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

Abstract

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.

Data availability

Source Data files for all figures are available online:http://dx.doi.org/10.17632/5rz28jr8gc.1Grunwald Kadow, Ilona (2022), "Boehm et al. (A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females)", Mendeley Data, V1, doi: 10.17632/5rz28jr8gc.1

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Author details

  1. Ariane C Boehm

    School of Life Sciences, Technical University of Munich, Freising, Germany
    Competing interests
    No competing interests declared.
  2. Anja B Friedrich

    School of Life Sciences, Technical University of Munich, Freising, Germany
    Competing interests
    No competing interests declared.
  3. Sydney Hunt

    School of Life Sciences, Technical University of Munich, Freising, Germany
    Competing interests
    No competing interests declared.
  4. Paul Bandow

    School of Life Sciences, Technical University of Munich, Freising, Germany
    Competing interests
    No competing interests declared.
  5. K P Siju

    School of Life Sciences, Technical University of Munich, Freising, Germany
    Competing interests
    No competing interests declared.
  6. Jean-Francois De Backer

    School of Life Sciences, Technical University of Munich, Freising, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2861-9994
  7. Julia Claussen

    School of Life Sciences, Technical University of Munich, Freising, Germany
    Competing interests
    No competing interests declared.
  8. Marie-Helen Link

    School of Life Sciences, Technical University of Munich, Freising, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6065-2057
  9. Thomas F Hofmann

    ZIEL - Institute for Food and Health, Technical University of Munich, Freising, Germany
    Competing interests
    No competing interests declared.
  10. Corinna Dawid

    ZIEL - Institute for Food and Health, Technical University of Munich, Freising, Germany
    Competing interests
    No competing interests declared.
  11. Ilona C Grunwald Kadow

    Faculty of Medicine, University of Bonn, Bonn, Germany
    For correspondence
    ilona.grunwald@tum.de
    Competing interests
    Ilona C Grunwald Kadow, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9085-4274

Funding

European Research Council (ERC StG FlyContext)

  • Anja B Friedrich
  • Sydney Hunt
  • K P Siju
  • Julia Claussen
  • Ilona C Grunwald Kadow

Deutsche Forschungsgemeinschaft (GR4310/5-1)

  • Ariane C Boehm
  • Paul Bandow

Deutsche Forschungsgemeinschaft (CRC870,A04)

  • K P Siju

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Sonia Sen, Tata Institute for Genetics and Society, India

Version history

  1. Preprint posted: July 25, 2021 (view preprint)
  2. Received: February 7, 2022
  3. Accepted: September 20, 2022
  4. Accepted Manuscript published: September 21, 2022 (version 1)
  5. Version of Record published: October 6, 2022 (version 2)

Copyright

© 2022, Boehm et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Ariane C Boehm
  2. Anja B Friedrich
  3. Sydney Hunt
  4. Paul Bandow
  5. K P Siju
  6. Jean-Francois De Backer
  7. Julia Claussen
  8. Marie-Helen Link
  9. Thomas F Hofmann
  10. Corinna Dawid
  11. Ilona C Grunwald Kadow
(2022)
A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females
eLife 11:e77643.
https://doi.org/10.7554/eLife.77643

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https://doi.org/10.7554/eLife.77643

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