Abstract

Aggressive social interactions are used to compete for limited resources and are regulated by complex sensory cues and the organism's internal state. While both sexes exhibit aggression, its neuronal underpinnings are understudied in females. Here, we identify a population of sexually dimorphic aIPg neurons in the adult Drosophila melanogaster central brain whose optogenetic activation increased, and genetic inactivation reduced, female aggression. Analysis of GAL4 lines identified in an unbiased screen for increased female chasing behavior revealed the involvement of another sexually dimorphic neuron, pC1d, and implicated aIPg and pC1d neurons as core nodes regulating female aggression. Connectomic analysis demonstrated that aIPg neurons and pC1d are interconnected and suggest that aIPg neurons may exert part of their effect by gating the flow of visual information to descending neurons. Our work reveals important regulatory components of the neuronal circuitry that underlies female aggressive social interactions and provides tools for their manipulation.

Data availability

Data is included in the paper and the supplemental files. Source data have been provided for Figures 1,2, 4 and 9.

The following data sets were generated

Article and author information

Author details

  1. Catherine E Schretter

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3957-6838
  2. Yoshi Aso

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2939-1688
  3. Alice A Robie

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Marisa Dreher

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0041-9229
  5. Michael-John Dolan

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9666-3682
  6. Nan Chen

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Masayoshi Ito

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Tansy Yang

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1131-0410
  9. Ruchi Parekh

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8060-2807
  10. Kristin M Branson

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Gerald M Rubin

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    rubing@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8762-8703

Funding

Howard Hughes Medial Institute

  • Catherine E Schretter
  • Yoshi Aso
  • Alice A Robie
  • Marisa Dreher
  • Michael-John Dolan
  • Nan Chen
  • Masayoshi Ito
  • Tansy Yang
  • Ruchi Parekh
  • Kristin M Branson

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

Reviewing Editor

  1. Mani Ramaswami, Trinity College Dublin, Ireland

Publication history

  1. Received: May 14, 2020
  2. Accepted: November 2, 2020
  3. Accepted Manuscript published: November 3, 2020 (version 1)
  4. Version of Record published: January 6, 2021 (version 2)

Copyright

© 2020, Schretter 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

  • 3,768
    Page views
  • 540
    Downloads
  • 30
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

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. Catherine E Schretter
  2. Yoshi Aso
  3. Alice A Robie
  4. Marisa Dreher
  5. Michael-John Dolan
  6. Nan Chen
  7. Masayoshi Ito
  8. Tansy Yang
  9. Ruchi Parekh
  10. Kristin M Branson
  11. Gerald M Rubin
(2020)
Cell types and neuronal circuitry underlying female aggression in Drosophila
eLife 9:e58942.
https://doi.org/10.7554/eLife.58942

Further reading

    1. Neuroscience
    Meghan Laturney, Gabriella R Sterne, Kristin Scott
    Research Article Updated

    Mated females reallocate resources to offspring production, causing changes to nutritional requirements and challenges to energy homeostasis. Although observed across species, the neural and endocrine mechanisms that regulate the nutritional needs of mated females are not well understood. Here, we find that mated Drosophila melanogaster females increase sugar intake, which is regulated by the activity of sexually dimorphic insulin receptor (Lgr3) neurons. In virgins, Lgr3+ cells have reduced activity as they receive inhibitory input from active, female-specific pCd-2 cells, restricting sugar intake. During copulation, males deposit sex peptide into the female reproductive tract, which silences a three-tier mating status circuit and initiates the female postmating response. We show that pCd-2 neurons also become silenced after mating due to the direct synaptic input from the mating status circuit. Thus, in mated females pCd-2 inhibition is attenuated, activating downstream Lgr3+ neurons and promoting sugar intake. Together, this circuit transforms the mated signal into a long-term hunger signal. Our results demonstrate that the mating circuit alters nutrient sensing centers to increase feeding in mated females, providing a mechanism to increase intake in anticipation of the energetic costs associated with reproduction.

    1. Neuroscience
    Narges Doostani, Gholam-Ali Hossein-Zadeh, Maryam Vaziri-Pashkam
    Research Article Updated

    Divisive normalization of the neural responses by the activity of the neighboring neurons has been proposed as a fundamental operation in the nervous system based on its success in predicting neural responses recorded in primate electrophysiology studies. Nevertheless, experimental evidence for the existence of this operation in the human brain is still scant. Here, using functional MRI, we examined the role of normalization across the visual hierarchy in the human visual cortex. Using stimuli form the two categories of human bodies and houses, we presented objects in isolation or in clutter and asked participants to attend or ignore the stimuli. Focusing on the primary visual area V1, the object-selective regions LO and pFs, the body-selective region EBA, and the scene-selective region PPA, we first modeled single-voxel responses using a weighted sum, a weighted average, and a normalization model and demonstrated that although the weighted sum and weighted average models also made acceptable predictions in some conditions, the response to multiple stimuli could generally be better described by a model that takes normalization into account. We then determined the observed effects of attention on cortical responses and demonstrated that these effects were predicted by the normalization model, but not by the weighted sum or the weighted average models. Our results thus provide evidence that the normalization model can predict responses to objects across shifts of visual attention, suggesting the role of normalization as a fundamental operation in the human brain.