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Learning with reinforcement prediction errors in a model of the Drosophila mushroom body

Effective decision making in a changing environment demands that accurate predictions are learned about decision outcomes. In Drosophila, such learning is orchestrated in part by the mushroom body, where dopamine neurons signal reinforcing stimuli to modulate plasticity presynaptic to mushroom body...

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Autores principales: Bennett, James E. M., Philippides, Andrew, Nowotny, Thomas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8105414/
https://www.ncbi.nlm.nih.gov/pubmed/33963189
http://dx.doi.org/10.1038/s41467-021-22592-4
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author Bennett, James E. M.
Philippides, Andrew
Nowotny, Thomas
author_facet Bennett, James E. M.
Philippides, Andrew
Nowotny, Thomas
author_sort Bennett, James E. M.
collection PubMed
description Effective decision making in a changing environment demands that accurate predictions are learned about decision outcomes. In Drosophila, such learning is orchestrated in part by the mushroom body, where dopamine neurons signal reinforcing stimuli to modulate plasticity presynaptic to mushroom body output neurons. Building on previous mushroom body models, in which dopamine neurons signal absolute reinforcement, we propose instead that dopamine neurons signal reinforcement prediction errors by utilising feedback reinforcement predictions from output neurons. We formulate plasticity rules that minimise prediction errors, verify that output neurons learn accurate reinforcement predictions in simulations, and postulate connectivity that explains more physiological observations than an experimentally constrained model. The constrained and augmented models reproduce a broad range of conditioning and blocking experiments, and we demonstrate that the absence of blocking does not imply the absence of prediction error dependent learning. Our results provide five predictions that can be tested using established experimental methods.
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spelling pubmed-81054142021-05-11 Learning with reinforcement prediction errors in a model of the Drosophila mushroom body Bennett, James E. M. Philippides, Andrew Nowotny, Thomas Nat Commun Article Effective decision making in a changing environment demands that accurate predictions are learned about decision outcomes. In Drosophila, such learning is orchestrated in part by the mushroom body, where dopamine neurons signal reinforcing stimuli to modulate plasticity presynaptic to mushroom body output neurons. Building on previous mushroom body models, in which dopamine neurons signal absolute reinforcement, we propose instead that dopamine neurons signal reinforcement prediction errors by utilising feedback reinforcement predictions from output neurons. We formulate plasticity rules that minimise prediction errors, verify that output neurons learn accurate reinforcement predictions in simulations, and postulate connectivity that explains more physiological observations than an experimentally constrained model. The constrained and augmented models reproduce a broad range of conditioning and blocking experiments, and we demonstrate that the absence of blocking does not imply the absence of prediction error dependent learning. Our results provide five predictions that can be tested using established experimental methods. Nature Publishing Group UK 2021-05-07 /pmc/articles/PMC8105414/ /pubmed/33963189 http://dx.doi.org/10.1038/s41467-021-22592-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Bennett, James E. M.
Philippides, Andrew
Nowotny, Thomas
Learning with reinforcement prediction errors in a model of the Drosophila mushroom body
title Learning with reinforcement prediction errors in a model of the Drosophila mushroom body
title_full Learning with reinforcement prediction errors in a model of the Drosophila mushroom body
title_fullStr Learning with reinforcement prediction errors in a model of the Drosophila mushroom body
title_full_unstemmed Learning with reinforcement prediction errors in a model of the Drosophila mushroom body
title_short Learning with reinforcement prediction errors in a model of the Drosophila mushroom body
title_sort learning with reinforcement prediction errors in a model of the drosophila mushroom body
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8105414/
https://www.ncbi.nlm.nih.gov/pubmed/33963189
http://dx.doi.org/10.1038/s41467-021-22592-4
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