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Neonatal manipulations of oxytocin alter expression of oxytocin and vasopressin immunoreactive cells in the paraventricular nucleus of the hypothalamus in a gender-specific manner
Abstract
Early postnatal manipulations of oxytocin have long-term behavioral and physiological consequences; the present study examined the hypothesis that oxytocin or its absence influences the subsequent expression of either oxytocin or arginine vasopressin in the CNS. On postnatal day 1 female and male prairie voles (Microtus ochrogaster) received a single i.p. injection of oxytocin (3 microg), oxytocin antagonist (0.3 microg), or 50 microl of isotonic saline or were only handled. On postnatal days 1, 8 and 21, brains were fixed, sectioned and stained for oxytocin or vasopressin immunoreactivity and analyzed as a function of age, treatment and sex. Both oxytocin and vasopressin immunoreactivity were observed on day 1 in the supraoptic and paraventricular nuclei (PVN) of the hypothalamus. Numbers of oxytocin and vasopressin neurons increased with age in both nuclei. Females treated on postnatal day 1 with oxytocin or oxytocin antagonist displayed a significant increase in oxytocin immunoreactivity on day 21 in the PVN. In contrast, males treated with antagonist tended to have decreased vasopressin immunoreactivity in the same region. These results revealed that the effects of neonatal manipulation of oxytocin are age-dependent, site-specific and sexually dimorphic. The long-lasting effects of neonatal exposure to exogenous oxytocin and oxytocin antagonist indicate a role for oxytocin in the development of the CNS during the neonatal period, affecting the development of the oxytocinergic system in females and the vasopressinergic system in males. The developmental effects observed suggest one possible mechanism by which neonatal exposure to oxytocin or neonatal inhibition of endogenous oxytocin produces long-lasting behavioral and physiological alterations and could play a role in the development of male- and female-typical behavior.
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In the citing paper
“Manipulation of OT/AVP levels via direct exposures to exogenous hormones, agonists, or alteration of the social environment can significantly modify the number of OT, AVP, and TH neurons in the PVN, thereby resulting in anxiety-like behavior and alterations of prototypical male and female sociosexual behavior (123–127).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [123]
In the citing paper
“i.p. injections of either OT or OTR antagonist on postnatal day 1 induced sex-specific changes in OT, estrogen receptor alpha (ERα), and V1aR in adult prairie voles.”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Yamamoto et al., 2004
In the citing paper
“in females, but not males, neonatal OT and OTR antagonist both increased OT-immunoreactivity in the PVN”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Yamamoto et al., 2004
In the citing paper
“In female prairie voles, neonates treated with Oxt and an OTA have increases in Oxt immunoreactivity (Oxt-ir) within the PVN by 3 weeks of age.”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [27]
In the citing paper
“Yet, in males, Oxt has no effect on Oxt-ir, but treatment with an OTA does decrease arginine vasopressin (Avp) immunoreactivity in the PVN (27).”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [27]
In the citing paper
“Prairie voles also have a postnatal increase in Oxt peptide expression, with the number of Oxt expressing neurons significantly increasing from PND1 to PND21 in both males and females (27).”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [27]
Citations
Cites
The oxytocin receptor system: structure, function, and regulation
Gimpl, G., & Fahrenholz, F. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.629 · Cited by 3,089
The neurobiology of attachment
Insel, T. R., & Young, L. J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35053579 · Cited by 1,173
Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat
Buijs, R. M., Swaab, D. F., Dogterom, J., & van Leeuwen, F. W. (1978) · Cell and Tissue Research · doi:10.1007/bf00224932 · Cited by 1,029
Paraventricular Nucleus:A Site for the Integration of Neuroendocrine and Autonomic Mechanisms
Swanson, L. W., & Sawchenko, P. E. (2008) · Neuroendocrinology · doi:10.1159/000123111 · Cited by 1,001
A role for central vasopressin in pair bonding in monogamous prairie voles
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. (1993) · Nature · doi:10.1038/365545a0 · Cited by 948 · cited 1×
“A sexually dimorphic response is consistent with patterns seen in adult prairie voles, where OT plays a greater role in the regulation of female behavior (Williams et al., 1994; Cushing and Carter, 2000), while AVP appears to be more important in males ( Winslow et al., 1993; Insel et al., 1998).”
MethodUse of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology
Watson, R. E., Wiegand, S. J., Clough, R. W., & Hoffman, G. E. (1986) · Peptides · doi:10.1016/0196-9781(86)90076-8 · Cited by 933
The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat
Sawchenko, P. E., & Swanson, L. W. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902180202 · Cited by 684
Cho, M. M., DeVries, A. C., Williams, J. R., & Carter, C. S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.1071 · Cited by 529
Williams, J. R., Insel, T. R., Harbaugh, C. R., & Carter, C. S. (1994) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1994.tb00579.x · Cited by 483
Neumann, Wigger, Torner, Holsboer, & Landgraf (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00442.x · Cited by 452
Research works printed but not linked: 1
- Cushing, 2001, Comparison of fixation techniques, Horm Behav, 39, 329
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Effah, F., Silva, N. K. D. G. T., Camarini, R., Joly, F., Rabot, S., Bombail, V., & Bailey, A. (2021) · Developmental Neurobiology · doi:10.1002/dneu.22805 · Cited by 11
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Thomas, N. R. (2014) · Syracuse University Libraries (Syracuse University)
Withuhn, T. F. (2004) · University Libraries (University of Maryland)
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Mazo, M. P. (2014) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r38w3885r
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Nürnberger, J. I., & Stigler, K. (2013) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.718052674.793482799
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Kato, Y., Kuwabara, H., Okada, T., Munesue, T., Benner, S., Kuroda, M., Kojima, M., Yassin, W., Eriguchi, Y., Kameno, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14100733
Kato, Y., Kuwabara, H., Okada, T., Munesue, T., Benner, S., Kuroda, M., Kojima, M., Yassin, W., Eriguchi, Y., Kameno, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14100736
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Metadata
- Authors
- Yamamoto, Y., Cushing, B. S., Kramer, K. M., Epperson, P. D., Hoffman, G. E., & Carter, C. S.
- Affiliations
- University of Illinois Chicago (US)
- University of Maryland, Baltimore (US)
- Corresponding author
- Cushing, B.S
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2004-01
- Volume
- 125
- Issue
- 4
- Pages
- 947-955
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W1975654938
- Cited by
- 155
- References
- 50
- Citations by year
- 2025: 3 · 2024: 3 · 2023: 2 · 2022: 5 · 2021: 10 · 2020: 4 · 2019: 6 · 2018: 10 · 2017: 13 · 2016: 13 · 2015: 12 · 2014: 14 · 2013: 7 · 2012: 6
- FWCI
- 8.34
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- China Scholarship Council
- National Institute of Mental Health (MH 01992, K01MH001992)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD 41293, P01HD038490, HD38490, F32HD041293)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › 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, vasopressin, paraventricular nucleus, hypothalamus, neonatal manipulation, oxytocin antagonist, sex differences, Microtus ochrogaster, supraoptic nucleus, postnatal development, social behavior
- MeSH terms
- Animals, Animals, Newborn, Arginine Vasopressin, Arvicolinae, Female, Image Processing, Computer-Assisted, Immunohistochemistry, Male, Neurons, Oxytocin, Paraventricular Hypothalamic Nucleus, Sexual Behavior, Animal, Sex Factors
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