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

Author:

Aso Yoshinori1,Sitaraman Divya1234,Ichinose Toshiharu56,Kaun Karla R1,Vogt Katrin5,Belliart-Guérin Ghislain7,Plaçais Pierre-Yves7,Robie Alice A1,Yamagata Nobuhiro56,Schnaitmann Christopher5,Rowell William J1,Johnston Rebecca M1,Ngo Teri-T B1,Chen Nan1,Korff Wyatt1ORCID,Nitabach Michael N1234,Heberlein Ulrike1,Preat Thomas7,Branson Kristin M1,Tanimoto Hiromu56,Rubin Gerald M1

Affiliation:

1. Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

2. Department of Cellular and Molecular Physiology, Yale School of Medicine, New Haven, United States

3. Department of Genetics, Yale School of Medicine, New Haven, United States

4. Program in Cellular Neuroscience, Neurodegeneration and Repair, Yale School of Medicine, New Haven, United States

5. Max Planck Institute of Neurobiology, Martinsried, Germany

6. Graduate School of Life Sciences, Tohoku University, Sendai, Japan

7. Genes and Dynamics of Memory Systems, Brain Plasticity Unit, Centre National de la Recherche Scientifique, ESPCI, Paris, France

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.

Funder

Howard Hughes Medical Institute

Agence Nationale de la Recherche

Labex MemoLife

Bundesministerium für Bildung und Forschung

Max-Planck-Gesellschaft

Deutsche Forschungsgemeinschaft

Japan Society for the Promotion of Science

Naito Foundation

National Institute of Neurological Disorders and Stroke

National Institute of General Medical Sciences

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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