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Upregulated energy metabolism in the Drosophila mushroom body is the trigger for long-term memory

Efficient energy use has constrained the evolution of nervous systems. However, it is unresolved whether energy metabolism may resultantly regulate major brain functions. Our observation that Drosophila flies double their sucrose intake at an early stage of long-term memory formation initiated the i...

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Autores principales: Plaçais, Pierre-Yves, de Tredern, Éloïse, Scheunemann, Lisa, Trannoy, Séverine, Goguel, Valérie, Han, Kyung-An, Isabel, Guillaume, Preat, Thomas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5465319/
https://www.ncbi.nlm.nih.gov/pubmed/28580949
http://dx.doi.org/10.1038/ncomms15510
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author Plaçais, Pierre-Yves
de Tredern, Éloïse
Scheunemann, Lisa
Trannoy, Séverine
Goguel, Valérie
Han, Kyung-An
Isabel, Guillaume
Preat, Thomas
author_facet Plaçais, Pierre-Yves
de Tredern, Éloïse
Scheunemann, Lisa
Trannoy, Séverine
Goguel, Valérie
Han, Kyung-An
Isabel, Guillaume
Preat, Thomas
author_sort Plaçais, Pierre-Yves
collection PubMed
description Efficient energy use has constrained the evolution of nervous systems. However, it is unresolved whether energy metabolism may resultantly regulate major brain functions. Our observation that Drosophila flies double their sucrose intake at an early stage of long-term memory formation initiated the investigation of how energy metabolism intervenes in this process. Cellular-resolution imaging of energy metabolism reveals a concurrent elevation of energy consumption in neurons of the mushroom body, the fly's major memory centre. Strikingly, upregulation of mushroom body energy flux is both necessary and sufficient to drive long-term memory formation. This effect is triggered by a specific pair of dopaminergic neurons afferent to the mushroom bodies, via the D5-like DAMB dopamine receptor. Hence, dopamine signalling mediates an energy switch in the mushroom body that controls long-term memory encoding. Our data thus point to an instructional role for energy flux in the execution of demanding higher brain functions.
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spelling pubmed-54653192017-06-22 Upregulated energy metabolism in the Drosophila mushroom body is the trigger for long-term memory Plaçais, Pierre-Yves de Tredern, Éloïse Scheunemann, Lisa Trannoy, Séverine Goguel, Valérie Han, Kyung-An Isabel, Guillaume Preat, Thomas Nat Commun Article Efficient energy use has constrained the evolution of nervous systems. However, it is unresolved whether energy metabolism may resultantly regulate major brain functions. Our observation that Drosophila flies double their sucrose intake at an early stage of long-term memory formation initiated the investigation of how energy metabolism intervenes in this process. Cellular-resolution imaging of energy metabolism reveals a concurrent elevation of energy consumption in neurons of the mushroom body, the fly's major memory centre. Strikingly, upregulation of mushroom body energy flux is both necessary and sufficient to drive long-term memory formation. This effect is triggered by a specific pair of dopaminergic neurons afferent to the mushroom bodies, via the D5-like DAMB dopamine receptor. Hence, dopamine signalling mediates an energy switch in the mushroom body that controls long-term memory encoding. Our data thus point to an instructional role for energy flux in the execution of demanding higher brain functions. Nature Publishing Group 2017-06-05 /pmc/articles/PMC5465319/ /pubmed/28580949 http://dx.doi.org/10.1038/ncomms15510 Text en Copyright © 2017, The Author(s) http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Plaçais, Pierre-Yves
de Tredern, Éloïse
Scheunemann, Lisa
Trannoy, Séverine
Goguel, Valérie
Han, Kyung-An
Isabel, Guillaume
Preat, Thomas
Upregulated energy metabolism in the Drosophila mushroom body is the trigger for long-term memory
title Upregulated energy metabolism in the Drosophila mushroom body is the trigger for long-term memory
title_full Upregulated energy metabolism in the Drosophila mushroom body is the trigger for long-term memory
title_fullStr Upregulated energy metabolism in the Drosophila mushroom body is the trigger for long-term memory
title_full_unstemmed Upregulated energy metabolism in the Drosophila mushroom body is the trigger for long-term memory
title_short Upregulated energy metabolism in the Drosophila mushroom body is the trigger for long-term memory
title_sort upregulated energy metabolism in the drosophila mushroom body is the trigger for long-term memory
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5465319/
https://www.ncbi.nlm.nih.gov/pubmed/28580949
http://dx.doi.org/10.1038/ncomms15510
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