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A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females

Motherhood induces a drastic, sometimes long-lasting, change in internal state and behavior in many female animals. How a change in reproductive state or the discrete event of mating modulates specific female behaviors is still incompletely understood. Using calcium imaging of the whole brain of Dro...

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Autores principales: Boehm, Ariane C, Friedrich, Anja B, Hunt, Sydney, Bandow, Paul, Siju, KP, De Backer, Jean Francois, Claussen, Julia, Link, Marie Helen, Hofmann, Thomas F, Dawid, Corinna, Grunwald Kadow, Ilona C
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9536836/
https://www.ncbi.nlm.nih.gov/pubmed/36129174
http://dx.doi.org/10.7554/eLife.77643
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author Boehm, Ariane C
Friedrich, Anja B
Hunt, Sydney
Bandow, Paul
Siju, KP
De Backer, Jean Francois
Claussen, Julia
Link, Marie Helen
Hofmann, Thomas F
Dawid, Corinna
Grunwald Kadow, Ilona C
author_facet Boehm, Ariane C
Friedrich, Anja B
Hunt, Sydney
Bandow, Paul
Siju, KP
De Backer, Jean Francois
Claussen, Julia
Link, Marie Helen
Hofmann, Thomas F
Dawid, Corinna
Grunwald Kadow, Ilona C
author_sort Boehm, Ariane C
collection PubMed
description Motherhood induces a drastic, sometimes long-lasting, change in internal state and behavior in many female animals. How a change in reproductive state or the discrete event of mating modulates specific female behaviors is still incompletely understood. Using calcium imaging of the whole brain of Drosophila females, we find that mating does not induce a global change in brain activity. Instead, mating modulates the pheromone response of dopaminergic neurons innervating the fly’s learning and memory center, the mushroom body (MB). Using the mating-induced increased attraction to the odor of important nutrients, polyamines, we show that disruption of the female fly’s ability to smell, for instance the pheromone cVA, during mating leads to a reduction in polyamine preference for days later indicating that the odor environment at mating lastingly influences female perception and choice behavior. Moreover, dopaminergic neurons including innervation of the β’1 compartment are sufficient to induce the lasting behavioral increase in polyamine preference. We further show that MB output neurons (MBON) of the β’1 compartment are activated by pheromone odor and their activity during mating bidirectionally modulates preference behavior in mated and virgin females. Their activity is not required, however, for the expression of polyamine attraction. Instead, inhibition of another type of MBON innervating the β’2 compartment enables expression of high odor attraction. In addition, the response of a lateral horn (LH) neuron, AD1b2, which output is required for the expression of polyamine attraction, shows a modulated polyamine response after mating. Taken together, our data in the fly suggests that mating-related sensory experience regulates female odor perception and expression of choice behavior through a dopamine-gated learning circuit.
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spelling pubmed-95368362022-10-07 A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females Boehm, Ariane C Friedrich, Anja B Hunt, Sydney Bandow, Paul Siju, KP De Backer, Jean Francois Claussen, Julia Link, Marie Helen Hofmann, Thomas F Dawid, Corinna Grunwald Kadow, Ilona C eLife Neuroscience Motherhood induces a drastic, sometimes long-lasting, change in internal state and behavior in many female animals. How a change in reproductive state or the discrete event of mating modulates specific female behaviors is still incompletely understood. Using calcium imaging of the whole brain of Drosophila females, we find that mating does not induce a global change in brain activity. Instead, mating modulates the pheromone response of dopaminergic neurons innervating the fly’s learning and memory center, the mushroom body (MB). Using the mating-induced increased attraction to the odor of important nutrients, polyamines, we show that disruption of the female fly’s ability to smell, for instance the pheromone cVA, during mating leads to a reduction in polyamine preference for days later indicating that the odor environment at mating lastingly influences female perception and choice behavior. Moreover, dopaminergic neurons including innervation of the β’1 compartment are sufficient to induce the lasting behavioral increase in polyamine preference. We further show that MB output neurons (MBON) of the β’1 compartment are activated by pheromone odor and their activity during mating bidirectionally modulates preference behavior in mated and virgin females. Their activity is not required, however, for the expression of polyamine attraction. Instead, inhibition of another type of MBON innervating the β’2 compartment enables expression of high odor attraction. In addition, the response of a lateral horn (LH) neuron, AD1b2, which output is required for the expression of polyamine attraction, shows a modulated polyamine response after mating. Taken together, our data in the fly suggests that mating-related sensory experience regulates female odor perception and expression of choice behavior through a dopamine-gated learning circuit. eLife Sciences Publications, Ltd 2022-09-21 /pmc/articles/PMC9536836/ /pubmed/36129174 http://dx.doi.org/10.7554/eLife.77643 Text en © 2022, Boehm et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Boehm, Ariane C
Friedrich, Anja B
Hunt, Sydney
Bandow, Paul
Siju, KP
De Backer, Jean Francois
Claussen, Julia
Link, Marie Helen
Hofmann, Thomas F
Dawid, Corinna
Grunwald Kadow, Ilona C
A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females
title A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females
title_full A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females
title_fullStr A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females
title_full_unstemmed A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females
title_short A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females
title_sort dopamine-gated learning circuit underpins reproductive state-dependent odor preference in drosophila females
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9536836/
https://www.ncbi.nlm.nih.gov/pubmed/36129174
http://dx.doi.org/10.7554/eLife.77643
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