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Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila

eLife · 2014 · Vol. 3 · pp. e04580–e04580
Yoshinori AsoDivya SitaramanToshiharu IchinoseKarla R. KaunKatrin VogtGhislain Belliart-GuérinPierre-Yves PlaçaisAlice A. RobieNobuhiro YamagataChristopher SchnaitmannWilliam J. RowellRebecca M. JohnstonTeri-T B. NgoNan ChenWyatt KorffMichael N. NitabachUlrike HeberleinThomas PréatKristin BransonHiromu TanimotoGerald M. Rubin

Abstract

Animals discriminate stimuli, learn their predictive value and use this knowledge to modify their behavior. In Drosophila, the mushroom body (MB) plays a key role in these processes. Sensory stimuli are sparsely represented by ∼2000 Kenyon cells, which converge onto 34 output neurons (MBONs) of 21 types. We studied the role of MBONs in several associative learning tasks and in sleep regulation, revealing the extent to which information flow is segregated into distinct channels and suggesting possible roles for the multi-layered MBON network. We also show that optogenetic activation of MBONs can, depending on cell type, induce repulsion or attraction in flies. The behavioral effects of MBON perturbation are combinatorial, suggesting that the MBON ensemble collectively represents valence. We propose that local, stimulus-specific dopaminergic modulation selectively alters the balance within the MBON network for those stimuli. Our results suggest that valence encoded by the MBON ensemble biases memory-based action selection.

Neurobiology and Insect Physiology ResearchInsect and Arachnid Ecology and BehaviorPlant and animal studiesMushroom bodiesNeuroscienceOptogeneticsStimulus (psychology)Associative learningBiologyENCODESensory systemValence (chemistry)Drosophila melanogaster

MeSH terms

AnimalsAppetitive BehaviorAssociation LearningAvoidance LearningBehavior, AnimalChoice BehaviorDrosophila melanogasterLightMemoryModels, NeurologicalNeuronsOdorantsSleepTime FactorsVision, Ocular

Funding

  • Howard Hughes Medical Institute
  • Naito Foundation
  • Deutsche Forschungsgemeinschaft
  • Agence Nationale de la Recherche
  • Bundesministerium für Bildung und Forschung
  • Max-Planck-Gesellschaft
  • Japan Society for the Promotion of Science
  • National Institute of General Medical Sciences
  • National Institute of Neurological Disorders and Stroke
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