Proprioceptive feedback determines visuomotor gain in Drosophila

Abstract

Multisensory integration is a prerequisite for effective locomotor control in most animals. Especially the impressive aerial performance of insects relies on rapid and precise integration of multiple sensory modalities that provide feedback on different time scales. In flies, continuous visual signalling from the compound eyes is fused with phasic proprioceptive feedback to ensure precise neural activation of wing steering muscles within narrow temporal phase bands of the stroke cycle. This phase-locked activation relies on mechanoreceptors distributed over wings and gyroscopic halteres. Here we investigate visual steering performance of tethered flying fruit flies with reduced haltere and wing feedback signalling. Using a flight simulator, we evaluated visual object fixation behaviour, optomotor altitude control, and saccadic escape reflexes. The behavioural assays show an antagonistic effect of wing and haltere signalling on visuomotor gain during flight. Compared to controls, suppression of haltere feedback attenuates while suppression of wing feedback enhances the animals wing steering range. Our results suggest that the generation of motor commands owing to visual perception is dynamically controlled by proprioception. We outline a potential physiological mechanism based on the biomechanical properties of wing steering muscles and sensory integration processes at the level of motoneurons. Collectively, the findings contribute to our general understanding how moving animals integrate sensory information with dynamically changing temporal structure.