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Published February 15, 2013 | Published
Journal Article Open

Visual motion speed determines a behavioral switch from forward flight to expansion avoidance in Drosophila


As an animal translates through the world, its eyes will experience a radiating pattern of optic flow in which there is a focus of expansion directly in front and a focus of contraction behind. For flying fruit flies, recent experiments indicate that flies actively steer away from patterns of expansion. Whereas such a reflex makes sense for avoiding obstacles, it presents a paradox of sorts because an insect could not navigate stably through a visual scene unless it tolerated flight towards a focus of expansion during episodes of forward translation. One possible solution to this paradox is that a fly's behavior might change such that it steers away from strong expansion, but actively steers towards weak expansion. In this study, we use a tethered flight arena to investigate the influence of stimulus strength on the magnitude and direction of turning responses to visual expansion in flies. These experiments indicate that the expansion-avoidance behavior is speed dependent. At slower speeds of expansion, flies exhibit an attraction to the focus of expansion, whereas the behavior transforms to expansion avoidance at higher speeds. Open-loop experiments indicate that this inversion of the expansion-avoidance response depends on whether or not the head is fixed to the thorax. The inversion of the expansion-avoidance response with stimulus strength has a clear manifestation under closed-loop conditions. Flies will actively orient towards a focus of expansion at low temporal frequency but steer away from it at high temporal frequency. The change in the response with temporal frequency does not require motion stimuli directly in front or behind the fly. Animals in which the stimulus was presented within 120 deg sectors on each side consistently steered towards expansion at low temporal frequency and steered towards contraction at high temporal frequency. A simple model based on an array of Hassenstein–Reichardt type elementary movement detectors suggests that the inversion of the expansion-avoidance reflex can explain the spatial distribution of straight flight segments and collision-avoidance saccades when flies fly freely within an open circular arena.

Additional Information

© 2013 Published by The Company of Biologists Ltd. Received 4 May 2012; Accepted 26 October 2012. We thank Dr Mark Frye and members of the Dickinson lab for constructive feedback throughout the development of this project. This work was supported by the Institute for Collaborative Biotechnologies through grant DAAD 19-03-D-0004 from the US Army Research Office, by the National Science Foundation (NSF) through award 0623527 to M.H.D. and by the Center for Neuromorphic Systems Engineering (CNSE) Engineering Research Center at Caltech through NSF award EEC-9402726.

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August 19, 2023
August 19, 2023