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The Journal of Neuroscience, October 10, 2007, 27(41):11122-11131; doi:10.1523/JNEUROSCI.2704-07.2007

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Behavioral/Systems/Cognitive
Flight Initiation and Maintenance Deficits in Flies with Genetically Altered Biogenic Amine Levels

Björn Brembs,^1 * Frauke Christiansen,^1 * Hans Joachim Pflüger,¹ and Carsten Duch²

¹Institute of Biology, Free University of Berlin, 14195 Berlin, Germany, and ²School of Life Sciences, Arizona State University, Tempe, Arizona 85287

Correspondence should be addressed to Carsten Duch, School of Life Sciences, Arizona State University, Tempe, AZ 85287. Email: carsten.duch{at}asu.edu

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 acts directly on the flight central pattern generator, and it affects motivational states. In the periphery, octopamine sensitizes sensory receptors, alters muscle contraction kinetics, and enhances flight muscle glycolysis. This study addresses the roles for octopamine and its precursor tyramine in flight behavior by genetic and pharmacological manipulation in Drosophila. Octopamine is not the natural signal for flight initiation because flies lacking octopamine [tyramine-ß-hydroxylase (TßH) null mutants] can fly. However, they show profound differences with respect to flight initiation and flight maintenance compared with wild-type controls. The morphology, kinematics, and development of the flight machinery are not impaired in TßH mutants because wing-beat frequencies and amplitudes, flight muscle structure, and overall dendritic structure of flight motoneurons are unaffected in TßH mutants. Accordingly, the flight behavior phenotypes can be rescued acutely in adult flies. Flight deficits are rescued by substituting octopamine but also by blocking the receptors for tyramine, which is enriched in TßH mutants. Conversely, ablating all neurons containing octopamine or tyramine phenocopies TßH mutants. Therefore, both octopamine and tyramine systems are simultaneously involved in regulating flight initiation and maintenance. Different sets of rescue experiments indicate different sites of action for both amines. These findings are consistent with a complex system of multiple amines orchestrating the control of motor behaviors on multiple levels rather than single amines eliciting single behaviors.

Key words: octopamine; Drosophila; tyramine; motor behavior; modulation; invertebrate

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Received June 14, 2007; revised Aug. 28, 2007; accepted Aug. 29, 2007.

Correspondence should be addressed to Carsten Duch, School of Life Sciences, Arizona State University, Tempe, AZ 85287. Email: carsten.duch{at}asu.edu

This article has been cited by other articles:

				E. M. Blumenthal Isoform- and cell-specific function of tyrosine decarboxylase in the Drosophila Malpighian tubule J. Exp. Biol., December 1, 2009; 212(23): 3802 - 3809. [Abstract] [Full Text] [PDF]

				T. Hesselberg and F.-O. Lehmann The role of experience in flight behaviour of Drosophila J. Exp. Biol., October 15, 2009; 212(20): 3377 - 3386. [Abstract] [Full Text] [PDF]

				C. Duch, F. Vonhoff, and S. Ryglewski Dendrite Elongation and Dendritic Branching Are Affected Separately by Different Forms of Intrinsic Motoneuron Excitability J Neurophysiol, November 1, 2008; 100(5): 2525 - 2536. [Abstract] [Full Text] [PDF]

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