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Evolution has shaped nervous systems to produce stereotyped behavioural responses to ethologically relevant stimuli. For example when laying eggs, female Drosophila avoid geosmin, an odorant produced by toxic moulds. Here we identify second, third, and fourth order neurons required for this innate olfactory aversion. Connectomics data place these neurons in a complete synaptic circuit from sensory input to descending output. We find multiple levels of valence-specific convergence, including a novel form of axo-axonic input onto second order neurons conveying another danger signal, the pheromone of parasitoid wasps. However, we also observe extensive divergence: second order geosmin neurons connect with a diverse array of 80 third order cell types. We find a pattern of convergence of aversive odour channels at this level. Crossing one more synaptic layer, we identified descending neurons critical for egg-laying aversion. Our data suggest a transition from a labelled line organisation in the periphery to a highly distributed central brain representation that is then coupled to distinct descending pathways.

SummaryA 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.

We have approached the problem of reverse-engineering the flight control mechanism of the fruit fly by studying the dynamics of the responses to a visual stimulus during takeoff. Building upon a prior framework [G. Card and M. Dickinson, J. Exp. Biol., vol. 211, pp. 341-353, 2008], we seek to understand the strategies employed by the animal to stabilize attitude and orientation during these evasive, highly dynamical maneuvers. As a first step, we consider the dynamics from a gray-box perspective: examining lumped forces produced by the insect's legs and wings. The reconstruction of the flight initiation dynamics, based on the unconstrained motion formulation for a rigid body, allows us to assess the fly's responses to a variety of initial conditions induced by its jump. Such assessment permits refinement by using a visual tracking algorithm to extract the kinematic envelope of the wings [E. I. Fontaine, F. Zabala, M. Dickinson, and J. Burdick, "Wing and body motion during flight initiation in Drosophila revealed by automated visual tracking," submitted for publication] in order to estimate lift and drag forces [F. Zabala, M. Dickinson, and R. Murray, "Control and stability of insect flight during highly dynamical maneuvers," submitted for publication], and recording actual leg-joint kinematics and using them to estimate jump forces [F. Zabala, "A bio-inspired model for directionality control of flight initiation," to be published.]. In this paper, we present the details of our approach in a comprehensive manner, including the salient results.

SUMMARYThe fruit fly Drosophila melanogaster performs at least two distinct types of flight initiation. One kind is a stereotyped escape response to a visual stimulus that is mediated by the hard-wired giant fiber neural pathway, and the other is a more variable `voluntary' response that can be performed without giant fiber activation. Because the simpler escape take-offs are apparently successful, it is unclear why the fly has multiple pathways to coordinate flight initiation. In this study we use high-speed videography to observe flight initiation in unrestrained wild-type flies and assess the flight performance of each of the two types of take-off. Three-dimensional kinematic analysis of take-off sequences indicates that wing use during the jumping phase of flight initiation is essential for stabilizing flight. During voluntary take-offs, early wing elevation leads to a slower and more stable take-off. In contrast, during visually elicited escapes, the wings are pulled down close to the body during take-off, resulting in tumbling flights in which the fly translates faster but also rotates rapidly about all three of its body axes. Additionally, we find evidence that the power delivered by the legs is substantially greater during visually elicited escapes than during voluntary take-offs. Thus, we find that the two types of Drosophila flight initiation result in different flight performances once the fly is airborne,and that these performances are distinguished by a trade-off between speed and stability.