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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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-09-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/77643 |
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| author | Ariane C Boehm Anja B Friedrich Sydney Hunt Paul Bandow KP Siju Jean Francois De Backer Julia Claussen Marie Helen Link Thomas F Hofmann Corinna Dawid Ilona C Grunwald Kadow |
| author_facet | Ariane C Boehm Anja B Friedrich Sydney Hunt Paul Bandow KP Siju Jean Francois De Backer Julia Claussen Marie Helen Link Thomas F Hofmann Corinna Dawid Ilona C Grunwald Kadow |
| author_sort | Ariane C Boehm |
| collection | DOAJ |
| 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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| id | doaj.art-1ccf9f536d5247f89786d687937c2e6e |
| institution | Directory Open Access Journal |
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| language | English |
| last_indexed | 2024-04-13T23:22:13Z |
| publishDate | 2022-09-01 |
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| series | eLife |
| spelling | doaj.art-1ccf9f536d5247f89786d687937c2e6e2022-12-22T02:25:12ZengeLife Sciences Publications LtdeLife2050-084X2022-09-011110.7554/eLife.77643A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila femalesAriane C Boehm0Anja B Friedrich1Sydney Hunt2Paul Bandow3KP Siju4Jean Francois De Backer5https://orcid.org/0000-0002-2861-9994Julia Claussen6Marie Helen Link7https://orcid.org/0000-0002-6065-2057Thomas F Hofmann8Corinna Dawid9Ilona C Grunwald Kadow10https://orcid.org/0000-0002-9085-4274Technical University Munich, School of Life Sciences, Neuronal Control of Metabolism, Freising, Germany; Graduate School of Systemic Neurosciences, Ludwig Maximilian University, Martinsried, GermanyTechnical University Munich, School of Life Sciences, Neuronal Control of Metabolism, Freising, GermanyTechnical University Munich, School of Life Sciences, Neuronal Control of Metabolism, Freising, GermanyTechnical University Munich, School of Life Sciences, Neuronal Control of Metabolism, Freising, Germany; Graduate School of Systemic Neurosciences, Ludwig Maximilian University, Martinsried, Germany; ZIEL – Institute for Food and Health, Technical University Munich, School of Life Sciences, Freising, GermanyTechnical University Munich, School of Life Sciences, Neuronal Control of Metabolism, Freising, GermanyTechnical University Munich, School of Life Sciences, Neuronal Control of Metabolism, Freising, GermanyTechnical University Munich, School of Life Sciences, Neuronal Control of Metabolism, Freising, GermanyTechnical University Munich, School of Life Sciences, Neuronal Control of Metabolism, Freising, GermanyZIEL – Institute for Food and Health, Technical University Munich, School of Life Sciences, Freising, Germany; Technical University Munich, School of Life Sciences, Chair of Food Chemistry and Molecular Sensory Science, Freising, GermanyZIEL – Institute for Food and Health, Technical University Munich, School of Life Sciences, Freising, Germany; Technical University Munich, School of Life Sciences, Chair of Food Chemistry and Molecular Sensory Science, Freising, GermanyTechnical University Munich, School of Life Sciences, Neuronal Control of Metabolism, Freising, Germany; Graduate School of Systemic Neurosciences, Ludwig Maximilian University, Martinsried, Germany; ZIEL – Institute for Food and Health, Technical University Munich, School of Life Sciences, Freising, Germany; University of Bonn, Faculty of Medicine, Institute of Physiology II, Bonn, GermanyMotherhood 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.https://elifesciences.org/articles/77643olfactory systemmushroom bodyDrosophilaneural circuitsinternal stateimaging |
| spellingShingle | Ariane C Boehm Anja B Friedrich Sydney Hunt Paul Bandow KP Siju Jean Francois De Backer Julia Claussen Marie Helen Link Thomas F Hofmann Corinna Dawid Ilona C Grunwald Kadow A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females eLife olfactory system mushroom body Drosophila neural circuits internal state imaging |
| 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 | olfactory system mushroom body Drosophila neural circuits internal state imaging |
| url | https://elifesciences.org/articles/77643 |
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