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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...

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Autores principales: Aso, Yoshinori, Sitaraman, Divya, Ichinose, Toshiharu, Kaun, Karla R, Vogt, Katrin, Belliart-Guérin, Ghislain, Plaçais, Pierre-Yves, Robie, Alice A, Yamagata, Nobuhiro, Schnaitmann, Christopher, Rowell, William J, Johnston, Rebecca M, Ngo, Teri-T B, Chen, Nan, Korff, Wyatt, Nitabach, Michael N, Heberlein, Ulrike, Preat, Thomas, Branson, Kristin M, Tanimoto, Hiromu, Rubin, Gerald M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4273436/
https://www.ncbi.nlm.nih.gov/pubmed/25535794
http://dx.doi.org/10.7554/eLife.04580
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author Aso, Yoshinori
Sitaraman, Divya
Ichinose, Toshiharu
Kaun, Karla R
Vogt, Katrin
Belliart-Guérin, Ghislain
Plaçais, Pierre-Yves
Robie, Alice A
Yamagata, Nobuhiro
Schnaitmann, Christopher
Rowell, William J
Johnston, Rebecca M
Ngo, Teri-T B
Chen, Nan
Korff, Wyatt
Nitabach, Michael N
Heberlein, Ulrike
Preat, Thomas
Branson, Kristin M
Tanimoto, Hiromu
Rubin, Gerald M
author_facet Aso, Yoshinori
Sitaraman, Divya
Ichinose, Toshiharu
Kaun, Karla R
Vogt, Katrin
Belliart-Guérin, Ghislain
Plaçais, Pierre-Yves
Robie, Alice A
Yamagata, Nobuhiro
Schnaitmann, Christopher
Rowell, William J
Johnston, Rebecca M
Ngo, Teri-T B
Chen, Nan
Korff, Wyatt
Nitabach, Michael N
Heberlein, Ulrike
Preat, Thomas
Branson, Kristin M
Tanimoto, Hiromu
Rubin, Gerald M
author_sort Aso, Yoshinori
collection PubMed
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. DOI: http://dx.doi.org/10.7554/eLife.04580.001
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spelling pubmed-42734362015-01-29 Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila Aso, Yoshinori Sitaraman, Divya Ichinose, Toshiharu Kaun, Karla R Vogt, Katrin Belliart-Guérin, Ghislain Plaçais, Pierre-Yves Robie, Alice A Yamagata, Nobuhiro Schnaitmann, Christopher Rowell, William J Johnston, Rebecca M Ngo, Teri-T B Chen, Nan Korff, Wyatt Nitabach, Michael N Heberlein, Ulrike Preat, Thomas Branson, Kristin M Tanimoto, Hiromu Rubin, Gerald M eLife Neuroscience 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. DOI: http://dx.doi.org/10.7554/eLife.04580.001 eLife Sciences Publications, Ltd 2014-12-23 /pmc/articles/PMC4273436/ /pubmed/25535794 http://dx.doi.org/10.7554/eLife.04580 Text en © 2014, Aso et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Aso, Yoshinori
Sitaraman, Divya
Ichinose, Toshiharu
Kaun, Karla R
Vogt, Katrin
Belliart-Guérin, Ghislain
Plaçais, Pierre-Yves
Robie, Alice A
Yamagata, Nobuhiro
Schnaitmann, Christopher
Rowell, William J
Johnston, Rebecca M
Ngo, Teri-T B
Chen, Nan
Korff, Wyatt
Nitabach, Michael N
Heberlein, Ulrike
Preat, Thomas
Branson, Kristin M
Tanimoto, Hiromu
Rubin, Gerald M
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila
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 Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4273436/
https://www.ncbi.nlm.nih.gov/pubmed/25535794
http://dx.doi.org/10.7554/eLife.04580
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