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

Yoshinori Aso, Divya Sitaraman, Toshiharu Ichinose, Karla R. Kaun, Katrin Vogt, Ghislain Belliart-Guérin, Pierre Yves Plaçais, Alice A. Robie, Nobuhiro Yamagata, Christopher Schnaitmann, William J. Rowell, Rebecca M. Johnston, Teri T.B. Ngo, Nan Chen, Wyatt Korff, Michael N. Nitabach, Ulrike Heberlein, Thomas Preat, Kristin M. Branson, Hiromu TanimotoGerald M. Rubin

Research output: Contribution to journalArticle

245 Citations (Scopus)

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.

Original languageEnglish
Article numbere04580
Pages (from-to)e04580
JournaleLife
Volume3
DOIs
Publication statusPublished - 2014

Keywords

  • D. melanogaster
  • action selection
  • behavioral valence
  • memory
  • mushroom body
  • neuroscience
  • population code
  • sleep

ASJC Scopus subject areas

  • Neuroscience(all)
  • Immunology and Microbiology(all)
  • Biochemistry, Genetics and Molecular Biology(all)

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    Aso, Y., Sitaraman, D., Ichinose, T., Kaun, K. R., Vogt, K., Belliart-Guérin, G., Plaçais, P. Y., Robie, A. A., Yamagata, N., Schnaitmann, C., Rowell, W. J., Johnston, R. M., Ngo, T. T. B., Chen, N., Korff, W., Nitabach, M. N., Heberlein, U., Preat, T., Branson, K. M., ... Rubin, G. M. (2014). Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila. eLife, 3, e04580. [e04580]. https://doi.org/10.7554/eLife.04580