The spatial, temporal and contrast properties of expansion and rotation flight optomotor responses inDrosophila

Abstract

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.

Elementary Motion Detection

“…Qualitatively, the behavioral data are quite similar to the electrophysiological tuning curve acquired in LPTCs (Borst and Bahde, 1987;Duistermars et al, 2007;Fry et al, 2009;Hausen and Wehrhahn, 1989;Joesch et al, 2008;Schnell et al, 2010). However, studies in Drosophila revealed a discrepancy between the electrophysiologically-measured temporal frequency tuning curve in lobula plate tangential cells recorded in fixed flies and the behaviorally-observed optomotor response ( fig.…”

“…4.2 a & b). Whereas tuning properties of single cells showed an optimum around 1 Hz (Joesch et al, 2008;, behavioral analyses revealed an optimal response of 1-4 Hz for walking (Buchner, 1984;Goetz and Wenking, 1973) and 4-10 Hz for flying flies (Duistermars et al, 2007). A similar observation can be made from work on Calliphora vicina, although the data are less clear ( fig.…”

“…As predicted by the model, the optomotor response clearly shows a strong dependence on the temporal frequency and hence on particular pattern characteristics (Borst and Bahde, 1987;Duistermars et al, 2007). The measurement of flight speed is supposed to be independent of the pattern size (Fry et al, 2009;Srinivasan et al, 1991).…”

Neural correlates of illusory motion perception in Drosophila

“…For example, standard and reverse-optomotor responses persisted even when the spatial extent of the stimulus was reduced to a narrow window (Fig. S1), and responses to translational (23,24) standard and reverse-phi stimuli were similar to responses to rotation stimuli in directionality and temporal tuning (Fig. S2).…”

Bio-inspired visual ego-rotation sensor for MAVs

“…For walking Drosophila optima from 2 to 3 Hz have been shown (Götz and Wenking 1973;Chiappe et al 2010). In flying animals, optima have been reported between 3 and 10 Hz for Drosophila (Duistermars et al 2007;Fry et al 2009), 1 to 10 Hz for Musca (Borst and Bahde 1987) and 5 to 7 Hz for Calliphora (Hausen and Wehrhahn 1989;Jung et al 2011). We chose to adjust the filter time constants to values yielding a theoretical frequency optimum similar to Calliphora during flight, i.e., at 7.3 Hz (τ lp = 45 ms and τ hp = 33 ms).…”