How tp1, an indirect wing steering muscle, stabilizes Drosophila's flight

Flapping flight is inherently unstable, requiring Drosophila to fine-tune their wing motions on a milliseconds timescale. Pioneering studies have shown that the direct steering muscles, which attach to the wing hinge, are important for generating these rapid flight reflexes. Recent connectome data, however, reveal that indirect steering muscles or tension muscles, which alter the mechanics of the thorax, receive some of the same synaptic inputs from the sensory apparatus as the direct steering muscles. This discovery suggests that the indirect steering muscles may also be important for flight control. Here, we show that the indirect tergopleural muscles indeed contribute substantially to stabilization, particularly for large pitch perturbations. We find that for small perturbations (less than 1000 deg/s), flies modulate their wing stroke amplitude to generate lift-based corrective torques, a strategy that has been previously documented. For larger perturbations, however, we observe that Drosophila engage an additional wing degree of freedom-the wing pitch angle-to leverage additional lift and drag forces during the corrective maneuver. Quasi-steady aerodynamic simulations reveal that this strategy minimizes power consumption, anaolgous to how some mammals (including humans) adjust their steady-state gaits in a near energy-optimal manner. Using optogenetics and a control theory framework we demonstrate that the tergopleural muscle is activated by a proportional gain component of a nonlinear PI controller responsible for determining the wing pitch angle during large perturbations. A simplified torsional-spring model for the wing hinge captures the changes in the wing pitch dynamics observed during correction maneuvers by using the tergopleural muscle to adjust the rest angle of the wing. These findings provide a striking example of reflex strategy selection in time-critical behaviors and underscores the vital role of indirect steering muscles in flight stabilization.