Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster

Flies display a sophisticated suite of aerial behaviours that require rapid sensory-motor processing. Like all insects, flight control in flies is med iated in part by motion-sensitive visual interneurons that project to steer ing motor circuitry within the thorax. Flies, however, possess a unique fli ght control equilibrium sense that is encoded by mechanoreceptors at the ba se of the halteres, small dumb-bell-shaped organs derived through evolution ary transformation of the hind wings. To study the input of the haltere sys tem onto the flight control system, I constructed a mechanically oscillatin g flight arena consisting of a cylindrical array of light-emitting diodes t hat generated the moving image of a 30 degrees vertical stripe. The arena p rovided closed-loop visual feedback to elicit fixation behaviour, an orient ation response in which flies maintain the position of the stripe in the fr ont portion of their visual field by actively adjusting their wing kinemati cs. While flies orientate towards the stripe, the entire arena was swung ha ck and forth while an optoelectronic device recorded the compensatory chang es in wing stroke amplitude and frequency. In order to reduce the backgroun d changes in stroke kinematics resulting from the animal's closed-loop visu al fixation behaviour, the responses to eight identical mechanical rotation s were averaged in each trial. The results indicate that flies possess a ro bust equilibrium reflex in which angular rotations of the body elicit compe nsatory changes in both the amplitude and stroke frequency of the wings. Th e results of uni- and bilateral ablation experiments demonstrate that the h alteres are required for these stability reflexes. The results also confirm that halteres encode angular velocity of the body by detecting the Corioli s forces that result from the linear motion of the haltere within the rotat ing frame of reference of the fly's thorax. By rotating the flight arena at different orientations, it was possible to construct a complete directiona l tuning map of the haltere-mediated reflexes. The directional tuning of th e reflex is quite linear such that the kinematic responses vary as simple t rigonometric functions of stimulus orientation The reflexes function primar ily to stabilize pitch and yaw within the horizontal plane.