Abstract
Visual motion detection is among the best understood neuronal computations. As extensively investigated in tethered flies, visual motion signals are assumed to be crucial to detect and counteract involuntary course deviations. During free flight, however, course changes are also signalled by other sensory systems. Therefore, it is as yet unclear to what extent motion vision contributes to course control. To address this question, we genetically rendered flies motion-blind by blocking their primary motion-sensitive neurons and quantified their free-flight performance. We found that such flies have difficulty maintaining a straight flight trajectory, much like unimpaired flies in the dark. By unilateral wing clipping, we generated an asymmetry in propulsive force and tested the ability of flies to compensate for this perturbation. While wild-type flies showed a remarkable level of compensation, motion-blind animals exhibited pronounced circling behaviour. Our results therefore directly confirm that motion vision is necessary to fly straight under realistic conditions.
Highlights
The execution of coordinated muscle contractions underlying locomotion is inherently imprecise and requires continuous adjustments based on sensory feedback (Taylor and Krapp, 2007; Rossignol et al, 2006; Dickinson, 2014; Tuthill and Azim, 2018)
In agreement with previous accounts, recorded trajectories consisted of straight segments interspersed by sharp turns, so-called body saccades, which have been observed during free flight of different fly species (Collett and Land, 1975; Mronz and Lehmann, 2008; Schilstra and van Hateren, 1999; Tammero and Dickinson, 2002; Egelhaaf et al, 2012) (Fig. 1B–D)
It has long been recognized that motion vision is suitable to subserve various ethological functions
Summary
The execution of coordinated muscle contractions underlying locomotion is inherently imprecise and requires continuous adjustments based on sensory feedback (Taylor and Krapp, 2007; Rossignol et al, 2006; Dickinson, 2014; Tuthill and Azim, 2018). Vision is well suited to keep animals on track as any self-motion evokes characteristic image movements across the eye, termed optic flow (Gibson, 1950; Koenderink and van Doorn, 1987). Optic flow allows moving animals to detect and counteract involuntary course deviations. This is perhaps most relevant during flight, where locomotor trajectories need to be controlled fast and in three spatial dimensions to avoid detrimental collisions (Egelhaaf, 2013). Flies are among the most agile flying animals, performing minute coordinated changes in various aspects of wing motion to control course (Muijres et al, 2017). A great demand on stabilizing sensory feedback is expected (Egelhaaf, 2013; Dickinson and Muijres, 2016).
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