Two Parallel Pathways Assign Opposing Odor Valences during Drosophila Memory Formation

Summary: During olfactory associative learning in Drosophila, odors activate specific subsets of intrinsic mushroom body (MB) neurons. Coincident exposure to either rewards or punishments is thought to activate extrinsic dopaminergic neurons, which modulate synaptic connections between odor-encoding...

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Main Authors: Daisuke Yamazaki, Makoto Hiroi, Takashi Abe, Kazumichi Shimizu, Maki Minami-Ohtsubo, Yuko Maeyama, Junjiro Horiuchi, Tetsuya Tabata
Format: Article
Language:English
Published: Elsevier 2018-02-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124718301803
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spelling doaj-3251b43207d048a59f6ddb969103de0c2020-11-25T02:33:13ZengElsevierCell Reports2211-12472018-02-0122923462358Two Parallel Pathways Assign Opposing Odor Valences during Drosophila Memory FormationDaisuke Yamazaki0Makoto Hiroi1Takashi Abe2Kazumichi Shimizu3Maki Minami-Ohtsubo4Yuko Maeyama5Junjiro Horiuchi6Tetsuya Tabata7Institute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi 1-1-1, Tokyo 113-0032, Japan; Corresponding authorInstitute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi 1-1-1, Tokyo 113-0032, JapanInstitute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi 1-1-1, Tokyo 113-0032, JapanInstitute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi 1-1-1, Tokyo 113-0032, JapanInstitute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi 1-1-1, Tokyo 113-0032, JapanInstitute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi 1-1-1, Tokyo 113-0032, JapanTokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya, Tokyo, JapanInstitute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi 1-1-1, Tokyo 113-0032, Japan; Corresponding authorSummary: During olfactory associative learning in Drosophila, odors activate specific subsets of intrinsic mushroom body (MB) neurons. Coincident exposure to either rewards or punishments is thought to activate extrinsic dopaminergic neurons, which modulate synaptic connections between odor-encoding MB neurons and MB output neurons to alter behaviors. However, here we identify two classes of intrinsic MB γ neurons based on cAMP response element (CRE)-dependent expression, γCRE-p and γCRE-n, which encode aversive and appetitive valences. γCRE-p and γCRE-n neurons act antagonistically to maintain neutral valences for neutral odors. Activation or inhibition of either cell type upsets this balance, toggling odor preferences to either positive or negative values. The mushroom body output neurons, MBON-γ5β′2a/β′2mp and MBON-γ2α′1, mediate the actions of γCRE-p and γCRE-n neurons. Our data indicate that MB neurons encode valence information, as well as odor information, and this information is integrated through a process involving MBONs to regulate learning and memory. : Aversive and appetitive olfactory memories in fruit flies are formed in third order olfactory neurons, the mushroom body Kenyon cells (KCs). Yamazaki et al. identify parallel pathways consisting of two subpopulations of KCs and their output neurons that encode aversive and appetitive valences. Keywords: Drosophila, olfactory memory, γCRE-p neurons, γCRE-n neurons, valences, mutual inhibition, MBON-γ5β′2a/β′2mp, MBON-γ2α′1http://www.sciencedirect.com/science/article/pii/S2211124718301803
collection DOAJ
language English
format Article
sources DOAJ
author Daisuke Yamazaki
Makoto Hiroi
Takashi Abe
Kazumichi Shimizu
Maki Minami-Ohtsubo
Yuko Maeyama
Junjiro Horiuchi
Tetsuya Tabata
spellingShingle Daisuke Yamazaki
Makoto Hiroi
Takashi Abe
Kazumichi Shimizu
Maki Minami-Ohtsubo
Yuko Maeyama
Junjiro Horiuchi
Tetsuya Tabata
Two Parallel Pathways Assign Opposing Odor Valences during Drosophila Memory Formation
Cell Reports
author_facet Daisuke Yamazaki
Makoto Hiroi
Takashi Abe
Kazumichi Shimizu
Maki Minami-Ohtsubo
Yuko Maeyama
Junjiro Horiuchi
Tetsuya Tabata
author_sort Daisuke Yamazaki
title Two Parallel Pathways Assign Opposing Odor Valences during Drosophila Memory Formation
title_short Two Parallel Pathways Assign Opposing Odor Valences during Drosophila Memory Formation
title_full Two Parallel Pathways Assign Opposing Odor Valences during Drosophila Memory Formation
title_fullStr Two Parallel Pathways Assign Opposing Odor Valences during Drosophila Memory Formation
title_full_unstemmed Two Parallel Pathways Assign Opposing Odor Valences during Drosophila Memory Formation
title_sort two parallel pathways assign opposing odor valences during drosophila memory formation
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2018-02-01
description Summary: During olfactory associative learning in Drosophila, odors activate specific subsets of intrinsic mushroom body (MB) neurons. Coincident exposure to either rewards or punishments is thought to activate extrinsic dopaminergic neurons, which modulate synaptic connections between odor-encoding MB neurons and MB output neurons to alter behaviors. However, here we identify two classes of intrinsic MB γ neurons based on cAMP response element (CRE)-dependent expression, γCRE-p and γCRE-n, which encode aversive and appetitive valences. γCRE-p and γCRE-n neurons act antagonistically to maintain neutral valences for neutral odors. Activation or inhibition of either cell type upsets this balance, toggling odor preferences to either positive or negative values. The mushroom body output neurons, MBON-γ5β′2a/β′2mp and MBON-γ2α′1, mediate the actions of γCRE-p and γCRE-n neurons. Our data indicate that MB neurons encode valence information, as well as odor information, and this information is integrated through a process involving MBONs to regulate learning and memory. : Aversive and appetitive olfactory memories in fruit flies are formed in third order olfactory neurons, the mushroom body Kenyon cells (KCs). Yamazaki et al. identify parallel pathways consisting of two subpopulations of KCs and their output neurons that encode aversive and appetitive valences. Keywords: Drosophila, olfactory memory, γCRE-p neurons, γCRE-n neurons, valences, mutual inhibition, MBON-γ5β′2a/β′2mp, MBON-γ2α′1
url http://www.sciencedirect.com/science/article/pii/S2211124718301803
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