Flight power muscles have a coordinated, causal role in controlling hawkmoth pitch turns

Abstract

Flying insects solve a daunting control problem of generating a patterned and precise motor program to stay airborne and generate agile maneuvers. In this motor program consisting of every action potential controlling wing musculature, each muscle encodes significant information about movement in precise spike timing down to the millisecond scale. While individual muscles share information about movement, we do not yet know if they have separable effects on an animals motion, or if muscles functionally interact such that the effects of any muscles timing depends heavily on the state of the entire musculature. To answer these questions, we performed spike-resolution electromyography and precise stimulation of individual spikes in the hawkmoth Manduca sexta during tethered flapping. We specifically explored how the flight power muscles themselves may contribute to pitch control which is necessary to stabilize flight. Combining correlational study of visually-induced turns with causal manipulation of spike timing, we discovered likely coordination patterns for pitch turns, investigated if these correlational patterns can individually drive pitch control, and studied whether the precise spike timing of indirect power muscles can lead to pitch maneuvers. We observed significant timing change of the main downstroke muscles, the dorsolongitudinal muscles (DLMs), associated with whether a moth was pitching up or down. Causally inducing this timing change in the DLMs with electrical stimulation produced a consistent, mechanically relevant feature in pitch torque, establishing that indirect power muscles in Manduca have a control role in pitch. Because changes were evoked in unconstrained flapping in only the DLMs, however, these pitch torque features left large unexplained variation. We find this unexplained variation indicates significant functional overlap in pitch control such that precise timing of one power muscle does not produce a precise turn, demonstrating the importance of coordination across the entire motor program for flight. Summary StatementWe investigate how individual muscles contribute to flight by manipulating muscle timing in behaving hawkmoths. We find precise timing of single muscles does not produce precise turns, highlighting the importance of coordination across the entire motor program.