Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila
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 t...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2014-12-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/04580 |
| _version_ | 1811180483543826432 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Yoshinori Aso |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-11T09:03:52Z |
| format | Article |
| id | doaj.art-80cc4fc89fc9426e8ebf8f85444746e7 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:03:52Z |
| publishDate | 2014-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-80cc4fc89fc9426e8ebf8f85444746e72022-12-22T04:32:42ZengeLife Sciences Publications LtdeLife2050-084X2014-12-01310.7554/eLife.04580Mushroom body output neurons encode valence and guide memory-based action selection in DrosophilaYoshinori Aso0Divya Sitaraman1Toshiharu Ichinose2Karla R Kaun3Katrin Vogt4Ghislain Belliart-Guérin5Pierre-Yves Plaçais6Alice A Robie7Nobuhiro Yamagata8Christopher Schnaitmann9William J Rowell10Rebecca M Johnston11Teri-T B Ngo12Nan Chen13Wyatt Korff14https://orcid.org/0000-0001-8396-1533Michael N Nitabach15Ulrike Heberlein16Thomas Preat17Kristin M Branson18Hiromu Tanimoto19Gerald M Rubin20Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia 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 StatesMax Planck Institute of Neurobiology, Martinsried, Germany; Graduate School of Life Sciences, Tohoku University, Sendai, JapanJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesMax Planck Institute of Neurobiology, Martinsried, GermanyGenes and Dynamics of Memory Systems, Brain Plasticity Unit, Centre National de la Recherche Scientifique, ESPCI, Paris, FranceGenes and Dynamics of Memory Systems, Brain Plasticity Unit, Centre National de la Recherche Scientifique, ESPCI, Paris, FranceJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesMax Planck Institute of Neurobiology, Martinsried, Germany; Graduate School of Life Sciences, Tohoku University, Sendai, JapanMax Planck Institute of Neurobiology, Martinsried, GermanyJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia 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 StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesGenes and Dynamics of Memory Systems, Brain Plasticity Unit, Centre National de la Recherche Scientifique, ESPCI, Paris, FranceJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesMax Planck Institute of Neurobiology, Martinsried, Germany; Graduate School of Life Sciences, Tohoku University, Sendai, JapanJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesAnimals 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.https://elifesciences.org/articles/04580mushroom bodymemorybehavioral valencesleeppopulation codeaction selection |
| spellingShingle | 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 Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila eLife mushroom body memory behavioral valence sleep population code action selection |
| title | Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila |
| title_full | Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila |
| title_fullStr | Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila |
| title_full_unstemmed | Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila |
| title_short | Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila |
| title_sort | mushroom body output neurons encode valence and guide memory based action selection in drosophila |
| topic | mushroom body memory behavioral valence sleep population code action selection |
| url | https://elifesciences.org/articles/04580 |
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