When searching for food, fruit flies explore their landscape using a series of straight flight paths interspersed with rapid turns termed saccades (Fig. 1A). These rapid turns were first rigorously characterized by Collet and Land in hoverflies (Collett and Land, 1975
), but are exhibited by many dipteran species. During each saccade, a fruit fly changes heading by approximately 90° in 50 msec, completing the maneuver in about 10 wing strokes (Tammero and Dickinson, 2002b). When flying within a circular arena in the laboratory, the saccade rate is so regular that one is tempted to propose that each turn is triggered by an internal clock within the animal's brain. However, experiments suggest that each saccade is initiated by a specific sensory stimulus that the fly encounters as it flies through the air. By carefully tracking the flies within an arena lined with a printed visual pattern, it is possible to crudely reconstruct what the animal sees just prior to each saccade (Tammero and Dickinson, 2002b). Such an analysis suggests that flies turn away from visual expansion as they near obstacles. This behavior appears to represent a binary decision in that a fly either turns to the left or right, but does not adjust the magnitude of the turn depending on the strength of the visual stimulus. This feature of the behavior is most clearly seen when a fly flies directly through the center of the arena toward the opposite wall. Under these conditions the fly does not, as one might expect, exhibit a 180° turn, but rather makes the "choice" to turn 90° to either the left or right with equal probability (Fig. 1B, C). However, although the choice appears binary there is nevertheless enormous variance in the magnitude of the turn. Given that the neurons controlling this rapid behavior have only time enough to fire a few action potentials, the variability might arise from internal noise within flight control circuitry. However, it is also possible that the variance in saccade angle does represent an active modulation of motor output in response to features of the sensory input that have yet to be identified.
There are, however, several uncertainties in reconstructing the visual stimuli that trigger saccades based on free flight data. For example, the angular position of the body and head are not known and must be inferred from the animal's flight path. A more precise map of the visual reflexes may be reconstructed by performing experiment on tethered animals flying within an electronic arena (Fig. 1D). The flight arena consists of an optical wingbeat analyzer that tracks the amplitude and frequency of the two wings and a cylindrical electronic visual display that presents moving visual patterns to the fly (Götz, 1987; Lehmann and Dickinson, 1997). The flight arena works in either open-loop configuration, in which one measures the fly's behavioral response to a set of visual stimuli, or in closed-loop configuration, in which the fly itself can control the visual display by altering its pattern of wing motion—a simple form of "virtual reality." A convenient closed-loop experiment is the so-called fixation paradigm, in which a fly is permitted to control the azimuthal velocity of a narrow stripe or square by adjusting the relative stroke amplitude of its wings (Götz, 1987). Under such conditions, a fly will actively steer towards the object, maintaining it in the front field of view. To study the expansion response, the fly is allowed to fixate a small square in the presence of an oscillating bias (the equivalent of an electronic "cross wind") which makes the task more difficult (Tammero and Dickinson, 2002a). At random intervals the square is programmed to rapidly expand, thereby eliciting flight control reflexes. If the square expands to the animal's left, the left wingstroke amplitude transiently increases and the right wingstroke decreases. The opposite occurs if the expansion takes place on the animal's right. As discussed later, such changes in wing motion would have the aerodynamic effect of turning the animal away from the expanding stimulus. The results are consistent with free flight studies, and suggest that the saccade trigger circuitry might consist of a simple bilateral pair of expansion-detector circuits within the visual system. The tethered flight experiments also reveal that flies rapidly extend their legs and elevate wing beat frequency in response to frontal expansion—a reflex that is known as the landing response (Borst, 1990). Thus, the net behavioral response to visual expansion can be explained by three expansion detectors (one for the landing response, two for bilateral collision avoidance responses), each driving independent motor pathways. However, the terms "collision avoidance" and "landing response," though convenient, ascribe specific functions to these behaviors that have yet to be definitively demonstrated. It is possible, for example, that the kinematic changes during a landing response would actually cause an animal to pitch up and hover as it approaches an object. This ambiguity exemplifies the difficulty of predicting free flight behaviors from tethered flight responses.
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