A model of visual–olfactory integration for odour localisation in free-flying fruit flies

Abstract

. Although rather less is known about flight responses to olfactory stimuli, it has been established that the sudden onset of an attractive odour results in increased forward velocity and a suppression of turning (Frye and Dickinson, Accepted 21 February 2010 SUMMARY Flying fruit flies (Drosophila melanogaster) locate a concealed appetitive odour source most accurately in environments containing vertical visual contrasts. To investigate how visuomotor and olfactory responses may be integrated, we examine the free-flight behaviour of flies in three visual conditions, with and without food odour present. While odour localisation is facilitated by uniformly distributed vertical contrast as compared with purely horizontal contrast, localised vertical contrast also facilitates odour localisation, but only if the odour source is situated close to it. We implement a model of visuomotor control consisting of three parallel subsystems: an optomotor response stabilising the model fly's yaw orientation; a collision avoidance system to saccade away from looming obstacles; and a speed regulation system. This model reproduces many of the behaviours we observe in flies, including visually mediated 'rebound' turns following saccades. Using recordings of real odour plumes, we simulate the presence of an odorant in the arena, and investigate ways in which the olfactory input could modulate visuomotor control. We reproduce the experimental results by using the change in odour intensity to regulate the sensitivity of collision avoidance, resulting in visually mediated chemokinesis. Additionally, it is necessary to amplify the optomotor response whenever odour is present, increasing the model fly's tendency to steer towards features of the visual environment. We conclude that visual and olfactory responses of Drosophila are not independent, but that relatively simple interaction between these modalities can account for the observed visual dependence of odour source localisation. Supplementary material available online at

Visual motion speed determines a behavioral switch from forward flight to expansion avoidance inDrosophila

“…We note that this model does not require an explicit estimate of either distance to the wall or the speed of visual motion but only the magnitude and spatial structure of the EMD response. Moreover, it predicts that the animals should tolerate some left-right asymmetry in the EMD response from both eyes, which is in contrast to the classical optomotor equilibrium model (Götz, 1968) but is consistent with free flight results, where the animals rarely fly down the center of the arena (Tammero and Dickinson, 2002;Stewart et al, 2010). Another prediction of the model is that free-flight collision-avoidance is not initiated by expansion per se but rather by only the magnitude and location of the progressive (front-to-back) component of the visual motion.…”

“…This is further evidence suggesting that during much of Drosophila behavior the motion-detecting system is operating at output levels well below those corresponding to stimulation at the TFO. While Drosophila are clearly capable of flight speeds above 23cms -1 (David, 1978;Budick and Dickinson, 2006), these flight speeds are reduced in the presence of a highly textured visual surround (Tammero and Dickinson, 2002;Stewart et al, 2010). Therefore, it is unlikely that during faster flight a fly would encounter visual motion that is considerably stronger than in the simulations of Fig.6D-F.…”

“…The peak responses of the EMD array during flight segments that are within the strong stimulus (super-threshold) zone (gray ring in Fig.6D) exceed the range that corresponds to simulated open-loop responses for stimuli within the critical value of the expansion response (depicted by the violet bands in Fig.6E). This finding suggests that the expansionattraction response is required to explain the free flight data (Tammero and Dickinson, 2002;Stewart et al, 2010), and probably accounts for the weak centering tendency observed between saccades, where flies were found to turn slightly away from the closer side of the arena [ fig.8 of Tammero and Dickinson (Tammero and Dickinson, 2002)]. An inspection of the EMD responses in Fig.6E suggests that the proposed sensitivity of the expansion attraction response to lateral retinal positions (see Fig.5) is plainly sensible because very little motion is seen by frontal eye regions during forward flight, whereas the lateral regions exhibit the asymmetry that occurs during non-centered flight.…”

“…The most appropriate free-flight data collected under controlled visual conditions that can serve as a 'ground truth' for the simulation results is presented by Tammero and Dickinson (Tammero and Dickinson, 2002), with similar experiments performed by Stewart and co-workers (Stewart et al, 2010). In the Tammero and Dickinson (Tammero and Dickinson, 2002) study, flies were tracked flying within a 1m diameter cylinder, while the walls of the environment were covered with a randomized checkerboard pattern (each square of the checkerboard covered a 5deg×5deg patch when viewed from the center and was either black or white with 50% probability).…”

Flying Drosophila stabilize their vision-based velocity controller by sensing wind with their antennae

“…This multimodal feedback enables them to perform aerial feats, such as chasing conspecifics (3) and rapid self-righting after takeoff (4). Our neurobiological and biomechanical understanding of these behaviors is incomplete, but physiological studies and physics-based models have helped reveal salient features (5)(6)(7)(8)(9).…”