The DOI matches its Crossref record; 48 of the 50 references it cites were found in a registry or an index.
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
Francis, D. D., Young, L. J., Meaney, M. J., & Insel, T. R. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.0007-1331.2002.00776.x · Cited by 415
Vasopressin and oxytocin receptors in the central nervous system
Tribollet, E., & Barberis, C. (1996) · Critical Reviews™ in Neurobiology · doi:10.1615/critrevneurobiol.v10.i1.60 · Cited by 399
Developmental consequences of oxytocin
Carter, C. S. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00151-3 · Cited by 367
Tribollet, E., Charpak, S., Schmidt, A., Dubois-Dauphin, M., & Dreifuss, J. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-05-01764.1989 · Cited by 228
Whitnall, M., Key, S., Ben-Barak, Y., Ozato, K., & Gainer, H. (1985) · The Journal of Neuroscience · doi:10.1523/jneurosci.05-01-00098.1985 · Cited by 209
Vasopressin-immunoreactive cell bodies in the bed nucleus of the stria terminalis of the rat
van Leeuwen, F., & Caffé, R. (1983) · Cell and Tissue Research · doi:10.1007/bf00211473 · Cited by 206
Bales, K. L., & Carter, C. S. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00154-5 · Cited by 195
Permeability and vascularity of the developing brain: Cerebellum vs cerebral cortex
Johanson, C. E. (1980) · Brain Research · doi:10.1016/0006-8993(80)91155-5 · Cited by 191
Sherman, T., McKelvy, J., & Watson, S. J. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-06-01685.1986 · Cited by 182
Central and peripheral effects of oxytocin administration in prairie voles (Microtus ochrogaster)
Witt, D. M., Carter, C. S., & Walton, D. M. (1990) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(90)90042-g · Cited by 181
Oxytocin, Vasopressin, and the Neuroendocrine Basis of Pair Bond Formation
Insel, T. R., Winslow, J. T., Wang, Z., & Young, L. J. (1998) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-4871-3_28 · Cited by 170
Windle, R. J., Shanks, N., Lightman, S. L., & Ingram, C. D. (1997) · Endocrinology · doi:10.1210/en.138.7.2829 · Cited by 170
Hou-Yu, A., Lamme, A., Zimmerman, E. A., & Silverman, A. (2008) · Neuroendocrinology · doi:10.1159/000124651 · Cited by 160
Bales, K. L., & Carter, C. S. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.4.854 · Cited by 155
Peripheral Pulses of Oxytocin Increase Partner Preferences in Female, but Not Male, Prairie Voles
Cushing, B. S., & Carter, C. S. (2000) · Hormones and Behavior · doi:10.1006/hbeh.1999.1558 · Cited by 136
Ontogeny of oxytocin receptors in rat forebrain: A quantitative study
Shapiro, L. E., & Insel, T. R. (1989) · Synapse · doi:10.1002/syn.890040312 · Cited by 131
The Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00004-8 · Cited by 130
Sex differences in hormonal responses of vasopressin pathways in the rat brain
De Vries, G. J., & Al‐Shamma, H. A. (1990) · Journal of Neurobiology · doi:10.1002/neu.480210503 · Cited by 129
Soman-induced seizures rapidly activate astrocytes and microglia in discrete brain regions
Zimmer, L. A., Ennis, M. J., & Shipley, M. T. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970224)378:4 · Cited by 124
Permeability of the blood-brain barrier to neuropeptides: The case for penetration
Banks, W. A., & Kastin, A. J. (1985) · Psychoneuroendocrinology · doi:10.1016/0306-4530(85)90079-4 · Cited by 122
Interaction among Social Environment, the Hypothalamic–Pituitary–Adrenal Axis, and Behavior
DeVries, A. C. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2002.1780 · Cited by 105
Altstein, M., & Gainer, H. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-11-03967.1988 · Cited by 102
Uvnäs-Moberg, K., Alster, P., Petersson, M., Sohlström, A., & Björkstrand, E. (1998) · Pediatric Research · doi:10.1203/00006450-199803000-00006 · Cited by 94
Developmental effects of oxytocin on stress response: Single versus repeated exposure
KRAMER, K., CUSHING, B., & CARTER, C. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00175-6 · Cited by 79
Andaloro, V. J., Monaghan, D. T., & Rosenquist, T. H. (1998) · Pediatric Research · doi:10.1203/00006450-199801000-00001 · Cited by 79
Differential expression of oxytocin receptor mRNA in the developing rat brain
YOSHIMURA, R., Kimura, T., Watanabe, D., & Kiyama, H. (1996) · Neuroscience Research · doi:10.1016/0168-0102(95)01003-3 · Cited by 68
Getz, L. L., & McGuire, B. (1997) · Canadian Journal of Zoology · doi:10.1139/z97-065 · Cited by 62
Cushing, B. S., Yamamoto, Y., Hoffman, G. E., & Carter, C. S. (2003) · Developmental Brain Research · doi:10.1016/s0165-3806(03)00105-6 · Cited by 62
Ontogenetic changes in vasopressin binding site distribution in rat brain: An autoradiographic study
Petracca, F. M., Baskin, D. G., Díaz, J., & Dorsa, D. M. (1986) · Developmental Brain Research · doi:10.1016/0165-3806(86)90065-9 · Cited by 60
Snijdewint, F. G. M., van Leeuwen, F. W. B., & Gj, B. (1989) · PubMed · Cited by 56
Wang, Z., & Young, L. J. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(97)00138-7 · Cited by 54
Histogenesis of the supraoptic and paraventricular neurosecretory cells of the mouse hypothalamus.
Karim, M. A., & Sloper, J. C. (1980) · PubMed · Cited by 48
The Design of Effectivein VivoAntagonists of Rat Uterus and Milk Ejection Responses to Oxytocin*
Sawyer, W. H., Haldar, J., Gazis, D., SETO, J., Bańkowski, K., Lowbridge, J., TURAN, A., & Manning, M. (1980) · Endocrinology · doi:10.1210/endo-106-1-81 · Cited by 41
The hypothalamic magnocellular neurosecretory system in developing rats
Lipari, E. F., Lipari, D., Gerbino, A., Liberto, D. D., Bellafiore, M., Catalano, M., & Valentino, B. (2009) · European Journal of Histochemistry · doi:10.4081/1626 · Cited by 40
Design of Oxytocin Antagonists, which are more Selective than Atosiban
Manning, M., Stoev, S. B., Cheng, L., Wo, N. C., & Chan, W. Y. (2001) · Journal of Peptide Science · doi:10.1002/psc.339 · Cited by 39
Early exposure to oxytocin affects the age of vaginal opening and first estrus in female rats
Withuhn, T. F., Kramer, K. M., & Cushing, B. S. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00222-1 · Cited by 26
Sohlström, A., Olausson, H., Brismar, K., & Uvnäs‐Moberg, K. (2002) · Neonatology · doi:10.1159/000047198 · Cited by 25
Yang, Y., Ozawa, H., Yuri, K., & Kawata, M. (2000) · Endocrine Journal · doi:10.1507/endocrj.47.601 · Cited by 10
Research works printed but not linked: 1
- Cushing, 2001, Comparison of fixation techniques, Horm Behav, 39, 329
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Sorted by citations
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Lee, H.-J., Macbeth, A. H., Pagani, J., & Young, W. S. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.04.001 · Cited by 1,037
Ditzen, B., Schaer, M., Gabriel, B., Bodenmann, G., Ehlert, U., & Heinrichs, M. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.10.011 · Cited by 805
Dumais, K. M., & Veenema, A. H. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.04.003 · Cited by 520
“Specifically, in females, but not males, neonatal OT and OTR antagonist both increased OTimmunoreactivity in the PVN (Yamamoto et al., 2004).”
BackgroundSex differences in oxytocin and vasopressin: Implications for autism spectrum disorders?
CARTER, C. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.025 · Cited by 432
Exogenous and evoked oxytocin restores social behavior in the Cntnap2 mouse model of autism
Peñagarikano, O., Lázaro, M. T., Lu, X.-H., Gordon, A., Dong, H., Lam, H. A., Peles, E., Maidment, N. T., Murphy, N. P., Yang, X. W., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.3010257 · Cited by 378
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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