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Cited by 89Neurotransmitter Receptor Influence on BehaviorTreatment of Major DepressionStress Responses and Cortisol

Sex differences in stress-induced social withdrawal: role of brain derived neurotrophic factor in the bed nucleus of the stria terminalis

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Greenberg, Gian D., Laman-Maharg, Abigail, Campi, Katharine L., Voigt, Heather, Orr, Veronica N., Schaal, Leslie, Trainor, Brian C.·2014·Frontiers in Behavioral Neuroscience
DOI 10.3389/fnbeh.2013.00223PMC PMC3885825
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Abstract

Depression and anxiety disorders are more common in women than men, and little is known about the neurobiological mechanisms that contribute to this disparity. Recent data suggest that stress-induced changes in neurotrophins have opposing effects on behavior by acting in different brain networks. Social defeat has been an important approach for understanding neurotrophin action, but low female aggression levels in rats and mice have limited the application of these methods primarily to males. We examined the effects of social defeat in monogamous California mice (Peromyscus californicus), a species in which both males and females defend territories. We demonstrate that defeat stress increases mature brain-derived neurotrophic factor (BDNF) protein but not mRNA in the bed nucleus of the stria terminalis (BNST) in females but not males. Changes in BDNF protein were limited to anterior subregions of the BNST, and there were no changes in the adjacent nucleus accumbens (NAc). The effects of defeat on social withdrawal behavior and BDNF were reversed by chronic, low doses of the antidepressant sertraline. However, higher doses of sertraline restored social withdrawal and elevated BDNF levels. Acute treatment with a low dose of sertraline failed to reverse the effects of defeat. Infusions of the selective tyrosine-related kinase B receptor (TrkB) antagonist ANA-12 into the anterior BNST specifically increased social interaction in stressed females but had no effect on behavior in females naïve to defeat. These results suggest that stress-induced increases in BDNF in the anterior BNST contribute to the exaggerated social withdrawal phenotype observed in females.

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  • Previous work in California mice shows social defeat stress has stronger effects on BNST structure and function in adult females than males.

    “Previous work in California mice (Peromyscus californicus) shows that social defeat stress has stronger effects on BNST structure and function in adult females than males (37, 38) and that these changes drive stress-induced social avoidance and social vigilance (39–41).”

    From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [38]

    The Results (Experiment 1; page unavailable) report that social defeat increased anterior-BNST BDNF in female California mice but not males, and the Conclusions link BNST BDNF signaling to stress-induced social withdrawal. The paper does not report that defeat changed BNST structure, so it supports the sex difference in a BNST molecular response, not the full claim about structure and function. (LLM, conf=0.86)

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  • The BNST plays a key role in modulating stress-induced social avoidance and social vigilance in males and females.

    “The BNST plays a key role in modulating stress-induced social avoidance and social vigilance in males and females (38, 40, 41).”

    From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [38]

    The Results (Experiment 1; page unavailable) report stress-induced social withdrawal in female California mice but no effect of defeat in males. The Discussion links BDNF signaling in the anterior BNST to withdrawal in stressed females. The paper does not establish that the BNST modulates social vigilance or stress-induced avoidance in males. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • These results contrast with adults, where social defeat decreases social approach and increases social vigilance in females but not males.

    “These results contrast with observed sex differences in adults, which show that social defeat decreases social approach (38, 42, 43, 51) and increases social vigilance (40) in females but not males.”

    From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [38]

    The Introduction reports that three episodes of social defeat induce social aversion in female California mice but not males, and the Methods specify that the mice were adults (>3 months old). That supports the decreased-social-approach portion of the claim. The passages found do not report increased social vigilance; in the citing sentence, that point has a separate citation (40). (LLM, conf=0.86)

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Cited by

Sorted by citations

Authors
Greenberg, G. D., Laman-Maharg, A., Campi, K. L., Voigt, H., Orr, V. N., Schaal, L., & Trainor, B. C.
Affiliations
University of California, Davis (US)
Corresponding author
Greenberg, Gian D.
ORCID
Trainor, Brian C.
Venue
Frontiers in Behavioral Neuroscience
Publisher
Frontiers Media SA
Published
2014
Volume
7
Pages
223-223
ISSN
1662-5153 (ISSN-L)
DOI
10.3389/fnbeh.2013.00223
PMC
PMC3885825
OpenAlex
W2074135805
Cited by
89
References
17
Citations by year
2026: 3 · 2025: 3 · 2024: 10 · 2023: 2 · 2022: 5 · 2021: 7 · 2020: 11 · 2019: 4 · 2018: 9 · 2017: 9 · 2016: 9 · 2015: 10 · 2014: 7
FWCI
5.34
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Scholar Commons (Santa Clara University) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • National Institutes of Health
  • National Institute of Mental Health (R01MH097714, R21MH090392, T32MH082174)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords
sex differences, social defeat stress, social withdrawal, brain-derived neurotrophic factor, bed nucleus of the stria terminalis, TrkB receptor, sertraline, ANA-12, California mouse, depression, anxiety, neurotrophins, territorial aggression

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