Behavioral consequences of dopamine deficiency in the Drosophila central nervous system

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 108; no. 2; pp. 834 - 839
• Main Authors: Riemensperger, Thomas, Isabel, Guillaume, Coulom, Hélène, Neuser, Kirsa, Seugnet, Laurent, Kume, Kazuhiko, Iché-Torres, Magali, Cassar, Marlène, Strauss, Roland, Preat, Thomas, Hirsh, Jay, Birman, Serge, Nash, Howard
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 11.01.2011; National Acad Sciences
• Subjects: adults; Animal behavior; Animals; Behavior, Animal; Biological Sciences; Biosynthesis; Brain; Brain - metabolism; Central nervous system; Central Nervous System - physiology; Cognitive science; detection limit; Detection limits; Dopamine; Dopamine - deficiency; Dopamine - physiology; Dopaminergic neurons; Drosophila; Drosophila - physiology; Frameshift Mutation; Homozygote; Insects; L-dopa; Levodopa - chemistry; longevity; Memory; Memory interference; Movement; mutants; Mutation; Nervous system; Neurons; Neuroscience; Neurotransmitter Agents - metabolism; Neurotransmitters; Odors; Phototaxis; proboscis; Proteins; sleep; Smell; Sugar; Sugars; taste; Time Factors; tyrosine 3-monooxygenase; Tyrosine 3-Monooxygenase - genetics; visual perception; Walking
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.1010930108

The neuromodulatory function of dopamine (DA) is an inherent feature of nervous systems of all animals. To learn more about the function of neural DA in Drosophila, we generated mutant flies that lack tyrosine hydroxylase, and thus DA biosynthesis, selectively in the nervous system. We found that DA is absent or below detection limits in the adult brain of these flies. Despite this, they have a lifespan similar to WT flies. These mutants show reduced activity, extended sleep time, locomotor deficits that increase with age, and they are hypophagic. Whereas odor and electrical shock avoidance are not affected, aversive olfactory learning is abolished. Instead, DA-deficient flies have an apparently "masochistic" tendency to prefer the shock-associated odor 2 h after conditioning. Similarly, sugar preference is absent, whereas sugar stimulation of foreleg taste neurons induces normal proboscis extension. Feeding the DA precursor L-DOPA to adults substantially rescues the learning deficit as well as other impaired behaviors that were tested. DA-deficient flies are also defective in positive phototaxis, without alteration in visual perception and optomotor response. Surprisingly, visual tracking is largely maintained, and these mutants still possess an efficient spatial orientation memory. Our findings show that flies can perform complex brain functions in the absence of neural DA, whereas specific behaviors involving, in particular, arousal and choice require normal levels of this neuromodulator.