Developmental consequences of oxytocin

Carter, C.Sue

doi:10.1016/s0031-9384(03)00151-3

Cited by 367Neuroendocrine regulation and behaviorNeuropeptides and Animal PhysiologyStress Responses and Cortisol

Developmental consequences of oxytocin

Carter, C.Sue·2003·Physiology & Behavior

DOI 10.1016/s0031-9384(03)00151-3

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Abstract

This paper examines the developmental effects of the mammalian neuropeptide, oxytocin (OT). In adults, OT is the most abundant neuropeptide in the hypothalamus and serves integrative functions, coordinating behavioral and physiological processes. For example, OT has been implicated in parturition, lactation, maternal behavior and pair bond formation. In addition, OT is capable of moderating behavioral responses to various stressors as well as the reactivity of the hypothalamic-pituitary-adrenal (HPA) axis. Neonates may be exposed to hormones of maternal origin, possibly including peptides administered to the mother in the perinatal period to hasten or delay birth and in milk; however, whether peptide hormones from the mother influence the developing infant remains to be determined. In rodents, endogenous OT is first synthesized during the early postnatal period, although its functions at this time are not well known. Experiments in neonatal prairie voles have documented the capacity of OT and OT receptor antagonists to have immediate and lifelong consequences for social behaviors, including adult pair bonding and parental behaviors, as well as the reactivity of the HPA axis; most of these effects are sexually dimorphic. Possible mechanisms for such effects, including long-lasting changes in OT and vasopressin, are summarized.

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Female prairie voles seem more resilient to developmental manipulations of the oxytocin system, typically responding only at higher doses of oxytocin.
“Females seem more resilient to developmental manipulations, typically responding only at higher dose of OT (19,39).”
From Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles (2013) · cites this paper as [39]
Increased use of oxytocin receptor agonists such as Pitocin and antagonists such as Atosiban during human pregnancy to manage labor timing makes potential fetal oxytocin effects relevant.
“These potential effects are relevant, in part, because of the increased use of Oxtr agonists, such as Pitocin, and antagonists, such as Atosiban, during human pregnancy in order to manage labor timing (95, 96).”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [96]

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Oxytocin shapes the neural circuitry of trust and trust adaptation in humans
Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U., & Fehr, E. (2008) · Neuron · doi:10.1016/j.neuron.2008.04.009 · Cited by 1,258 · see citing works
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Evidence That Oxytocin Exerts Anxiolytic Effects via Oxytocin Receptor Expressed in Serotonergic Neurons in Mice
Yoshida, M., Takayanagi, Y., Inoue, K., Kimura, T., Young, L. J., Onaka, T., & Nishimori, K. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5593-08.2009 · Cited by 608 · see citing works
Mouse Behavioral Assays Relevant to the Symptoms of Autism*
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Intranasal Administration of Oxytocin Increases Envy and Schadenfreude (Gloating)
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A new Mother-to-Infant Bonding Scale: links with early maternal mood
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Empathy toward strangers triggers oxytocin release and subsequent generosity
Barraza, J. A., & Zak, P. J. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04504.x · Cited by 489 · see citing works
Neuropeptides and social behaviour: effects of oxytocin and vasopressin in humans
HEINRICHS, M., & DOMES, G. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00428-7 · Cited by 479 · see citing works
Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders?
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Association of the oxytocin receptor gene (OXTR) in Caucasian children and adolescents with autism
Jacob, S., Brune, C. W., Carter, C. S., Leventhal, B. L., Lord, C., & Cook, E. H. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.02.001 · Cited by 425 · see citing works
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Oxytocin Makes a Face in Memory Familiar
Rimmele, U., Hediger, K., Heinrichs, M., & Klaver, P. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4260-08.2009 · Cited by 402 · see citing works
Is oxytocin “nature’s medicine”
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Oxytocin during pregnancy and early postpartum: Individual patterns and maternal-fetal attachment
Levine, A., Zagoory-Sharon, O., Feldman, R., & Weller, A. (2007) · Peptides · doi:10.1016/j.peptides.2007.04.016 · Cited by 315 · see citing works
The neuroscience of affiliation: forging links between basic and clinical research on neuropeptides and social behavior
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Oxytocin receptors in the nucleus accumbens facilitate “spontaneous” maternal behavior in adult female prairie voles
Olazábal, D. E., & Young, L. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.04.017 · Cited by 289 · see citing works
Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles
Bales, K. L., Perkeybile, A. M., Conley, O. G., Lee, M. H., Guoynes, C. D., Downing, G. M., Yun, C. R., Solomon, M., Jacob, S., & Mendoza, S. P. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.08.025 · Cited by 265 · see citing works
Oxytocin protects against negative behavioral and autonomic consequences of long-term social isolation
Grippo, A. J., Trahanas, D. M., Zimmerman, R. R., Porges, S. W., & Carter, C. S. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.05.017 · Cited by 240 · see citing works
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Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum
Olazábal, D. E., & Young, L. J. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.010 · Cited by 230 · see citing works
A single postnatal injection of oxytocin rescues the lethal feeding behaviour in mouse newborns deficient for the imprinted Magel2 gene
Schaller, F., Watrin, F., Sturny, R., Massacrier, A., Szepetowski, P., & Muscatelli, F. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq424 · Cited by 234 · see citing works
Social approach behaviors in oxytocin knockout mice: comparison of two independent lines tested in different laboratory environments
Crawley, J. N., Chen, T., Puri, A., Washburn, R., Sullivan, T. L., Hill, J. M., Young, N. B., Nadler, J. J., Moy, S. S., Young, L. J., et al. (2007) · Neuropeptides · doi:10.1016/j.npep.2007.02.002 · Cited by 232 · see citing works
Oxytocin and social motivation
Gordon, I., Martin, C., Feldman, R., & Leckman, J. F. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.07.007 · Cited by 211 · see citing works
Oxytocin has dose-dependent developmental effects on pair-bonding and alloparental care in female prairie voles
Bales, K. L., van Westerhuyzen, J. A., Lewis-Reese, A. D., Grotte, N. D., Lanter, J. A., & Carter, C. S. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.05.004 · Cited by 192 · see citing works
Childhood maternal care is associated with DNA methylation of the genes for brain-derived neurotrophic factor ( BDNF ) and oxytocin receptor ( OXTR ) in peripheral blood cells in adult men and women
Unternaehrer, E., Meyer, A. H., Burkhardt, S. C. A., Dempster, E., Staehli, S., Theill, N., Lieb, R., & Meinlschmidt, G. (2015) · Stress · doi:10.3109/10253890.2015.1038992 · Cited by 181 · see citing works
Anterior hypothalamic neural activation and neurochemical associations with aggression in pair-bonded male prairie voles
Gobrogge, K. L., Liu, Y., Jia, X., & Wang, Z. (2007) · Journal of Comparative Neurology · doi:10.1002/cne.21364 · Cited by 178 · see citing works
Consequences of Early Experiences and Exposure to Oxytocin and Vasopressin Are Sexually Dimorphic
Carter, C. S., Boone, E. M., Pournajafi-Nazarloo, H., & Bales, K. L. (2009) · Developmental Neuroscience · doi:10.1159/000216544 · Cited by 176 · see citing works
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Hormonal mechanisms of cooperative behaviour
Soares, M. C., Bshary, R., Fusani, L., Goymann, W., Hau, M., Hirschenhauser, K., & Oliveira, R. F. (2010) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2010.0151 · Cited by 173 · see citing works
Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults
Keebaugh, A. C., & Young, L. J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.07.018 · Cited by 154 · see citing works
Neonatal manipulations of oxytocin alter expression of oxytocin and vasopressin immunoreactive cells in the paraventricular nucleus of the hypothalamus in a gender-specific manner
Yamamoto, Y., Cushing, B. S., Kramer, K. M., Epperson, P. D., Hoffman, G. E., & Carter, C. S. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.02.028 · Cited by 155 · see citing works
Neonatal oxytocin manipulations have long-lasting, sexually dimorphic effects on vasopressin receptors
Bales, K. L., Plotsky, P. M., Young, L. J., Lim, M. M., Grotte, N., Ferrer, E., & Carter, C. S. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.09.009 · Cited by 150 · see citing works
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Urinary oxytocin as a noninvasive biomarker of positive emotion in dogs
Mitsui, S., Yamamoto, M., Nagasawa, M., Mogi, K., Kikusui, T., Ohtani, N., & Ohta, M. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.05.012 · Cited by 147 · see citing works
Elevated salivary levels of oxytocin persist more than 7 h after intranasal administration
van IJzendoorn, M. H., Bhandari, R., van der Veen, R., Grewen, K. M., & Bakermans-Kranenburg, M. J. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00174 · Cited by 137 · see citing works
Oxytocin response to an experimental psychosocial challenge in adults exposed to traumatic experiences during childhood or adolescence
Pierrehumbert, B., Torrisi, R., Laufer, D., Halfon, O., Ansermet, F., & Beck Popovic, M. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2009.12.016 · Cited by 139 · see citing works
Oxytocin Mediates Social Neuroprotection After Cerebral Ischemia
Karelina, K., Stuller, K. A., Jarrett, B., Zhang, N., Wells, J., Norman, G. J., & DeVries, A. C. (2011) · Stroke · doi:10.1161/strokeaha.111.628008 · Cited by 138 · see citing works
Neuropeptides and the social brain: potential rodent models of autism
Lim, M. M., Bielsky, I. F., & Young, L. J. (2005) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.05.006 · Cited by 129 · see citing works
Oxytocin and Estrogen Receptor β in the Brain: An Overview
Acevedo-Rodriguez, A., Mani, S. K., & Handa, R. J. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00160 · Cited by 124 · see citing works
Modeling Social Influences on Human Health
Karelina, K., & DeVries, A. C. (2011) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3182002116 · Cited by 115 · see citing works
The physiology and pharmacology of oxytocin in labor and in the peripartum period
Uvnäs-Moberg, K. (2024) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2023.04.011 · Cited by 118 · see citing works
Oxytocin and appetite
LENG, G., ONAKA, T., CAQUINEAU, C., SABATIER, N., TOBIN, V, & TAKAYANAGI, Y. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00413-5 · Cited by 112 · see citing works
Sex differences and developmental effects of manipulations of oxytocin on alloparenting and anxiety in prairie voles
Bales, K. L., Pfeifer, L. A., & Carter, C. S. (2004) · Developmental Psychobiology · doi:10.1002/dev.10165 · Cited by 107 · see citing works
Obstetrical mode of delivery and childhood behavior and psychological development in a British cohort
Curran, E. A., Cryan, J. F., Kenny, L. C., Dinan, T. G., Kearney, P. M., & Khashan, A. S. (2016) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-015-2616-1 · Cited by 94 · see citing works
CD38 and its role in oxytocin secretion and social behavior
Higashida, H., Yokoyama, S., Kikuchi, M., & Munesue, T. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.011 · Cited by 98 · see citing works
Oxytocin signal and social behaviour: comparison among adult and infant oxytocin, oxytocin receptor and CD38 gene knockout mice
Higashida, H., Lopatina, O., Yoshihara, T., Pichugina, Y. A., Soumarokov, A. A., Munesue, T., Minabe, Y., Kikuchi, M., Ono, Y., Korshunova, N., et al. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.01976.x · Cited by 98 · see citing works
Repeated intranasal oxytocin administration in early life dysregulates the HPA axis and alters social behavior
Rault, J.-L., Carter, C. S., Garner, J. P., Marchant, J. N., Richert, B. T., & Lay, D. C. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.02.007 · Cited by 94 · see citing works
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Inhaled oxytocin increases positive social behaviors in newborn macaques
Simpson, E. A., Sclafani, V., Paukner, A., Hamel, A. F., Novak, M. A., Meyer, J. S., Suomi, S. J., & Ferrari, P. F. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1402471111 · Cited by 82 · see citing works
Oxytocin during Development: Possible Organizational Effects on Behavior
Miller, T. V., & Caldwell, H. K. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00076 · Cited by 79 · see citing works
Oxytocin receptors in brain cortical regions are reduced in haploinsufficient (+/−) reeler mice
Liu, W., Pappas, G. D., & Carter, C. S. (2005) · Neurological Research · doi:10.1179/016164105x35602 · Cited by 73 · see citing works
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Intergenerational transmission of alloparental behavior and oxytocin and vasopressin receptor distribution in the prairie vole
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
Maternal adversities during pregnancy and cord blood oxytocin receptor (OXTR) DNA methylation
Unternaehrer, E., Bolten, M., Nast, I., Staehli, S., Meyer, A. H., Dempster, E., Hellhammer, D. H., Lieb, R., & Meinlschmidt, G. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw051 · Cited by 75 · see citing works
Reproductive behavior of small animals
Kustritz, M. V. R. (2005) · Theriogenology · doi:10.1016/j.theriogenology.2005.05.022 · Cited by 72 · see citing works
Neonatal manipulation of oxytocin affects expression of estrogen receptor alpha
Yamamoto, Y., Carter, C. S., & Cushing, B. S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.065 · Cited by 70 · see citing works
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Is oxytocin a maternal-foetal signalling molecule at birth? Implications for development
Kenkel, W. M., Yee, J. R., & Carter, C. S. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12186 · Cited by 70 · see citing works
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Organizational 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
Effects of social isolation on mRNA expression for corticotrophin-releasing hormone receptors in prairie voles
Pournajafi-Nazarloo, H., Partoo, L., Yee, J., Stevenson, J., Sanzenbacher, L., Kenkel, W., Mohsenpour, S. R., Hashimoto, K., & Carter, C. S. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.10.015 · Cited by 53 · see citing works
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Early life adversity and adult social behavior: focus on arginine vasopressin and oxytocin as potential mediators
Kompier, N. F., Keysers, C., Gazzola, V., Lucassen, P. J., & Krugers, H. J. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00143 · Cited by 53 · see citing works
Chronic exposure to Δ9-tetrahydrocannabinol downregulates oxytocin and oxytocin-associated neurophysin in specific brain areas
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Authors: Carter, C. S.
Affiliations: University of Illinois Chicago (US)
Corresponding author: Carter, C.Sue
ORCID: Carter, C.Sue
Venue: Physiology & Behavior
Publisher: Elsevier BV
Published: 2003-08
Volume: 79
Issue: 3
Pages: 383-397
ISSN: 0031-9384 (ISSN-L)
DOI: 10.1016/s0031-9384(03)00151-3
OpenAlex: W1965138369
Cited by: 367
References: 127
Citations by year: 2026: 3 · 2025: 6 · 2024: 7 · 2023: 6 · 2022: 11 · 2021: 17 · 2020: 13 · 2019: 22 · 2018: 17 · 2017: 18 · 2016: 21 · 2015: 21 · 2014: 24 · 2013: 21 · 2012: 20
FWCI: 2.27
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Physiology & Behavior (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01 HD 38490, P01HD038490)
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, developmental programming, hypothalamus, neonatal development, Microtus ochrogaster, pair bonding, parental behavior, hypothalamic-pituitary-adrenal axis, stress reactivity, maternal hormones, vasopressin, social behavior, sexual dimorphism
MeSH terms: Animals, Behavior, Animal, Brain, Arvicolinae, Female, Humans, Hypothalamo-Hypophyseal System, Male, Neuropeptides, Oxytocin, Pituitary-Adrenal System, Reproduction, Social Behavior, Vasopressins, Mice, Knockout, Mice

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Developmental consequences of oxytocin

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