Abstract

Adaptive control of breathing is essential for life, yet the neural circuits that couple respiration to locomotion and internal physiological state remain poorly understood. Insects regulate gas exchange through spiracles: valve-like openings in the cuticle that allow oxygen uptake while minimizing water loss. We find that spiracle opening in Drosophila is dynamically matched to flight power and reduced by dehydration. We identify the motor neurons that innervate the spiracle muscles and show that their optogenetic activation closes all eighteen spiracles and rapidly limits flight power. Inhibitory interneurons transmit descending flight commands to the spiracle motor neurons, opening spiracles in proportion to metabolic demand. A parallel interoceptive pathway converges on the same interneurons to close the spiracles and suppress flight. Feedforward descending commands thus couple flight power to spiracle opening, while interoceptive feedback pathways close spiracles to balance oxygen supply against water loss. This compact circuit architecture may reflect a general solution for matching respiration to the competing demands of locomotion and water conservation.