An Anxiolytic Action of Oxytocin is Enhanced by Estrogen in the Mouse
Abstract
The established role of oxytocin (OT) in facilitation of steroid-modulated reproductive and affiliative behaviors led to the speculation that it may have anxiolytic actions under certain hormonal conditions. NIH-Swiss mice were tested for responsiveness to OT in two behavioral tests of anxiety, the holeboard apparatus and elevated plus-maze. Dose-response assessment indicated that 3 mg/kg was the optimal dose for peripherally administered (IP) OT on the elevated plus-maze. There were no consistent effects at any dose on the holeboard apparatus. In ovariectomized mice pretreated with estradiol (E2), peripherally administered OT increased the number of entrances onto the open arms, as well as the amount of time on the open arms compared to other groups (ANOVA; p < 0.05). There was little to no effect of OT in ovariectomized animals not pretreated with E2. When OT was administered intracerebroventricularly (ICV), there was an increase in entrances and time on the open arms compared to that of females infused with arginine vasopressin (AVP). This increase was apparent in ovariectomized females, but was further enhanced in those pretreated with E2 (ANOVA; p < 0.05). In contrast, the combination of E2 pretreatment and ICV AVP decreased the number of entrances and time spent on the open arms of the elevated plus-maze compared to those receiving OT, suggesting an estrogen-modulated anxiogenic action of AVP. Analyses of [125]I-OVTA binding density indicated a significant increase in binding density in the lateral septum of E2-treated females compared to OIL-treated controls (ANOVA; p < 0.05). There was no effect of E2 treatment on [125]I-OVTA binding density in the amygdala or ventromedial nucleus of the hypothalamus. Taken together, these data indicate that OT exerts an anxiolytic action that is enhanced in the presence of circulating estrogen. This behavioral effect may be mediated by estrogen-induced increases in OT binding density in the lateral septum and may be important to the facilitation of social interactions.
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Gonadal steroids can act in a synergistic manner to decrease HPA axis gain and anxiety-related behaviors.
“Gonadal steroids can act in a synergistic manner to decrease HPA axis gain and anxiety-related behaviors (Kudwa, McGivern, & Handa, 2014; McCarthy, McDonald, Brooks, & Goldman, 1996)”
From Hypothalamic–pituitary–adrenal and hypothalamic–pituitary–gonadal axes: sex differences in regulation of stress responsivity (2017) · cites this paper as McCarthy, McDonald, Brooks, & Goldman, 1996
Oxytocin production under stress is inhibited by androgens and stimulated by estrogen.
“Oxytocin production under stress is inhibited by androgens and stimulated by estrogen (Jezova et al., 1996; McCarthy, 1995; McCarthy et al., 1996)”
From The Adaptive Calibration Model of stress responsivity (2011) · cites this paper as McCarthy et al., 1996
Experiments in prairie voles reveal central roles for oxytocin in modulating emotional and social behaviors.
“Experiments in prairie voles have revealed central roles for oxytocin in modulating a variety of emotional and social behaviors [164–166].”
From Consensus Paper: Pathological Role of the Cerebellum in Autism (2012) · cites this paper as [164]
Androgens and progesterone modulate oxytocin and oxytocin receptor expression, while estrogens seem to have the greatest impact on the oxytocin system.
“While androgens and progesterone modulate Oxt and Oxtr expression (72–75), it is the estrogens that seem to have the greatest impact on the Oxt system (68, 70, 74, 76–78).”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [78]
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- Authors
- MCCARTHY, M. M., MCDONALD, C. H., BROOKS, P. J., & GOLDMAN, D.
- Affiliations
- University of Maryland, Baltimore (US)
- National Institutes of Health (US)
- Corresponding author
- MCCARTHY, MARGARET M
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 1996-11
- Volume
- 60
- Issue
- 5
- Pages
- 1209-1215
- ISSN
- 0031-9384 (ISSN-L)
- OpenAlex
- W2006179817
- Cited by
- 328
- References
- 31
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 7 · 2023: 6 · 2022: 9 · 2021: 7 · 2020: 10 · 2019: 7 · 2018: 10 · 2017: 11 · 2016: 17 · 2015: 15 · 2014: 20 · 2013: 16 · 2012: 21
- FWCI
- 3.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- oxytocin, estrogen, anxiolytic effects, anxiety, estradiol, ovariectomy, vasopressin, lateral septum, elevated plus maze, intracerebroventricular administration, social behavior, NIH Swiss mice
- MeSH terms
- Animals, Arginine Vasopressin, Autoradiography, Brain, Brain Chemistry, Estradiol, Exploratory Behavior, Female, Injections, Intraventricular, Iodine Radioisotopes, Ovariectomy, Oxytocin, Anti-Anxiety Agents, Receptors, Oxytocin, Mice
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