Brian J. Duistermars

Crossmodal Visual Input for Odor Tracking during Fly Flight

Flies generate robust and high-performance olfactory and visual behaviors. Adult fruit flies can distinguish small differences in odor concentration across antennae separated by less than 1 mm [1], and a single olfactory sensory neuron is sufficient for near-normal gradient tracking in larvae [2]. During flight a male housefly chasing a female executes a corrective turn within 40 ms after a course deviation by its target [3]. The challenges imposed by flying apparently benefit from the tight integration of unimodal sensory cues. Crossmodal interactions reduce the discrimination threshold for unimodal memory retrieval by enhancing stimulus salience [4], and dynamic crossmodal processing is required for odor search during free flight because animals fail to locate an odor source in the absence of rich visual feedback [5]. The visual requirements for odor localization are unknown. We tethered a hungry fly in a magnetic field, allowing it to yaw freely, presented odor plumes, and examined how visual cues influence odor tracking. We show that flies are unable to use a small-field object or landmark to assist plume tracking, whereas odor activates wide-field optomotor course control to enable accurate orientation toward an attractive food odor.

The spatial, temporal and contrast properties of expansion and rotation flight optomotor responses in Drosophila.

SUMMARY Fruit flies respond to panoramic retinal patterns of visual expansion with robust steering maneuvers directed away from the focus of expansion to avoid collisions and maintain an upwind flight posture. Panoramic rotation elicits comparatively weak syndirectional steering maneuvers, which also maintain visual stability. Full-field optic flow patterns like expansion and rotation are elicited by distinct flight maneuvers such as body translation during straight flight or body rotation during hovering, respectively. Recent analyses suggest that under some experimental conditions the rotation optomotor response reflects the linear sum of different expansion response components. Are expansion and rotation-mediated visual stabilization responses part of a single optomotor response subserved by a neural circuit that is differentially stimulated by the two flow fields, or rather do the two behavioral responses reflect two distinct control systems? Guided by the principle that the properties of neural circuits are revealed in the behaviors they mediate, we systematically varied the spatial, temporal and contrast properties of expansion and rotation stimuli, and quantified the time course and amplitude of optomotor responses during tethered flight. Our results support the conclusion that expansion and rotation optomotor responses are indeed two separate reflexes, which draw from the same system of elementary motion detectors, but are likely mediated by separate pre-motor circuits having different spatial integration properties, low-pass characteristics and contrast sensitivity.

Mechanisms of odor-tracking: multiple sensors for enhanced perception and behavior

Early in evolution, the ability to sense and respond to changing environments must have provided a critical survival advantage to living organisms. From bacteria and worms to flies and vertebrates, sophisticated mechanisms have evolved to enhance odor detection and localization. Here, we review several modes of chemotaxis. We further consider the relevance of a striking and recurrent motif in the organization of invertebrate and vertebrate sensory systems, namely the existence of two symmetrical olfactory sensors. By combining our current knowledge about the olfactory circuits of larval and adult Drosophila, we examine the molecular and neural mechanisms underlying robust olfactory perception and extend these analyses to recent behavioral studies addressing the relevance and function of bilateral olfactory input for gradient detection. Finally, using a comparative theoretical approach based on Braitenbergs vehicles, we speculate about the relationships between anatomy, circuit architecture and stereotypical orientation behaviors.

Dynamic properties of large-field and small-field optomotor flight responses in Drosophila

Optomotor flight control in houseflies shows bandwidth fractionation such that steering responses to an oscillating large-field rotating panorama peak at low frequency, whereas responses to small-field objects peak at high frequency. In fruit flies, steady-state large-field translation generates steering responses that are three times larger than large-field rotation. Here, we examine the optomotor steering reactions to dynamically oscillating visual stimuli consisting of large-field rotation, large-field expansion, and small-field motion. The results show that, like in larger flies, large-field optomotor steering responses peak at low frequency, whereas small-field responses persist under high frequency conditions. However, in fruit flies large-field expansion elicits higher magnitude and tighter phase-locked optomotor responses than rotation throughout the frequency spectrum, which may suggest a further segregation within the large-field pathway. An analysis of wing beat frequency and amplitude reveals that mechanical power output during flight varies according to the spatial organization and motion dynamics of the visual scene. These results suggest that, like in larger flies, the optomotor control system is organized into parallel large-field and small-field pathways, and extends previous analyses to quantify expansion-sensitivity for steering reflexes and flight power output across the frequency spectrum.

Binocular Interactions Underlying the Classic Optomotor Responses of Flying Flies

In response to imposed course deviations, the optomotor reactions of animals reduce motion blur and facilitate the maintenance of stable body posture. In flies, many anatomical and electrophysiological studies suggest that disparate motion cues stimulating the left and right eyes are not processed in isolation but rather are integrated in the brain to produce a cohesive panoramic percept. To investigate the strength of such inter-ocular interactions and their role in compensatory sensory–motor transformations, we utilize a virtual reality flight simulator to record wing and head optomotor reactions by tethered flying flies in response to imposed binocular rotation and monocular front-to-back and back-to-front motion. Within a narrow range of stimulus parameters that generates large contrast insensitive optomotor responses to binocular rotation, we find that responses to monocular front-to-back motion are larger than those to panoramic rotation, but are contrast sensitive. Conversely, responses to monocular back-to-front motion are slower than those to rotation and peak at the lowest tested contrast. Together our results suggest that optomotor responses to binocular rotation result from the influence of non-additive contralateral inhibitory as well as excitatory circuit interactions that serve to confer contrast insensitivity to flight behaviors influenced by rotatory optic flow.

A Magnetic Tether System to Investigate Visual and Olfactory Mediated Flight Control in Drosophila

It has been clear for many years that insects use visual cues to stabilize their heading in a wind stream. Many animals track odors carried in the wind. As such, visual stabilization of upwind tracking directly aids in odor tracking. But do olfactory signals directly influence visual tracking behavior independently from wind cues? Also, the recent deluge of research on the neurophysiology and neurobehavioral genetics of olfaction in Drosophila has motivated ever more technically sophisticated and quantitative behavioral assays. Here, we modified a magnetic tether system originally devised for vision experiments by equipping the arena with narrow laminar flow odor plumes. A fly is glued to a small steel pin and suspended in a magnetic field that enables it to yaw freely. Small diameter food odor plumes are directed downward over the fly s head, eliciting stable tracking by a hungry fly. Here we focus on the critical mechanics of tethering, aligning the magnets, devising the odor plume, and confirming stable odor tracking.

Visually Mediated Odor Tracking During Flight in Drosophila

Flying insects use visual cues to stabilize their heading in a wind stream. Many animals additionally track odors carried in the wind. As such, visual stabilization of upwind tracking directly aids in odor tracking. But do olfactory signals directly influence visual tracking behavior independently from wind cues? Additionally, recent advances in olfactory molecular genetics and neurophysiology have motivated novel quantitative behavioral analyses to assess the behavioral influence of (e.g.) genetically inactivating specific olfactory activation circuits. We modified a magnetic tether system originally devised for vision experiments by equipping the arena with narrow laminar flow odor plumes. Here we focus on experiments that can be performed after a fly is tethered and is able to navigate in the magnetic arena. We show how to acquire video images optimized for measuring body angle, how to judge stable odor tracking, and we illustrate two experiments to examine the influence of visual cues on odor tracking.