Aerial course stabilization is impaired in motion-blind flies

Visual motion detection is among the best understood neuronal computations. One assumed behavioural role is to detect self-motion and to counteract involuntary course deviations, extensively investigated in tethered walking or flying flies. In free flight, however, any deviation from a straight course is signalled by both the visual system as well as by proprioceptive mechanoreceptors called halteres, which are the equivalent of the vestibular system in vertebrates. Therefore, it is yet unclear to what extent motion vision contributes to course control, or whether straight flight is completely controlled by proprioceptive feedback from the halteres. To answer these questions, 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 difficulties maintaining a straight flight trajectory, much like control flies in the dark. By unilateral wing clipping, we generated an asymmetry in propulsory 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 unequivocally demonstrate that motion vision is necessary to fly straight under realistic conditions.