Effects of social defeat on dopamine neurons in the ventral tegmental area in male and female California mice

Greenberg, Gian D.; Steinman, Michael Q.; Doig, Ian E.; Hao, Rebecca; Trainor, Brian C.

doi:10.1111/ejn.13099

Cited by 49Neurotransmitter Receptor Influence on BehaviorStress Responses and CortisolNeuroendocrine regulation and behavior

Effects of social defeat on dopamine neurons in the ventral tegmental area in male and female California mice

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Greenberg, Gian D., Steinman, Michael Q., Doig, Ian E., Hao, Rebecca, Trainor, Brian C.·2015·European Journal of Neuroscience

DOI 10.1111/ejn.13099PMC PMC4715680

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Abstract

Dopamine neurons in the ventral tegmental area (VTA) have important functions related to rewards but are also activated in aversive contexts. Electrophysiology studies suggest that the degree to which VTA dopamine neurons respond to noxious stimuli is topographically organized across the dorsal-ventral extent. We used c-fos immunohistochemistry to examine the responses of VTA dopamine neurons in contexts of social defeat and social approach. Studying monogamous California mice (Peromyscus californicus) allowed us to observe the effects of social defeat on both males and females. Females exposed to three episodes of defeat, but not a single episode, had more tyrosine hydroxylase (TH)/c-fos-positive cells in the ventral (but not dorsal) VTA compared with controls. This observation suggests that repeated exposure to aversive contexts is necessary to trigger activation of VTA dopamine neurons. Defeat did not affect TH/c-fos colocalizations in males. We also examined the long-term effects of defeat on c-fos expression in a social interaction test. As previously reported, defeat reduced social interaction in females but not males. Surprisingly, there were no effects of defeat stress on TH/c-fos colocalizations in any subregion of the VTA. However, females had more TH/c-fos-positive cells than males across the entire VTA, and also had greater c-fos-positive cell counts in posterior subregions of the nucleus accumbens shell. Our results show that dopamine neurons in the VTA are more responsive to social contexts in females and that the ventral VTA in particular is sensitive to aversive contexts.

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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 [51]
In male California mice, social defeat stress did not reduce social interaction behavior.
“In males, social defeat stress did not reduce social interaction behavior, consistent with previous studies (15, 41, 42).”
From Oxytocin receptors in the anteromedial bed nucleus of the stria terminalis promote stress-induced social avoidance in female California mice (2018) · cites this paper as [41]

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Authors: Greenberg, G. D., Steinman, M. Q., Doig, I. E., Hao, R., & Trainor, B. C.
Affiliations: University of California, Davis (US)
Corresponding author: Trainor, Brian C.
ORCID: Trainor, Brian C.
Venue: European Journal of Neuroscience
Publisher: Wiley
Published: 2015-11-22
Volume: 42
Issue: 12
Pages: 3081-3094
ISSN: 0953-816X (ISSN-L)
1460-9568
DOI: 10.1111/ejn.13099
PMC: PMC4715680
OpenAlex: W1922108528
Cited by: 49
References: 85
Citations by year: 2026: 1 · 2025: 4 · 2024: 3 · 2023: 6 · 2022: 3 · 2021: 8 · 2020: 2 · 2019: 3 · 2018: 7 · 2017: 6 · 2016: 6
FWCI: 2.94
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: European Journal of Neuroscience (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Scholar Commons (Santa Clara University) (submittedVersion)
Funders: National Institutes of Health (T32 MH 82174‐3, F31 MH095253, R01 MH097714 01A1)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords: social defeat, ventral tegmental area, dopaminergic neurons, California mouse, Peromyscus californicus, sex differences, c-fos, tyrosine hydroxylase, nucleus accumbens shell, social approach, social interaction, repeated stress
MeSH terms: Animals, Cell Count, Dominance-Subordination, Female, Image Processing, Computer-Assisted, Immunohistochemistry, Male, Motor Activity, Neurons, Peromyscus, Photomicrography, Psychological Tests, Sex Characteristics, Stress, Psychological, Tyrosine 3-Monooxygenase, Proto-Oncogene Proteins c-fos, Ventral Tegmental Area

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Effects of social defeat on dopamine neurons in the ventral tegmental area in male and female California mice

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