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 Tanimoto,
Gerald M Rubin
Affiliations
Yoshinori Aso
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
Divya Sitaraman
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States; Department of Cellular and Molecular Physiology, Yale School of Medicine, New Haven, United States; Department of Genetics, Yale School of Medicine, New Haven, United States; Program in Cellular Neuroscience, Neurodegeneration and Repair, Yale School of Medicine, New Haven, United States
Toshiharu Ichinose
Max Planck Institute of Neurobiology, Martinsried, Germany; Graduate School of Life Sciences, Tohoku University, Sendai, Japan
Karla R Kaun
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
Katrin Vogt
Max Planck Institute of Neurobiology, Martinsried, Germany
Ghislain Belliart-Guérin
Genes and Dynamics of Memory Systems, Brain Plasticity Unit, Centre National de la Recherche Scientifique, ESPCI, Paris, France
Pierre-Yves Plaçais
Genes and Dynamics of Memory Systems, Brain Plasticity Unit, Centre National de la Recherche Scientifique, ESPCI, Paris, France
Alice A Robie
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
Nobuhiro Yamagata
Max Planck Institute of Neurobiology, Martinsried, Germany; Graduate School of Life Sciences, Tohoku University, Sendai, Japan
Christopher Schnaitmann
Max Planck Institute of Neurobiology, Martinsried, Germany
William J Rowell
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
Rebecca M Johnston
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
Teri-T B Ngo
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
Nan Chen
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
Michael N Nitabach
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States; Department of Cellular and Molecular Physiology, Yale School of Medicine, New Haven, United States; Department of Genetics, Yale School of Medicine, New Haven, United States; Program in Cellular Neuroscience, Neurodegeneration and Repair, Yale School of Medicine, New Haven, United States
Ulrike Heberlein
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
Thomas Preat
Genes and Dynamics of Memory Systems, Brain Plasticity Unit, Centre National de la Recherche Scientifique, ESPCI, Paris, France
Kristin M Branson
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
Hiromu Tanimoto
Max Planck Institute of Neurobiology, Martinsried, Germany; Graduate School of Life Sciences, Tohoku University, Sendai, Japan
Gerald M Rubin
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
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.