Drosophila flying in augmented reality reveals the vision-based control autonomy of the optomotor response

For walking, swimming, and flying animals, the optomotor response is essential to stabilize gaze. How flexible is the optomotor response? Classic work in Drosophila has argued that flies adapt flight control under augmented visual feedback conditions during goal-directed bar fixation. However, whether the lower-level, reflexive optomotor response can similarly adapt to augmented visual feedback (partially autonomous) or not (autonomous) over long timescales is poorly understood. To address this question, we developed an augmented reality paradigm to study the vision-based control autonomy of the yaw optomotor response of flying fruit flies (Drosophila). Flies were placed in a flight simulator, which permitted free body rotation about the yaw axis. By feeding back body movements in real time to a visual display, we augmented and inverted visual feedback. Thus, this experimental paradigm caused a constant visual error between expected and actual visual feedback to study potential adaptive visuomotor control. By combining experiments with control theory, we demonstrate that the optomotor response is autonomous during augmented reality flight bouts of up to 30 min, which exceeds the reported learning epoch during bar fixation. Agreement between predictions from linear systems theory and experimental data supports the notion that the optomotor response is approximately linear and time invariant within our experimental assay. Even under positive visual feedback, which revealed the stability limit of flies in augmented reality, the optomotor response was autonomous. Our results support a hierarchical motor control architecture in flies with fast and autonomous reflexes at the bottom and more flexible behavior at higher levels.