues•Flies share the capacity for path integration with other insects such as desert ants
After finding a small patch of food, hungry flies exhibit a local search behavior in which they repeatedly loop away from, but then return to, the food. The study by Kim and Dickinson demonstrates that this local search behavior is a form of path integration, homologous to sophisticated foraging strategies of other insects such as desert ants.
The aerodynamic performance of hovering insects is largely explained by the presence of a stably attached leading edge vortex (LEV) on top of their wings. Although LEVs have been visualized on real, ...physically modeled, and simulated insects, the physical mechanisms responsible for their stability are poorly understood. To gain fundamental insight into LEV stability on flapping fly wings we expressed the Navier-Stokes equations in a rotating frame of reference attached to the wing's surface. Using these equations we show that LEV dynamics on flapping wings are governed by three terms: angular, centripetal and Coriolis acceleration. Our analysis for hovering conditions shows that angular acceleration is proportional to the inverse of dimensionless stroke amplitude, whereas Coriolis and centripetal acceleration are proportional to the inverse of the Rossby number. Using a dynamically scaled robot model of a flapping fruit fly wing to systematically vary these dimensionless numbers, we determined which of the three accelerations mediate LEV stability. Our force measurements and flow visualizations indicate that the LEV is stabilized by the ;quasi-steady' centripetal and Coriolis accelerations that are present at low Rossby number and result from the propeller-like sweep of the wing. In contrast, the unsteady angular acceleration that results from the back and forth motion of a flapping wing does not appear to play a role in the stable attachment of the LEV. Angular acceleration is, however, critical for LEV integrity as we found it can mediate LEV spiral bursting, a high Reynolds number effect. Our analysis and experiments further suggest that the mechanism responsible for LEV stability is not dependent on Reynolds number, at least over the range most relevant for insect flight (100<Re<14,000). LEVs are stable and continue to augment force even when they burst. These and similar findings for propellers and wind turbines at much higher Reynolds numbers suggest that even large flying animals could potentially exploit LEV-based force augmentation during slow hovering flight, take-offs or landing. We calculated the Rossby number from single-wing aspect ratios of over 300 insects, birds, bats, autorotating seeds, and pectoral fins of fish. We found that, on average, wings and fins have a Rossby number close to that of flies (Ro=3). Theoretically, many of these animals should therefore be able to generate a stable LEV, a prediction that is supported by recent findings for several insects, one bat, one bird and one fish. This suggests that force augmentation through stably attached (leading edge) vortices could represent a convergent solution for the generation of high fluid forces over a quite large range in size.
Activity-dependent modulation of sensory systems has been documented in many organisms and is likely to be essential for appropriate processing of information during different behavioral states. ...However, the mechanisms underlying these phenomena remain poorly characterized.
We investigated the role of octopamine neurons in the flight-dependent modulation observed in visual interneurons in Drosophila. The vertical system (VS) cells exhibit a boost in their response to visual motion during flight compared to quiescence. Pharmacological application of octopamine evokes responses in quiescent flies that mimic those observed during flight, and octopamine cells that project to the optic lobes increase in activity during flight. Using genetic tools to manipulate the activity of octopamine neurons, we find that they are both necessary and sufficient for the flight-induced visual boost.
This study provides the first evidence that endogenous release of octopamine is involved in state-dependent modulation of visual interneurons in flies.
► Exogenously applied octopamine mimics flight effects in VS cells ► Octopamine neurons increase in activity during flight ► Octopamine neurons are necessary and sufficient to induce visual gain boost in VS cells
Most experiments on the flight behavior of Drosophila melanogaster have been performed within confined laboratory chambers, yet the natural history of these animals involves dispersal that takes ...place on a much larger spatial scale. Thirty years ago, a group of population geneticists performed a series of mark-and-recapture experiments on Drosophila flies, which demonstrated that even cosmopolitan species are capable of covering 10 km of open desert, probably in just a few hours and without the possibility of feeding along the way. In this review I revisit these fascinating and informative experiments and attempt to explain how-from takeoff to landing-the flies might have made these journeys based on our current knowledge of flight behavior. This exercise provides insight into how animals generate long behavioral sequences using sensory-motor modules that may have an ancient evolutionary origin.
A key feature of reactive behaviors is the ability to spatially localize a salient stimulus and act accordingly. Such sensory-motor transformations must be particularly fast and well tuned in escape ...behaviors, in which both the speed and accuracy of the evasive response determine whether an animal successfully avoids predation
1. We studied the escape behavior of the fruit fly,
Drosophila, and found that flies can use visual information to plan a jump directly away from a looming threat. This is surprising, given the architecture of the pathway thought to mediate escape
2, 3. Using high-speed videography, we found that approximately 200 ms before takeoff, flies begin a series of postural adjustments that determine the direction of their escape. These movements position their center of mass so that leg extension will push them away from the expanding visual stimulus. These preflight movements are not the result of a simple feed-forward motor program because their magnitude and direction depend on the flies' initial postural state. Furthermore, flies plan a takeoff direction even in instances when they choose not to jump. This sophisticated motor program is evidence for a form of rapid, visually mediated motor planning in a genetically accessible model organism.
Although anatomy is often the first step in assigning functions to neural structures, it is not always clear whether architecturally distinct regions of the brain correspond to operational units. ...Whereas neuroarchitecture remains relatively static, functional connectivity may change almost instantaneously according to behavioral context. We imaged panneuronal responses to visual stimuli in a highly conserved central brain region in the fruit fly, Drosophila, during flight. In one substructure, the fan-shaped body, automated analysis revealed three layers that were unresponsive in quiescent flies but became responsive to visual stimuli when the animal was flying. The responses of these regions to a broad suite of visual stimuli suggest that they are involved in the regulation of flight heading. To identify the cell types that underlie these responses, we imaged activity in sets of genetically defined neurons with arborizations in the targeted layers. The responses of this collection during flight also segregated into three sets, confirming the existence of three layers, and they collectively accounted for the panneuronal activity. Our results provide an atlas of flight-gated visual responses in a central brain circuit.
In most animals, the brain controls the body via a set of descending neurons (DNs) that traverse the neck. DN activity activates, maintains or modulates locomotion and other behaviors. Individual DNs ...have been well-studied in species from insects to primates, but little is known about overall connectivity patterns across the DN population. We systematically investigated DN anatomy in
and created over 100 transgenic lines targeting individual cell types. We identified roughly half of all
DNs and comprehensively map connectivity between sensory and motor neuropils in the brain and nerve cord, respectively. We find the nerve cord is a layered system of neuropils reflecting the fly's capability for two largely independent means of locomotion -- walking and flight -- using distinct sets of appendages. Our results reveal the basic functional map of descending pathways in flies and provide tools for systematic interrogation of neural circuits.
We present a camera-based method for automatically quantifying the individual and social behaviors of fruit flies, Drosophila melanogaster, interacting in a planar arena. Our system includes ...machine-vision algorithms that accurately track many individuals without swapping identities and classification algorithms that detect behaviors. The data may be represented as an ethogram that plots the time course of behaviors exhibited by each fly or as a vector that concisely captures the statistical properties of all behaviors displayed in a given period. We found that behavioral differences between individuals were consistent over time and were sufficient to accurately predict gender and genotype. In addition, we found that the relative positions of flies during social interactions vary according to gender, genotype and social environment. We expect that our software, which permits high-throughput screening, will complement existing molecular methods available in Drosophila, facilitating new investigations into the genetic and cellular basis of behavior.
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