Insect flight is one of the fastest, most intense and most energy-demanding motor behaviors. It is modulated on multiple levels by the biogenic amine, octopamine. Within the CNS octopamine can directly switch on the flight central pattern generator and it may affect the motivation to fly. In the periphery, octopamine sensitizes wing hinge receptors and alters muscle contraction kinetics. In locusts, octopamine released from central neurons directly onto wing power muscles enhances muscle glycolysis, poising them metabolically for take-off. During prolonged flight, locust flight muscles are fueled by lipids, due to inhibition of octopaminergic neurons. In contrast, Dipteran flight muscles rely exclusively on carbohydrate metabolisms. This study addresses the role for octopamine in dipteran flight behavior by genetic manipulation in Drosophila. We find that flies lacking octopamine (Tbh, tyramine-beta-hydroxylase null mutants) show a profound flight performance deficit in both spontaneous and stimulated flight compared to wildtype controls. Five lines of evidence suggest that morphology, kinematics and development of the flight machinery are not impaired in TbH mutants: (i) wing beat frequencies, (ii) wing beat amplitudes, (iii) flight muscle structure (length of myofibrils), (iv) the number and overall dendritic structure of flight motoneurons are unaffected in TbH mutants, and (v) flight performance deficits can acutely be rescued in adult flies. Interestingly, the flight deficit is also rescued by blocking the receptors for the octopamine precursor tyramine, which is enriched in tbh mutants. Our results strongly indicate that activity of the OA system alone is not sufficient to explain the modulation of flight performance. Instead, both OA and TA systems are simultaneously involved in regulating flight performance. In an antagonistic manner, OA increases flight performance, while TA decreases it. This finding is consistent with a complex system of multiple amines orchestrating the control of motor behaviors rather than single amines eliciting single behaviors.
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