Flies tune the sensitivity of their multifunctional gyroscope

Locomotion requires navigating unpredictable and complex environments, demanding both stability and maneuverability within short timeframes. This is particularly important for flying insects, and the true flies (Diptera) stand out among this group for their impressive flight capabilities. Flies’ aerial abilities are partially attributed to halteres, tiny club-shaped structures that evolved from the hindwings and play a crucial role in flight control. Halteres oscillate during flight, in antiphase with the wings, providing rhythmic input to the wing steering system via arrays of embedded mechanosensors called campaniform sensilla. These sensor arrays convey timing information to the wing steering muscles, but linking haltere sensor location to sensor activity and the functional organization of the wing steering system remains a central challenge. Here, we use in vivo calcium imaging during tethered flight to obtain population-level recordings of the haltere sensory afferents in specific fields of sensilla. We find that haltere feedback is continuously modulated by visual stimuli to stabilize flight. Additionally, this feedback is present during saccades and help flies actively maneuver. We also find that the haltere’s multifaceted role arises from the steering muscles of the haltere itself, regulating haltere stroke amplitude to modulate campaniform activity. Taken together, our results underscore the crucial role of biomechanics in regulating the dynamic range of sensors and provide insight into how the sensory and motor systems of flies coevolved.