Neonatal oxytocin manipulations have long-lasting, sexually dimorphic effects on vasopressin receptors
Open accessAbstract
Developmental exposure to oxytocin (OT) or oxytocin antagonists (OTAs) has been shown to cause long-lasting and often sexually dimorphic effects on social behaviors in prairie voles (Microtus ochrogaster). Because regulation of social behavior in monogamous mammals involves central receptors for OT, arginine vasopressin (AVP), and dopamine, we examined the hypothesis that the long-lasting, developmental effects of exposure to neonatal OT or OTA might reflect changes in the expression of receptors for these peptides. On postnatal day 1, prairie voles were injected intraperitoneally with either OT (1 mg/kg), an OTA (0.1 mg/kg), saline vehicle, or were handled only. At approximately 60 days of age, vasopressin V1a receptors, OT receptors (OTR) and dopamine D2 receptor binding were quantified using receptor autoradiography in brain tissue taken from males and females. Significant treatment effects on V1a binding were found in the bed nucleus of the stria terminalis (BNST), cingulate cortex (CgCtx), mediodorsal thalamus (MdThal), medial preoptic area of the hypothalamus (MPOA), and lateral septum (LS). The CgCtx, MPOA, ventral pallidum, and LS also showed significant sex by treatment interactions on V1a binding. No significant treatment or sex differences were observed for D2 receptor binding. No significant treatment difference was observed for OTR receptor binding, and only a marginal sex difference. Changes in the neuropeptide receptor expression, especially the V1a receptor, may help to explain sexually dimorphic changes in behavior that follow comparable neonatal manipulations.
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Developmental treatments can have particular ramifications to receptor binding and up- or down-regulation of peptide production.
“Developmental treatments can have particular ramifications to receptor binding and up- or down-regulation of peptide production (38,54,74,75).”
From Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles (2013) · cites this paper as [38]
Sex differences in responses to OT are pervasive in both adult voles and in single-dose developmental studies.
“While sex differences in responses to OT are pervasive in both adult voles (3,72) and in single-dose developmental studies (37,38,73)”
From Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles (2013) · cites this paper as [38]
High-dose OT might saturate OT receptors and subsequently bind to vasopressin receptors, to which OT also has binding affinity and which can cause differing and sometimes opposite behavioral effects.
“In other words, high dose OT might saturate OT receptors and subsequently bind to vasopressin receptors, to which OT also has binding affinity and which can cause differing and sometimes opposite behavioral effects (18,38,76,77).”
From Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles (2013) · cites this paper as [38]
There were no sex differences in OTR expression.
“There were no sex differences in OTR expression, consistent with previous reports in other species (53, 54).”
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 [53]
Studies in numerous species provide converging evidence that oxytocin during development can have permanent effects on the brain and behavior.
“Yet, in the last 12 years, there has been a resurgence of research in this area, with studies in numerous species providing converging evidence that Oxt during development can have permanent effects on the brain and behavior (3, 13–29) (see Table 1).”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [15]
In female prairie voles, oxytocin treatment on postnatal day 0 decreases vasopressin 1a receptor binding in the medial preoptic area, BNST, lateral septum, cingulate cortex, and medial thalamus on postnatal day 60.
“Specifically, in female prairie voles, Oxt treatment on PND0 decreases Avpr1a binding in the MPOA, BNST, LS, cingulate cortex (CgCtx), and medial thalamus on PND60”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [15]
In female prairie voles, oxytocin receptor antagonist treatment decreases vasopressin 1a receptor binding only in the BNST and cingulate cortex.
“OTA treatment in females decreases Avpr1a binding only in the BNST and CgCtx”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [15]
In male prairie voles, oxytocin treatment on postnatal day 0 increases vasopressin 1a receptor binding in the cingulate cortex.
“but in males it increases Avpr1a binding in the CgCtx.”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [15]
In male prairie voles, oxytocin receptor antagonist treatment decreases vasopressin 1a receptor binding in the medial preoptic area, BNST, and lateral septum.
“while in males it decreases Avpr1a binding in the MPOA, BNST, and LS (15).”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [15]
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Self-citationOxytocin during Development: Possible Organizational Effects on Behavior
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Perkeybile, A. M., Delaney-Busch, N., Hartman, S., Grimm, K. J., & Bales, K. L. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00191 · Cited by 76 · see citing works
Self-citationSchneider-Hassloff, H., Straube, B., Jansen, A., Nuscheler, B., Wemken, G., Witt, S. H., Rietschel, M., & Kircher, T. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.04.009 · Cited by 71 · see citing works
Is oxytocin a maternal-foetal signalling molecule at birth? Implications for development
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Self-citationOrganizational effects of oxytocin on serotonin innervation
Eaton, J. L., Roache, L., Nguyen, K. N., Cushing, B. S., Troyer, E., Papademetriou, E., & Raghanti, M. A. (2012) · Developmental Psychobiology · doi:10.1002/dev.20566 · Cited by 63 · see citing works
Long-term effects on hypothalamic neuropeptides after developmental exposure to chlorpyrifos in mice
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Effects of neonatal oxytocin manipulation on development of social behaviors in mice
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Postweaning, forebrain-specific perturbation of the oxytocin system impairs fear conditioning
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Early experience and the developmental programming of oxytocin and vasopressin
Sue carter, C., Boone, E. M., & Bales, K. L. (2008) · Neurobiology of the Parental Brain · doi:10.1016/b978-012374285-8.00027-5 · Cited by 14 · see citing works
- Authors
- Bales, K. L., Plotsky, P. M., Young, L. J., Lim, M. M., Grotte, N., Ferrer, E., & Carter, C. S.
- Affiliations
- University of California, Davis (US)
- Emory University (US)
- University of Illinois Chicago (US)
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2007-01
- Volume
- 144
- Issue
- 1
- Pages
- 38-45
- ISSN
- 0306-4522 (ISSN-L)
- PMC
- PMC1774559
- OpenAlex
- W2033597006
- Cited by
- 150
- References
- 61
- Citations by year
- 2026: 5 · 2024: 2 · 2023: 3 · 2022: 6 · 2021: 7 · 2020: 5 · 2019: 7 · 2018: 9 · 2017: 15 · 2016: 12 · 2015: 12 · 2014: 11 · 2013: 10 · 2012: 6
- FWCI
- 8.18
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
- Funders
- National Science Foundation
- National Institutes of Health
- University of Illinois at Chicago
- National Institute of Mental Health (MH-56539, R01MH073022, MH073022, R01MH056538, R01MH056539)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01 HD 38490, P01HD038490, F32 HD08702, F32HD008702)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- oxytocin antagonist, dopamine D2 receptor, oxytocin receptor, sexually dimorphic effects, Microtus ochrogaster, social behavior, monogamy, bed nucleus of the stria terminalis, cingulate cortex, medial preoptic area, lateral septum, mediodorsal thalamus, receptor binding
- MeSH terms
- Animals, Animals, Newborn, Autoradiography, Arvicolinae, Female, Globus Pallidus, Male, Nucleus Accumbens, Ornipressin, Oxytocin, Preoptic Area, Septal Nuclei, Sex Characteristics, Social Behavior, Neostriatum, Receptors, Dopamine D2, Receptors, Vasopressin, Mediodorsal Thalamic Nucleus, Septum of Brain
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