Crossmodal Visual Input for Odor Tracking during Fly Flight

Duistermars, Brian J.; Frye, Mark A.

doi:10.1016/j.cub.2008.01.027

Cited by 60 publications

(72 citation statements)

References 37 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…1). Under normal flight conditions, flies depend upon visual feedback to localize the source of an odor during flight (Frye et al, 2003), which they use to maintain flight heading in a plume (Duistermars and Frye, 2008). Here we demonstrate an olfaction-dependent increase in the gain of yaw optomotor transformations and a decrease in the gain of sideslip transformations (Figs.…”

Section: Discussionmentioning

confidence: 99%

An Olfactory Circuit Increases the Fidelity of Visual Behavior

Chow¹,

Theobald²,

Frye³

2011

J. Neurosci.

View full text Add to dashboard Cite

Multimodal integration allows neural circuits to be activated in a behaviorally context-specific manner. In the case of odor plume tracking by Drosophila, an attractive odorant increases the influence of yaw-optic flow on steering behavior in flight, which enhances visual stability reflexes, resulting in straighter flight trajectories within an odor plume. However, it is not well understood whether contextspecific changes in optomotor behavior are the result of an increased sensitivity to motion inputs (e.g., through increased visual attention) or direct scaling of motor outputs (i.e., increased steering gain). We address this question by examining the optomotor behavior of Drosophila melanogaster in a tethered flight assay and demonstrate that whereas olfactory cues decrease the gain of the optomotor response to sideslip optic flow, they concomitantly increase the gain of the yaw optomotor response by enhancing the animal's ability to follow transient visual perturbations. Furthermore, ablating the mushroom bodies (MBs) of the fly brain via larval hydroxyurea (HU) treatment results in a loss of olfaction-dependent increase in yaw optomotor fidelity. By expressing either tetanus toxin light chain or diphtheria toxin in gal4-defined neural circuits, we were able to replicate the loss of function observed in the HU treatment within the lines expressing broadly in the mushroom bodies, but not within specific mushroom body lobes. Finally, we were able to genetically separate the yaw responses and sideslip responses in our behavioral assay. Together, our results implicate the MBs in a fast-acting, memoryindependent olfactory modification of a visual reflex that is critical for flight control.

show abstract

Section: Discussionmentioning

confidence: 99%

An Olfactory Circuit Increases the Fidelity of Visual Behavior

Chow¹,

Theobald²,

Frye³

2011

J. Neurosci.

View full text Add to dashboard Cite

show abstract

“…Closed-loop experiments with this method are more challenging but might alter the response dynamics by putting the fly in an alternative behavioral state. Finally, our experimental conditions were designed specifically to isolate optomotor responses from other important sensory inputs such as mechanosensory feedback from the halteres and odor signals from the antennae, which strongly influence the dynamics of wing-beat-mediated equilibrium responses (Sherman and Dickinson, 2004;Duistermars and Frye, 2008). During free flight these additional inputs certainly interact with the visual dynamical wing beat response.…”

Section: Impulse Response Estimates For Optomotor Behaviormentioning

confidence: 99%

Dynamics of optomotor responses in Drosophila to perturbations in optic flow

Theobald

Ringach

Frye

2010

Journal of Experimental Biology

Self Cite

View full text Add to dashboard Cite

SUMMARYFor a small flying insect, correcting unplanned course perturbations is essential for navigating through the world. Visual course control relies on estimating optic flow patterns which, in flies, are encoded by interneurons of the third optic ganglion. However, the rules that translate optic flow into flight motor commands remain poorly understood. Here, we measured the temporal dynamics of optomotor responses in tethered flies to optic flow fields about three cardinal axes. For each condition, we used white noise analysis to determine the optimal linear filters linking optic flow to the sum and difference of left and right wing beat amplitudes. The estimated filters indicate that flies react very quickly to perturbations of the motion field, with pure delays in the order of ~20 ms and time-to-peak of ~100 ms. By convolution the filters also predict responses to arbitrary stimulus sequences, accounting for over half the variance in 5 of our 6 stimulus types, demonstrating the approximate linearity of the system with respect to optic flow variables. In the remaining case of yaw optic flow we improved predictability by measuring individual flies, which also allowed us to analyze the variability of optomotor responses within a population. Finally, the linear filters at least partly explain the optomotor responses to superimposed and decomposed compound flow fields. Supplementary material available online at

show abstract

“…The combination of reduced saccadic reorientations and spatial gradient evaluation biases overall flight orientation towards either the plume (steering 'up' the gradient) or the anti-plume (steering 'down' the gradient). This demonstrates that the animal actively tracks the local minimum of aversive BA intensity in a manner qualitatively identical to tracking the local maximum of attractive vinegar intensity (Duistermars and Frye, 2008a;Duistermars et al, 2009). There was no difference between the mean plume acquisition time or probability in the presence of an attractive or aversive stimulus (Fig.3C,D), further evidence that flies are as adept at locating and orienting away from an aversive odor source as orienting towards an attractive odor source, even at low concentrations of BA.…”

Section: Flies Use the Same Sensorimotor Transformations To Dynamicalmentioning

confidence: 74%

“…visual conditions) similarly impacts active tracking of an attractive and aversive odorant (Fig.5). Previous work from our laboratory and others has demonstrated that flies integrate visual and olfactory stimuli to track appetitive odor plumes in flight (Chow and Frye, 2008;Frye and Duistermars, 2009;Chow et al, 2011;Krishnan et al, 2011), and that saccade amplitude and frequency represent independent control parameters (Wolf and Heisenberg, 1990;Tammero and Dickinson, 2002;Bender and Dickinson, 2006), which are themselves influenced by odor (Duistermars and Frye, 2008a). …”

Section: Flies Use the Same Sensorimotor Transformations To Dynamicalmentioning

confidence: 96%

“…The olfactory magnetic tether arena has been previously described in detail (Duistermars and Frye, 2008b;Duistermars and Frye, 2008a;Maimon et al, 2008;Frye and Duistermars, 2009;Krishnan et al, 2011). Briefly, adult female flies 3-6days post-eclosion were cold-anesthetized and tethered to minutien pins (Fine Science Tools, item no.…”

Section: Magnetic Tether Flight Simulator and Odor Deliverymentioning

confidence: 99%

See 1 more Smart Citation

Flies dynamically anti-track, rather than ballistically escape, aversive odor during flight

Wasserman

Aptekar

et al. 2012

Journal of Experimental Biology

Self Cite

View full text Add to dashboard Cite

SUMMARYTracking distant odor sources is crucial to foraging, courtship and reproductive success for many animals including fish, flies and birds. Upon encountering a chemical plume in flight, Drosophila melanogaster integrates the spatial intensity gradient and temporal fluctuations over the two antennae, while simultaneously reducing the amplitude and frequency of rapid steering maneuvers, stabilizing the flight vector. There are infinite escape vectors away from a noxious source, in contrast to a single best tracking vector towards an attractive source. Attractive and aversive odors are segregated into parallel neuronal pathways in flies; therefore, the behavioral algorithms for avoidance may be categorically different from tracking. Do flies plot random ballistic or otherwise variable escape vectors? Or do they instead make use of temporally dynamic mechanisms for continuously and directly avoiding noxious odors in a manner similar to tracking appetitive ones? We examine this question using a magnetic tether flight simulator that permits free yaw movements, such that flies can actively orient within spatially defined odor plumes. We show that in-flight aversive flight behavior shares all of the key features of attraction such that flies continuously ʻanti-trackʼ the noxious source.

show abstract

Crossmodal Visual Input for Odor Tracking during Fly Flight

Cited by 60 publications

References 37 publications

An Olfactory Circuit Increases the Fidelity of Visual Behavior

An Olfactory Circuit Increases the Fidelity of Visual Behavior

Dynamics of optomotor responses in Drosophila to perturbations in optic flow

Flies dynamically anti-track, rather than ballistically escape, aversive odor during flight

Contact Info

Product

Resources

About