Aversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom body

In Drosophila, negatively reinforcing dopaminergic neurons also provide the inhibitory control of satiety over appetitive memory expression. Here we show that aversive learning causes a persistent depression of the conditioned odor drive to two downstream feed-forward inhibitory GABAergic interneuro...

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Main Authors: Perisse, E, Owald, D, Barnstedt, O, Talbot, C, Huetteroth, W, Waddell, S
Format: Journal article
Language:English
Published: Cell Press 2016
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author Perisse, E
Owald, D
Barnstedt, O
Talbot, C
Huetteroth, W
Waddell, S
author_facet Perisse, E
Owald, D
Barnstedt, O
Talbot, C
Huetteroth, W
Waddell, S
author_sort Perisse, E
collection OXFORD
description In Drosophila, negatively reinforcing dopaminergic neurons also provide the inhibitory control of satiety over appetitive memory expression. Here we show that aversive learning causes a persistent depression of the conditioned odor drive to two downstream feed-forward inhibitory GABAergic interneurons of the mushroom body, called MVP2, or mushroom body output neuron (MBON)-γ1pedc>α/β. However, MVP2 neuron output is only essential for expression of short-term aversive memory. Stimulating MVP2 neurons preferentially inhibits the odor-evoked activity of avoidance-directing MBONs and odor-driven avoidance behavior, whereas their inhibition enhances odor avoidance. In contrast, odor-evoked activity of MVP2 neurons is elevated in hungry flies, and their feed-forward inhibition is required for expression of appetitive memory at all times. Moreover, imposing MVP2 activity promotes inappropriate appetitive memory expression in food-satiated flies. Aversive learning and appetitive motivation therefore toggle alternate modes of a common feed-forward inhibitory MVP2 pathway to promote conditioned odor avoidance or approach.
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spelling oxford-uuid:b80188c1-7a9e-4438-bb21-51b3131e9e312022-03-27T04:52:55ZAversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom bodyJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:b80188c1-7a9e-4438-bb21-51b3131e9e31EnglishSymplectic Elements at OxfordCell Press2016Perisse, EOwald, DBarnstedt, OTalbot, CHuetteroth, WWaddell, SIn Drosophila, negatively reinforcing dopaminergic neurons also provide the inhibitory control of satiety over appetitive memory expression. Here we show that aversive learning causes a persistent depression of the conditioned odor drive to two downstream feed-forward inhibitory GABAergic interneurons of the mushroom body, called MVP2, or mushroom body output neuron (MBON)-γ1pedc>α/β. However, MVP2 neuron output is only essential for expression of short-term aversive memory. Stimulating MVP2 neurons preferentially inhibits the odor-evoked activity of avoidance-directing MBONs and odor-driven avoidance behavior, whereas their inhibition enhances odor avoidance. In contrast, odor-evoked activity of MVP2 neurons is elevated in hungry flies, and their feed-forward inhibition is required for expression of appetitive memory at all times. Moreover, imposing MVP2 activity promotes inappropriate appetitive memory expression in food-satiated flies. Aversive learning and appetitive motivation therefore toggle alternate modes of a common feed-forward inhibitory MVP2 pathway to promote conditioned odor avoidance or approach.
spellingShingle Perisse, E
Owald, D
Barnstedt, O
Talbot, C
Huetteroth, W
Waddell, S
Aversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom body
title Aversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom body
title_full Aversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom body
title_fullStr Aversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom body
title_full_unstemmed Aversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom body
title_short Aversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom body
title_sort aversive learning and appetitive motivation toggle feed forward inhibition in the drosophila mushroom body
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