1. Neuroscience
Download icon

Social dominance mediates behavioral adaptation to chronic stress in a sex-specific manner

  1. Stoyo Karamihalev
  2. Elena Brivio
  3. Cornelia Flachskamm
  4. Rainer Stoffel
  5. Mathias V Schmidt
  6. Alon Chen  Is a corresponding author
  1. Max Planck Institute of Psychiatry, Germany
  2. Weizmann Institute of Science, Israel
Research Article
  • Cited 2
  • Views 2,511
  • Annotations
Cite this article as: eLife 2020;9:e58723 doi: 10.7554/eLife.58723

Abstract

Sex differences and social context independently contribute to the development of stress-related disorders. However, less is known about how their interplay might influence behavior and physiology. Here we focused on social hierarchy status, a major component of the social environment in mice, and whether it influences the behavioral adaptation to chronic stress in a sex-specific manner. We used a high-throughput automated behavioral monitoring system to assess social dominance in same-sex group-living mice. We found that position in the social hierarchy at baseline was a significant predictor of multiple behavioral outcomes following exposure to chronic stress. Crucially, this association carried opposite consequences for the two sexes. This work demonstrates the importance of recognizing the interplay between sex and social factors and enhances our understating of how individual differences shape the stress response.

Data availability

All data used to support the findings of this work and the code used in performing the analyses and producing the figures for this manuscript is freely accessible in a GitHub repository:https://stoyokaramihalev.github.io/CMS_Dominance/The MATLAB-based mouse tracking system is available from the corresponding author upon request.

Article and author information

Author details

  1. Stoyo Karamihalev

    Department of Stress Neurobiology and Neurogenetics, Max Planck Institute of Psychiatry, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Elena Brivio

    Department of Stress Neurobiology and Neurogenetics, Max Planck Institute of Psychiatry, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6213-0973
  3. Cornelia Flachskamm

    Department of Stress Neurobiology and Neurogenetics, Max Planck Institute of Psychiatry, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Rainer Stoffel

    Department of Stress Neurobiology and Neurogenetics, Max Planck Institute of Psychiatry, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Mathias V Schmidt

    Department of Stress Neurobiology and Neurogenetics, Max Planck Institute of Psychiatry, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3788-2268
  6. Alon Chen

    Department of Neurobiology, Weizmann Institute of Science, Rehovot, Israel
    For correspondence
    Alon.Chen@weizmann.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3625-8233

Funding

H2020 European Research Council (260463)

  • Alon Chen

Israel Science Foundation (1565/15 and 1916/12)

  • Alon Chen

Bundesministerium für Bildung und Forschung (01KU1501A)

  • Alon Chen

Max-Planck-Gesellschaft (Open-access funding)

  • Alon Chen

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

Ethics

Animal experimentation: All experiments were approved by and conducted in accordance with the regulations of the local Animal Care and Use Committee (Government of Upper Bavaria, Munich, Germany), under licenses Az.: 55.2-1-54-2532-148-2012, Az.:55.2-1-54-2532-32-2016 and ROB-55.2-2532.Vet_02-18-50.

Reviewing Editor

  1. Matthew N Hill, University of Calgary, Canada

Publication history

  1. Received: May 8, 2020
  2. Accepted: October 8, 2020
  3. Accepted Manuscript published: October 9, 2020 (version 1)
  4. Version of Record published: November 20, 2020 (version 2)

Copyright

© 2020, Karamihalev 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

  • 2,511
    Page views
  • 370
    Downloads
  • 2
    Citations

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

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)

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

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

  1. Further reading

Further reading

    1. Neuroscience
    Yul HR Kang et al.
    Research Article Updated

    The brain is capable of processing several streams of information that bear on different aspects of the same problem. Here, we address the problem of making two decisions about one object, by studying difficult perceptual decisions about the color and motion of a dynamic random dot display. We find that the accuracy of one decision is unaffected by the difficulty of the other decision. However, the response times reveal that the two decisions do not form simultaneously. We show that both stimulus dimensions are acquired in parallel for the initial ∼0.1 s but are then incorporated serially in time-multiplexed bouts. Thus, there is a bottleneck that precludes updating more than one decision at a time, and a buffer that stores samples of evidence while access to the decision is blocked. We suggest that this bottleneck is responsible for the long timescales of many cognitive operations framed as decisions.

    1. Neuroscience
    Yu Takagi et al.
    Research Article

    Choices rely on a transformation of sensory inputs into motor responses. Using invasive single neuron recordings, the evolution of a choice process has been tracked by projecting population neural responses into state spaces. Here we develop an approach that allows us to recover similar trajectories on a millisecond timescale in non-invasive human recordings. We selectively suppress activity related to three task-axes, relevant and irrelevant sensory inputs and response direction in magnetoencephalography data acquired during context-dependent choices. Recordings from premotor cortex show a progression from processing sensory input to processing the response. In contrast to previous macaque recordings, information related to choice-irrelevant features is represented more weakly than choice-relevant sensory information. To test whether this mechanistic difference between species is caused by extensive overtraining common in non-human primate studies, we trained humans on >20,000 trials of the task. Choice-irrelevant features were still weaker than relevant features in premotor cortex after overtraining.