Drosophila haltere steering muscles are active during voluntary maneuvers and are directionally tuned

Abstract

As flies navigate their environment in search of food or mates, they execute sharp turns known as saccades that occur faster than the blink of a human eye. These maneuvers are initiated by changes in visual motion detected by the eyes, whereas their termination is under the control of small, dumbbell-shaped structures called halteres. The halteres are located behind the forewings and evolved from the hindwings. These structures oscillate during flight and function as biological gyroscopes; they detect unexpected body rotations during flight and trigger wing reflex maneuvers. Like the wings, the halteres possess a small set of muscles that control the structure's motion from their base and receive input from the visual system. However, while the critical role of the halteres in stabilizing flight is long known as flies crash catastrophically without them, the role of the haltere and its steering muscles during flight maneuvers remains unclear. Using fluorescence imaging of the genetically encoded calcium sensor GCaMP6f, we observed haltere steering muscle activity in the fruit fly, Drosophila melanogaster, during a broad array of visual stimuli. We found that these muscles are particularly responsive during voluntary escape maneuvers and are tuned to rotations about the body's cardinal axes. These results suggest that the visual system is able to activate individual muscles to control haltere motion, and thus mechanosensory input. With this work, we are beginning to understand how hard-wired reflexes may be modified by the nervous system to produce voluntary behaviors.

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