Sex-specific effects of stress on oxytocin neurons correspond with responses to intranasal oxytocin

Steinman, Michael Q.; Duque-Wilckens, Natalia; Greenberg, Gian D.; Hao, Rebecca; Campi, Katharine L.; Laredo, Sarah A.; Laman-Maharg, Abigail; Manning, Claire E.; Doig, Ian E.; Lopez, Eduardo M.; Walch, Keenan; Bales, Karen L.; Trainor, Brian C.

doi:10.1016/j.biopsych.2015.10.007

Cited by 131Neuroendocrine regulation and behaviorStress Responses and CortisolNeuropeptides and Animal Physiology

Sex-specific effects of stress on oxytocin neurons correspond with responses to intranasal oxytocin

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Steinman, Michael Q., Duque-Wilckens, Natalia, Greenberg, Gian D., Hao, Rebecca, Campi, Katharine L., Laredo, Sarah A., Laman-Maharg, Abigail, Manning, Claire E. +5 more·2016·Biological Psychiatry

DOI 10.1016/j.biopsych.2015.10.007PMC PMC4837091

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Abstract

Background Oxytocin (OT) is considered to be a stress-buffering hormone, dampening the physiologic effects of stress. However, OT can also be anxiogenic. We examined acute and long-lasting effects of social defeat on OT neurons in male and female California mice.Methods We used immunohistochemistry for OT and c-fos cells to examine OT neuron activity immediately after defeat (n = 6-9) and 2 weeks (n = 6-9) and 10 weeks (n = 4-5) later. We quantified Oxt messenger RNA with quantitative polymerase chain reaction (n = 5-9). Intranasal OT was administered to naïve and stressed mice tested in social interaction and resident-intruder tests (n = 8-14).Results Acute exposure to a third episode of defeat increased OT/c-fos colocalizations in the paraventricular nucleus of both sexes. In the medioventral bed nucleus of the stria terminalis, defeat increased Oxt messenger RNA, total OT neurons, and OT/c-fos colocalizations in female mice but not male mice. Intranasal OT failed to reverse stress-induced social withdrawal in female mice and reduced social interaction behavior in female mice naïve to defeat. In contrast, intranasal OT increased social interaction in stressed male mice and reduced freezing in the resident-intruder test.Conclusions Social defeat induces long-lasting increases in OT production and OT/c-fos cells in the medioventral bed nucleus of the stria terminalis of female mice but not male mice. Intranasal OT largely reversed the effects of stress on behavior in male mice, but effects were mixed in female mice. These results suggest that changes in OT-sensitive networks contribute to sex differences in behavioral responses to stress.

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Social defeat stress increases c-fos expression in oxytocin neurons in the PVN.
“Social defeat stress increases c-fos expression in oxytocin neurons in the Paraventricular Nucleus of the Hypothalamus (PVN) (37), a response that has been associated with heightened immediate early gene expression in the anteromedial BNST (40).”
From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [37]
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 [37]
Oxytocin neurons have been reported in the extended medial amygdala (bed nucleus of the stria terminalis and medial amygdala proper) in rats, California mice, and marmosets.
“Oxytocin OXT neurons have been reported in the extended medial amygdala (eg, the BNST and medial amygdala proper [MeA]) in rats (63), California mice (64), and marmosets (65).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [64]
Social defeat increases the activity of OT neurons in the medioventral BNST and PVN in female but not male California mice.
“We previously observed that social defeat increases the activity of OT neurons in the medioventral bed nucleus of the stria terminalis (BNSTmv) and paraventricular nucleus (PVN) in female but not male California mice (15).”
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 [15]
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 [15]

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Inhibition of vasopressin V1a receptors in the medioventral bed nucleus of the stria terminalis has sex- and context-specific anxiogenic effects
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Understanding the Biological Relationship between Migraine and Depression
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The neurocircuitry involved in oxytocin modulation of methamphetamine addiction
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Effects of chronic social defeat on social behaviors in adult female mandarin voles (Microtus mandarinus): Involvement of the oxytocin system in the nucleus accumbens
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Early life social stress and resting state functional connectivity in postpartum rat anterior cingulate circuits
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The social network: Neural control of sex differences in reproductive behaviors, motivation, and response to social isolation
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Combining top-down and bottom-up interventions targeting the vagus nerve to increase resilience
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Sex differences in neural activation following different routes of oxytocin administration in awake adult rats
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Single-Cell Reconstruction of Oxytocinergic Neurons Reveals Separate Hypophysiotropic and Encephalotropic Subtypes in Larval Zebrafish
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Therapeutic uses of oxytocin in stress-related neuropsychiatric disorders
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Circles of engagement: Childhood pain and parent brain
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Brain-Derived Neurotrophic Factor and Oxytocin Signaling in Association With Clinical Symptoms in Adolescent Inpatients With Anorexia Nervosa—A Longitudinal Study
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Mean Girls: Social Stress Models for Female Rodents
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Oxytocin reverses ethanol consumption and neuroinflammation induced by social defeat in male mice
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An acute dose of intranasal oxytocin rapidly increases maternal communication and maintains maternal care in primiparous postpartum California mice
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A vasopressin circuit that modulates mouse social investigation and anxiety-like behavior in a sex-specific manner
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Effects of social defeat on paternal behavior and pair bonding behavior in male California mice (Peromyscus californicus)
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Oxytocin has sex-specific effects on social behaviour and hypothalamic oxytocin immunoreactive cells but not hippocampal neurogenesis in adult rats
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Can intranasal oxytocin reduce craving in automated addictive behaviours? A systematic review
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Rapid nonapeptide synthesis during a critical period of development in the prairie vole: plasticity of the paraventricular nucleus of the hypothalamus
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Exposure to extrinsic stressors, social defeat or bisphenol A, eliminates sex differences in DNA methyltransferase expression in the amygdala
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Sex and hormonal status influence the anxiolytic-like effect of oxytocin in mice
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Effects of Chronic Social Stress and Maternal Intranasal Oxytocin and Vasopressin on Offspring Interferon-γ and Behavior
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Different oxytocin and corticotropin-releasing hormone system changes in bipolar disorder and major depressive disorder patients
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The involvement of oxytocin in the effects of chronic social defeat stress on emotional behaviours in adult female mandarin voles
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Oxytocin Reduces Sensitized Stress–Induced Alcohol Relapse in a Model of Posttraumatic Stress Disorder and Alcohol Use Disorder Comorbidity
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Sex differences in stress reactivity after intranasal oxytocin in recreational cannabis users
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Chronic intranasal oxytocin reverses stress-induced social avoidance in female prairie voles
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Sex differences in chronic pain-induced mental disorders: Mechanisms of cerebral circuitry
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Alteration in oxytocin levels induced by early social environment affects maternal behavior and estrogen receptor alpha in mandarin voles (Microtus mandarinus)
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Oxytocin, Vasopressin and Stress: A Hormetic Perspective
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Oxytocin Signaling Acts as a Marker for Environmental Stressors in Zebrafish
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Oxytocin and Stress Response
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Blending oxytocin and dopamine with everyday creativity
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Oxytocin protects against 3-NP induced learning and memory impairment in rats: Sex differences in behavioral and molecular responses to the context of prenatal stress
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Oxytocin treatments or activation of the paraventricular nucleus-the shell of nucleus accumbens pathway reduce adverse effects of chronic social defeat stress on emotional and social behaviors in Mandarin voles
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Limbic oxytocin receptor expression alters molecular signaling and social avoidance behavior in female prairie voles (Microtus ochrogaster)
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Intranasal oxytocin reduces pre-courtship aggression and increases paternal response in California mice ( Peromyscus californicus )
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Chronic central oxytocin infusion impairs sociability in mandarin voles
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Effects of Chronic and Acute Intranasal Oxytocin Treatments on Temporary Social Separation in Adult Titi Monkeys (Plecturocebus cupreus)
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Oxytocin Signaling as a Target to Block Social Defeat-Induced Increases in Drug Abuse Reward
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Oxytocin reactivity to a lab-based stressor predicts support seeking after stress in daily life: Implications for the Tend-and-Befriend theory
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Oxytocin signaling regulates maternally directed behavior during early life
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Sex and context differences in the effects of trauma on comorbid alcohol use and post‐traumatic stress phenotypes in actively drinking rats
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Intranasal oxytocin drives coordinated social approach
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Activation of kappa opioid receptors in the dorsal raphe have sex dependent effects on social behavior in California mice
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Oxytocin and ‘social hyperthermia’: Interaction with β3-adrenergic receptor-mediated thermogenesis and significance for the expression of social behavior in male and female mice
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Sex-Dependent Effects of Chronic Social Defeat on Emotional and Social Behaviors, and Parameters of Oxytocin and Vasopressin Systems in Mandarin Voles (Microtus mandarinus)
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Revealing the Increased Stress Response Behavior through Transcriptomic Analysis of Adult Zebrafish Brain after Chronic Low to Moderate Dose Rates of Ionizing Radiation
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Leveraging the unique social organization of California mice to study circuit-specific effects of oxytocin on behavior
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Immunoglobulin G is a natural oxytocin carrier which modulates oxytocin receptor signaling: relevance to aggressive behavior in humans
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Molecular programs underlying differences in the expression of mood disorders in males and females
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Intranasal oxytocin, testosterone reactivity, and human competitiveness
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Social behaviour is altered in the insulin-regulated aminopeptidase knockout mouse
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Sex differences in responses to aggressive encounters among California mice
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The Molecular Basis of Love
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Chronic intranasal oxytocin increases acoustic eavesdropping and adult neurogenesis
Monari, P. K., Herro, Z. J., Bymers, J., & Marler, C. A. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105443 · Cited by 6 · see citing works

Oxytocin–Oxytocin Receptor Systems Facilitate Social Defeat Posture in Male Mice
Nasanbuyan, N., Yoshida, M., Takayanagi, Y., Inutsuka, A., Nishimori, K., Yamanaka, A., & Onaka, T. (2017) · Endocrinology · doi:10.1210/en.2017-00606 · Cited by 69 · see citing works
Oxytocin receptors in the anteromedial bed nucleus of the stria terminalis promote stress-induced social avoidance in female California mice
Duque-Wilckens, N., Steinman, M. Q., Busnelli, M., Chini, B., Yokoyama, S., Pham, M., Laredo, S. A., Hao, R., Perkeybile, A. M., Minie, V. A., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.08.024 · Cited by 181 · see citing works
Self-citation
Sex-Dependent Effects of Chronic Social Defeat on Emotional and Social Behaviors, and Parameters of Oxytocin and Vasopressin Systems in Mandarin Voles (Microtus mandarinus)
Hou, W., Ma, H., Xun, Y., Zhang, X., Cai, W., Huang, S., He, Z., Tai, F., & Jia, R. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.625116 · Cited by 10 · see citing works
Sex-dependent regulation of social avoidance by oxytocin signaling in the ventral tegmental area
Grieb, Z. A., Lee, S. D., Stoehr, M. C., Horne, B. W., Norvelle, A., Shaughnessy, E. K., Albers, H. E., & Huhman, K. L. (2024) · Behavioural Brain Research · doi:10.1016/j.bbr.2024.114881 · Cited by 8 · see citing works
Chronic intranasal oxytocin reverses stress-induced social avoidance in female prairie voles
Hale, L. H., Tickerhoof, M. C., & Smith, A. S. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108770 · Cited by 19 · see citing works

Authors: Steinman, M. Q., Duque-Wilckens, N., Greenberg, G. D., Hao, R., Campi, K. L., Laredo, S. A., Laman-Maharg, A., Manning, C. E., Doig, I. E., Lopez, E. M., Walch, K., Bales, K. L., & Trainor, B. C.
Affiliations: University of California, Davis (US)
Corresponding author: Trainor, Brian C.
ORCID: Manning, Claire E.
Bales, Karen L.
Trainor, Brian C.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2016-09
Volume: 80
Issue: 5
Pages: 406-414
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2015.10.007
PMC: PMC4837091
OpenAlex: W2173794558
Cited by: 131
References: 49
Citations by year: 2026: 4 · 2025: 10 · 2024: 9 · 2023: 11 · 2022: 10 · 2021: 24 · 2020: 15 · 2019: 14 · 2018: 17 · 2017: 9 · 2016: 7 · 2015: 1
FWCI: 18.55
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Scholar Commons (Santa Clara University) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
Funders: National Institute on Alcohol Abuse and Alcoholism (T32AA007456)
National Institute of Mental Health (F31MH095253, R01MH085069)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords: oxytocin, social defeat, stress, sex differences, oxytocin neurons, c-fos, paraventricular nucleus, bed nucleus of the stria terminalis, intranasal oxytocin, social interaction, social withdrawal, anxiety
MeSH terms: Administration, Intranasal, Animals, Disease Models, Animal, Female, Male, Neurons, Oxytocin, Paraventricular Hypothalamic Nucleus, RNA, Messenger, Sex Characteristics, Social Behavior, Stress, Psychological, Time Factors, Proto-Oncogene Proteins c-fos, Mice

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Sex-specific effects of stress on oxytocin neurons correspond with responses to intranasal oxytocin

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