Descending neuronal pathways for aerodynamic control in Drosophila*

To maintain controlled flight, animals and aerial vehicles alike must execute continuous trimming adjustments to compensate for internal and external perturbations, such as physical asymmetries or sudden gusts. Flying animals make use of a PID-like control strategy, using visual, inertial, and proprioceptive cues to determine deviations from the desired speed and flight path and adjust accordingly. Prior work in the fruit fly Drosophila melanogaster identified a population of neurons descending from the brain to the ventral nerve cord, the DNg02s, that collectively regulate wing stroke amplitude over a large dynamic range and appear to be involved in visually-mediated flight stabilization. We present additional findings illuminating the function of these important neurons in flight control. Our experiments exploit the optomotor response, a behavior in which fruit flies steer to minimize wide-field optic flow, which is quantified in tethered flies as a difference in the left and right wingbeat amplitudes. Using a suite of genetic tools to selectively silence various subsets of the population, we found a clear negative linear relationship between the number of DNg02 neurons silenced and the magnitude of the optomotor response, suggesting that the animals adjust the strength of this reflex via recruitment of different numbers of the descending cells. We then utilized high speed videography to track the wings while activating neurons in the population to determine the precise changes in stroke amplitude, stroke plane deviation, wing pitch, and wing deformation. Using a dynamically scaled physical model of a fly wing, we measured the changes in forces and moments associated with the recorded kinematic changes. This interdisciplinary study of flight control in Drosophila provides new insight into the neural mechanisms by which animals implement control strategies during locomotion.