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

The following data sets were generated

Article and author information

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.

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.

Metrics

  • 2,189
    views
  • 449
    downloads
  • 10
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

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

Further reading

    1. Neuroscience
    Moritz F Wurm, Doruk Yiğit Erigüç
    Research Article

    Recognizing goal-directed actions is a computationally challenging task, requiring not only the visual analysis of body movements, but also analysis of how these movements causally impact, and thereby induce a change in, those objects targeted by an action. We tested the hypothesis that the analysis of body movements and the effects they induce relies on distinct neural representations in superior and anterior inferior parietal lobe (SPL and aIPL). In four fMRI sessions, participants observed videos of actions (e.g. breaking stick, squashing plastic bottle) along with corresponding point-light-display (PLD) stick figures, pantomimes, and abstract animations of agent–object interactions (e.g. dividing or compressing a circle). Cross-decoding between actions and animations revealed that aIPL encodes abstract representations of action effect structures independent of motion and object identity. By contrast, cross-decoding between actions and PLDs revealed that SPL is disproportionally tuned to body movements independent of visible interactions with objects. Lateral occipitotemporal cortex (LOTC) was sensitive to both action effects and body movements. These results demonstrate that parietal cortex and LOTC are tuned to physical action features, such as how body parts move in space relative to each other and how body parts interact with objects to induce a change (e.g. in position or shape/configuration). The high level of abstraction revealed by cross-decoding suggests a general neural code supporting mechanical reasoning about how entities interact with, and have effects on, each other.

    1. Neuroscience
    Gyeong Hee Pyeon, Hyewon Cho ... Yong Sang Jo
    Research Article Updated

    Recent studies suggest that calcitonin gene-related peptide (CGRP) neurons in the parabrachial nucleus (PBN) represent aversive information and signal a general alarm to the forebrain. If CGRP neurons serve as a true general alarm, their activation would modulate both passive nad active defensive behaviors depending on the magnitude and context of the threat. However, most prior research has focused on the role of CGRP neurons in passive freezing responses, with limited exploration of their involvement in active defensive behaviors. To address this, we examined the role of CGRP neurons in active defensive behavior using a predator-like robot programmed to chase mice. Our electrophysiological results revealed that CGRP neurons encode the intensity of aversive stimuli through variations in firing durations and amplitudes. Optogenetic activation of CGRP neurons during robot chasing elevated flight responses in both conditioning and retention tests, presumably by amplifying the perception of the threat as more imminent and dangerous. In contrast, animals with inactivated CGRP neurons exhibited reduced flight responses, even when the robot was programmed to appear highly threatening during conditioning. These findings expand the understanding of CGRP neurons in the PBN as a critical alarm system, capable of dynamically regulating active defensive behaviors by amplifying threat perception, and ensuring adaptive responses to varying levels of danger.