Abdicating power for control: a precision timing strategy to modulate function of flight power muscles

Abstract

Muscles driving rhythmic locomotion typically show strong dependence of power on the timing or phase of activation. This is particularly true in insects' main flight muscles, canonical examples of muscles thought to have a dedicated power function. However, in the moth (Manduca sexta), these muscles normally activate at a phase where the instantaneous slope of the power–phase curve is steep and well below maximum power. We provide four lines of evidence demonstrating that, contrary to the current paradigm, the moth's nervous system establishes significant control authority in these muscles through precise timing modulation: (i) left–right pairs of flight muscles normally fire precisely, within 0.5–0.6 ms of each other; (ii) during a yawing optomotor response, left—right muscle timing differences shift throughout a wider 8 ms timing window, enabling at least a 50 per cent left–right power differential; (iii) timing differences correlate with turning torque; and (iv) the downstroke power muscles alone causally account for 47 per cent of turning torque. To establish (iv), we altered muscle activation during intact behaviour by stimulating individual muscle potentials to impose left—right timing differences. Because many organisms also have muscles operating with high power–phase gains (Δpower/Δphase), this motor control strategy may be ubiquitous in locomotor systems.