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Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila
Yoshinori Aso (Howard Hughes Medical Institute, Janelia Research Campus), Divya Sitaraman (Howard Hughes Medical Institute, Janelia Research Campus), Toshiharu Ichinose (Max Planck Society, Tohoku University), Karla R. Kaun (Howard Hughes Medical Institute, Janelia Research Campus), Katrin Vogt (Max Planck Institute of Neurobiology), Ghislain Belliart-Guérin (Centre National de la Recherche Scientifique, ESPCI Paris), Pierre-Yves Plaçais (Centre National de la Recherche Scientifique, ESPCI Paris), Alice A. Robie (Howard Hughes Medical Institute, Janelia Research Campus), Nobuhiro Yamagata (Tohoku University, Max Planck Institute of Neurobiology), Christopher Schnaitmann (Max Planck Institute of Neurobiology), William J. Rowell (Howard Hughes Medical Institute, Janelia Research Campus), Rebecca M. Johnston (Howard Hughes Medical Institute, Janelia Research Campus), Teri-T B. Ngo (Howard Hughes Medical Institute, Janelia Research Campus), Nan Chen (Howard Hughes Medical Institute, Janelia Research Campus), Wyatt L. Korff (Howard Hughes Medical Institute, Janelia Research Campus), Michael N. Nitabach (Howard Hughes Medical Institute, Janelia Research Campus), Ulrike Heberlein (Howard Hughes Medical Institute, Janelia Research Campus), Thomas Préat (Centre National de la Recherche Scientifique, ESPCI Paris), Kristin M. Branson (Howard Hughes Medical Institute, Janelia Research Campus), Hiromu Tanimoto (Max Planck Society, Tohoku University), Gerald M. Rubin (Howard Hughes Medical Institute, Janelia Research Campus)
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.