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Reward signal in a recurrent circuit drives appetitive long-term memory formation

Dopamine signals reward in animal brains. A single presentation of a sugar reward to Drosophila activates distinct subsets of dopamine neurons that independently induce short- and long-term olfactory memories (STM and LTM, respectively). In this study, we show that a recurrent reward circuit underli...

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Autores principales: Ichinose, Toshiharu, Aso, Yoshinori, Yamagata, Nobuhiro, Abe, Ayako, Rubin, Gerald M, Tanimoto, Hiromu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4643015/
https://www.ncbi.nlm.nih.gov/pubmed/26573957
http://dx.doi.org/10.7554/eLife.10719
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author Ichinose, Toshiharu
Aso, Yoshinori
Yamagata, Nobuhiro
Abe, Ayako
Rubin, Gerald M
Tanimoto, Hiromu
author_facet Ichinose, Toshiharu
Aso, Yoshinori
Yamagata, Nobuhiro
Abe, Ayako
Rubin, Gerald M
Tanimoto, Hiromu
author_sort Ichinose, Toshiharu
collection PubMed
description Dopamine signals reward in animal brains. A single presentation of a sugar reward to Drosophila activates distinct subsets of dopamine neurons that independently induce short- and long-term olfactory memories (STM and LTM, respectively). In this study, we show that a recurrent reward circuit underlies the formation and consolidation of LTM. This feedback circuit is composed of a single class of reward-signaling dopamine neurons (PAM-α1) projecting to a restricted region of the mushroom body (MB), and a specific MB output cell type, MBON-α1, whose dendrites arborize that same MB compartment. Both MBON-α1 and PAM-α1 neurons are required during the acquisition and consolidation of appetitive LTM. MBON-α1 additionally mediates the retrieval of LTM, which is dependent on the dopamine receptor signaling in the MB α/β neurons. Our results suggest that a reward signal transforms a nascent memory trace into a stable LTM using a feedback circuit at the cost of memory specificity. DOI: http://dx.doi.org/10.7554/eLife.10719.001
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spelling pubmed-46430152015-11-18 Reward signal in a recurrent circuit drives appetitive long-term memory formation Ichinose, Toshiharu Aso, Yoshinori Yamagata, Nobuhiro Abe, Ayako Rubin, Gerald M Tanimoto, Hiromu eLife Neuroscience Dopamine signals reward in animal brains. A single presentation of a sugar reward to Drosophila activates distinct subsets of dopamine neurons that independently induce short- and long-term olfactory memories (STM and LTM, respectively). In this study, we show that a recurrent reward circuit underlies the formation and consolidation of LTM. This feedback circuit is composed of a single class of reward-signaling dopamine neurons (PAM-α1) projecting to a restricted region of the mushroom body (MB), and a specific MB output cell type, MBON-α1, whose dendrites arborize that same MB compartment. Both MBON-α1 and PAM-α1 neurons are required during the acquisition and consolidation of appetitive LTM. MBON-α1 additionally mediates the retrieval of LTM, which is dependent on the dopamine receptor signaling in the MB α/β neurons. Our results suggest that a reward signal transforms a nascent memory trace into a stable LTM using a feedback circuit at the cost of memory specificity. DOI: http://dx.doi.org/10.7554/eLife.10719.001 eLife Sciences Publications, Ltd 2015-11-17 /pmc/articles/PMC4643015/ /pubmed/26573957 http://dx.doi.org/10.7554/eLife.10719 Text en © 2015, Ichinose 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
Ichinose, Toshiharu
Aso, Yoshinori
Yamagata, Nobuhiro
Abe, Ayako
Rubin, Gerald M
Tanimoto, Hiromu
Reward signal in a recurrent circuit drives appetitive long-term memory formation
title Reward signal in a recurrent circuit drives appetitive long-term memory formation
title_full Reward signal in a recurrent circuit drives appetitive long-term memory formation
title_fullStr Reward signal in a recurrent circuit drives appetitive long-term memory formation
title_full_unstemmed Reward signal in a recurrent circuit drives appetitive long-term memory formation
title_short Reward signal in a recurrent circuit drives appetitive long-term memory formation
title_sort reward signal in a recurrent circuit drives appetitive long-term memory formation
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4643015/
https://www.ncbi.nlm.nih.gov/pubmed/26573957
http://dx.doi.org/10.7554/eLife.10719
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