Gaze characteristics of freely walking blowflies in a goal-directed task

Abstract

In contrast to flying flies, walking flies experience relatively strong rotational gaze shifts, even during overall straight phases of locomotion. These gaze shifts are caused by the walking apparatus and modulated by the stride frequency. Accordingly, even during straight walking phases, the retinal image flow is composed of both translational and rotational optic flow, which might affect spatial vision, as well as fixation behavior. We addressed this issue for an orientation task where walking blowflies approached a black vertical bar. The visual stimulus was stationary, or either the bar or the background moved horizontally. The stride-coupled gaze shifts of flies walking toward the bar had similar amplitudes under all visual conditions tested. This finding indicates that these shifts are an inherent feature of walking, which are not even compensated during a visual goal fixation task. By contrast, approaching flies showed a frequent stop-and-go behavior that was affected by the stimulus conditions. As sustained image rotations may impair distance estimation during walking, we propose a hypothesis that explains how rotation-independent translatory image flow containing distance information can be determined. The algorithm proposed works without requiring differentiation at the behavioral level of the rotational and translational flow components. By contrast, disentangling both has been proposed to be necessary during flight. By comparing the retinal velocities of the edges of the goal, its rotational image motion component can be removed. Consequently, the expansion velocity of the goal and, thus, its proximity can be extracted, irrespective of distance-independent stride-coupled rotational image shifts.

Head roll stabilisation in the nocturnal bull ant Myrmecia pyriformis: Implications for visual navigation

“…This head roll oscillation has the same frequency as the stride cycle and is reminiscent of the yaw head oscillations of approximately 4 deg that were recently described in the walking blowfly Calliphora vicina (Kress and Egelhaaf, 2014). Retinal image shifts that are due to the alternating tripod gait have also been described in predatory tiger beetles Cicindela tranquebarica, who run after their prey using visual guidance and adapt their stride cycle to compensate for the imposed oscillation of their gait when turning towards their prey (Haselsteiner et al, 2014).…”

“…As animals move, they experience complex retinal image shifts (e.g. Eckert and Zeil, 2001; Kress and Egelhaaf, 2014;Schilstra and van Hateren, 1998;Srinivasan and Bernard, 1975). Image motion generated by pure translation provides useful information on heading direction and on the relative distance of objects (Collett et al, 1993), but image motion signals generated by rotation degrade the quality of that visual information (reviewed in Zeil et al, 2008).…”

Saccadic body turns in walking Drosophila

“…The active movement of the head during these saccades was analyzed with varying results (Land, 1973 ; Geiger and Poggio, 1977 ), but could be clarified by high-speed observations in freely flying insects (Schilstra and van Hateren, 1998 ): The head rotates relatively to the body, reducing the saccade duration even further. The role of head body coordination in walking insects is gaining new momentum (Ribak et al, 2009 ; Kress and Egelhaaf, 2012 , 2014a ) and questions the information content of the optic flow obtained during walking (Kress and Egelhaaf, 2014b ). Nonetheless optic flow has been shown to allow walking Drosophila to estimate distances of up to 80 times the length of its body (Schuster et al, 2002 ).…”

Head orientation of walking blowflies is controlled by visual and mechanical cues

“…A vertical bar made of red cardboard (6.5×58 cm) and of the same height as the arena walls was attached to the wall as a target for the blowflies, as walking flies have previously been shown to be attracted by dark vertical bars (Bülthoff et al, 1982;Kress and Egelhaaf, 2014). Both the stripes and the bar provide highcontrast cues, as blowfly photoreceptors are insensitive in the long-wavelength range (Bernard and Stavenga, 1979).…”