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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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, resulting in anxiety-like behavior and alterations of prototypical male and female sociosexual behavior.
“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]
i.p. injections of either OT or OTR antagonist on postnatal day 1 induced sex-specific changes in OT, ERα, and V1aR in adult prairie voles.
“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 female, but not male, prairie voles, neonatal OT and OTR antagonist both increased OT-immunoreactivity in the PVN.
“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 female prairie voles, neonates treated with oxytocin and an oxytocin receptor antagonist have increases in oxytocin immunoreactivity within the paraventricular nucleus by 3 weeks of age.
“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 male prairie voles, oxytocin has no effect on oxytocin immunoreactivity, but treatment with an oxytocin receptor antagonist decreases arginine vasopressin immunoreactivity in the paraventricular nucleus.
“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]
Prairie voles 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.
“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]
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 · see citing works
The neurobiology of attachment
Insel, T. R., & Young, L. J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35053579 · Cited by 1,173 · see citing works
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 · see citing works
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 · see citing works
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× · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Neumann, Wigger, Torner, Holsboer, & Landgraf (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00442.x · Cited by 452 · see citing works
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 · see citing works
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 · see citing works
Developmental consequences of oxytocin
Carter, C. S. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00151-3 · Cited by 367 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Bales, K. L., & Carter, C. S. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00154-5 · Cited by 195 · see citing works
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 · see citing works
Sherman, T., McKelvy, J., & Watson, S. J. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-06-01685.1986 · Cited by 181 · see citing works
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 · see citing works
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 · see citing works
Windle, R. J., Shanks, N., Lightman, S. L., & Ingram, C. D. (1997) · Endocrinology · doi:10.1210/en.138.7.2829 · Cited by 170 · see citing works
Hou-Yu, A., Lamme, A., Zimmerman, E. A., & Silverman, A. (2008) · Neuroendocrinology · doi:10.1159/000124651 · Cited by 160 · see citing works
Bales, K. L., & Carter, C. S. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.4.854 · Cited by 155 · see citing works
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 · see citing works
Wang, Z., Young, L. J., Liu, Y., & Insel, T. R. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970224)378:4 · Cited by 135 · see citing works
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 · see citing works
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 · see citing works
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 128 · see citing works
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 · see citing works
Altstein, M., & Gainer, H. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-11-03967.1988 · Cited by 102 · see citing works
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 101 · see citing works
Uvnäs-Moberg, K., Alster, P., Petersson, M., Sohlström, A., & Björkstrand, E. (1998) · Pediatric Research · doi:10.1203/00006450-199803000-00006 · Cited by 94 · see citing works
Andaloro, V. J., Monaghan, D. T., & Rosenquist, T. H. (1998) · Pediatric Research · doi:10.1203/00006450-199801000-00001 · Cited by 80 · see citing works
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 · see citing works
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 · see citing works
Getz, L. L., & McGuire, B. (1997) · Canadian Journal of Zoology · doi:10.1139/z97-065 · Cited by 62 · see citing works
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 · see citing works
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 · see citing works
Snijdewint, F. G. M., van Leeuwen, F. W. B., & Gj, B. (1989) · PubMed · Cited by 56 · see citing works
Wang, Z., & Young, L. J. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(97)00138-7 · Cited by 54 · see citing works
Histogenesis of the supraoptic and paraventricular neurosecretory cells of the mouse hypothalamus.
Karim, M. A., & Sloper, J. C. (1980) · PubMed · Cited by 48 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Sohlström, A., Olausson, H., Brismar, K., & Uvnäs‐Moberg, K. (2002) · Neonatology · doi:10.1159/000047198 · Cited by 25 · see citing works
Yang, Y., Ozawa, H., Yuri, K., & Kawata, M. (2000) · Endocrine Journal · doi:10.1507/endocrj.47.601 · Cited by 10 · see citing works
Flagged first, then by citations
2 of the 50 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Oxytocin: The Great Facilitator of Life
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 · see citing works
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 784 · see citing works
Dumais, K. M., & Veenema, A. H. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.04.003 · Cited by 520 · see citing works
“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 · see citing works
Exogenous and evoked oxytocin restores social behavior in the <i>Cntnap2</i> 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 · see citing works
The Interpersonal Dimension of Borderline Personality Disorder: Toward a Neuropeptide Model
Stanley, B., & Siever, L. J. (2009) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.09050744 · Cited by 291 · see citing works
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
Ahern, T. H. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.017.2009 · Cited by 239 · see citing works
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
CUSHING, B., & KRAMER, K. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.001 · Cited by 209 · see citing works
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
Méziane, H., Schaller, F., Bauer, Š., Villard, C., Matarazzo, V. A., Riet, F., Guillon, G., Lafitte, D., Desarménien, M. G., Tauber, M., et al. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.11.010 · Cited by 194 · see citing works
Developmental Perspectives on Oxytocin and Vasopressin
Hammock, E. A. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.120 · Cited by 177 · 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
Bales, K. L., & Carter, C. S. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.4.854 · Cited by 155 · see citing works
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
Developmental experiences and the oxytocin receptor system
Bales, K. L., & Perkeybile, A. M. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.013 · Cited by 142 · see citing works
A psychobiological rationale for oxytocin in the treatment of posttraumatic stress disorder
Olff, M., Langeland, W., Witteveen, A., & Denys, D. (2010) · CNS Spectrums · doi:10.1017/s109285290000047x · Cited by 135 · see citing works
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 128 · see citing works
The neurobiological causes and effects of alloparenting
Kenkel, W. M., Perkeybile, A. M., & Carter, C. S. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22465 · Cited by 120 · see citing works
Bales, K. L., Pfeifer, L. A., & Carter, C. S. (2004) · Developmental Psychobiology · doi:10.1002/dev.10165 · Cited by 107 · see citing works
Hyperglycemia Exacerbates Intracerebral Hemorrhage via the Downregulation of Aquaporin-4
Chiu, C., Chen, C.-C. V., Shen, C., Chin, L., Ma, H.-I., Chuang, H.-Y., Cho, D., Chu, C., & Chang, C. (2013) · Stroke · doi:10.1161/strokeaha.113.675983 · Cited by 104 · see citing works
Oxytocin and vasopressin systems in genetic syndromes and neurodevelopmental disorders
Francis, S. M., Sagar, A., Levin-Decanini, T., Liu, W., Carter, C. S., & Jacob, S. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.021 · Cited by 101 · see citing works
Self-citationProsocial effects of oxytocin in two mouse models of autism spectrum disorders
Teng, B. L., Nonneman, R. J., Agster, K. L., Nikolova, V. D., Davis, T. T., Riddick, N. V., Baker, L. K., Pedersen, C. A., Jarstfer, M. B., & Moy, S. S. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.038 · Cited by 98 · see citing works
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
Lahoud, N., & Maroun, M. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.04.006 · Cited by 87 · see citing works
Dai, Y., Zhang, H., Schön, M., Böckers, T. M., Han, S., Han, J., & Zhang, R. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00355 · Cited by 82 · see citing works
Oxytocin receptor dynamics in the brain across development and species
Vaidyanathan, R., & Hammock, E. A. D. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22403 · 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
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
Oxytocin Modulation of Neural Circuits
Mitre, M., Minder, J. L., Morina, E., Chao, M. V., & Froemke, R. C. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_7 · Cited by 76 · see citing works
Sullivan, A. W., Beach, E. C., Stetzik, L. A., Perry, A., D'Addezio, A. S., Cushing, B. S., & Patisaul, H. B. (2014) · Endocrinology · doi:10.1210/en.2014-1379 · Cited by 79 · see citing works
Song, Z., Tai, F., Yu, C., Wu, R., Zhang, X., Broders, H. G., He, F., & Guo, R. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.05.045 · Cited by 73 · 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
Sannino, S., Chini, B., & Grinevich, V. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22450 · Cited by 70 · see citing works
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
Shao-jun, C., Yang, J.-F., Kong, F., Ren, J., Hao, K., Li, M., Yuan, Y., Chen, X.-C., Yu, R., Li, J., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1404493111 · Cited by 66 · see citing works
Kingsbury, M. A., & Bilbo, S. D. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100794 · Cited by 64 · see citing works
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
Long-term effects on hypothalamic neuropeptides after developmental exposure to chlorpyrifos in mice
Tait, S., Ricceri, L., Venerosi, A., Maranghi, F., Mantovani, A., & Calamandrei, G. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.11696 · Cited by 64 · see citing works
Wang, T., Shi, C., Li, X., Zhang, P., Liu, B., Wang, H., Wang, Y., Yang, Y., Wu, Y., Li, H., et al. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.09.012 · Cited by 62 · see citing works
Oxytocin as Treatment for Social Cognition, Not There Yet
Erdozain, A. M., & Peñagarikano, O. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00930 · Cited by 61 · see citing works
The oxytocin system and early‐life experience‐dependent plastic changes
Onaka, T., & Takayanagi, Y. (2021) · Journal of Neuroendocrinology · doi:10.1111/jne.13049 · Cited by 60 · see citing works
New opportunities in vasopressin and oxytocin research: a perspective from the amygdala.
Stoop, R., Hegoburu, C., & van den Burg, E. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-033904 · Cited by 56 · see citing works
Kramer, K. M., Choe, C., Carter, C. S., & Cushing, B. S. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.07.001 · Cited by 58 · see citing works
Sex Differences in the Embryonic Development of the Central Oxytocin System in Mice
Tamborski, S., Mintz, E. M., & Caldwell, H. K. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12364 · Cited by 55 · see citing works
Bell, A. F., White‐Traut, R. C., & Rankin, K. (2012) · Early Human Development · doi:10.1016/j.earlhumdev.2012.09.017 · Cited by 55 · see citing works
Dhakar, M. B., Rich, M. E., Reno, E. L., Lee, H.-J., & Caldwell, H. K. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.05.007 · Cited by 54 · see citing works
Endocrine Disruption of Vasopressin Systems and Related Behaviors
Patisaul, H. B. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00134 · Cited by 54 · see citing works
Vargas-Martínez, F., Uvnás-Moberg, K., Petersson, M., Olausson, H., & Jiménez-Estrada, I. (2014) · Progress in neurobiology · doi:10.1016/j.pneurobio.2014.10.001 · Cited by 49 · see citing works
Tanaka, K., Osako, Y., & Yuri, K. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.01.029 · Cited by 50 · see citing works
Štefánik, P., Olexová, L., & Kršková, L. (2015) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2015.01.021 · Cited by 49 · see citing works
Effects of neonatal oxytocin manipulations on male reproductive potential in prairie voles
BALES, K., ABDELNABI, M., CUSHING, B., OTTINGER, M., & CARTER, C. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.02.016 · Cited by 47 · see citing works
Muscatelli, F., Desarménien, M. G., Matarazzo, V. A., & Grinevich, V. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_16 · Cited by 46 · see citing works
BDNF-TrkB signaling in oxytocin neurons contributes to maternal behavior
Maynard, K. R., Hobbs, J. W., Phan, B. N., Gupta, A., Rajpurohit, S., Williams, C. A., Rajpurohit, A., Shin, J. H., Jaffe, A. E., & Martinowich, K. (2018) · eLife · doi:10.7554/elife.33676 · Cited by 46 · see citing works
Neuropeptide Regulation of Social Attachment: The Prairie Vole Model
Tabbaa, M., Paedae, B., Liu, Y., & Wang, Z. (2016) · Comprehensive physiology · doi:10.1002/cphy.c150055 · Cited by 53 · see citing works
Birth signalling hormones and the developmental consequences of caesarean delivery
Kenkel, W. M. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12912 · Cited by 45 · see citing works
The two fold role of oxytocin in social developmental disorders: A cause and a remedy?
Lefèvre, A., & Angela Sirigu, B. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.01.011 · Cited by 45 · see citing works
Perkeybile, A. M., & Bales, K. L. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.142182 · Cited by 42 · see citing works
Kim, J. G., Son, Y. J., Yun, C. H., Kim, Y. I., Nam‐Goong, I. S., Park, J. H., Park, S. K., Ojeda, S. R., D'Elia, A. V., Damante, G., et al. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701411200 · Cited by 44 · see citing works
Dannenhoffer, C. A., Kim, E. U., Saalfield, J., Werner, D. F., Varlinskaya, E. I., & SPEAR, L. P. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5003-8 · Cited by 43 · see citing works
Stohn, J. P., Martinez, M. E., Zafer, M., López-Espíndola, D., Keyes, L. M., & Hernández, A. (2017) · Genes Brain & Behavior · doi:10.1111/gbb.12400 · Cited by 41 · see citing works
Zinc and Mercuric Ions Distinguish TRESK from the Other Two-Pore-Domain K+ Channels
Czirják, G., & Enyedi, P. (2005) · Molecular Pharmacology · doi:10.1124/mol.105.018556 · Cited by 40 · see citing works
Guoynes, C. D., Simmons, T. C., Downing, G., Jacob, S., Solomon, M., & Bales, K. L. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.11.037 · Cited by 38 · see citing works
Effects of neonatal oxytocin manipulation on development of social behaviors in mice
Mogi, K., Ooyama, R., Nagasawa, M., & Kikusui, T. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.05.010 · Cited by 37 · see citing works
Freeman, S. M., Ngo, J., Singh, B., Masnaghetti, M., Bales, K. L., & Blevins, J. E. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.07.037 · Cited by 37 · see citing works
Specification of oxytocinergic and vasopressinergic circuits in the developing mouse brain
Madrigal, M. P., & Jurado, S. (2021) · Communications Biology · doi:10.1038/s42003-021-02110-4 · Cited by 38 · see citing works
Kramer, K. M., Yoshida, S., Papademetriou, E., & Cushing, B. S. (2007) · BMC Neuroscience · doi:10.1186/1471-2202-8-71 · Cited by 36 · see citing works
Self-citationJia, R., Tai, F., An, S., Broders, H., & Sun, R. (2008) · Neuropeptides · doi:10.1016/j.npep.2008.06.001 · Cited by 35 · see citing works
Commentary: Oxytocin-gaze positive loop and the coevolution of human–dog bonds
Kekecs, Z., Szollosi, A., Pálfi, B., Szászi, B., Kovács, K., Dienes, Z. P., & Aczél, B. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00155 · Cited by 35 · see citing works
Jankowski, M., Wang, D., Danalache, B. A., Gangal, M., & Gutkowska, J. (2010) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00487.2009 · Cited by 32 · see citing works
Neonatal manipulation of oxytocin influences female reproductive behavior and success
Cushing, B. S., Levine, K., & Cushing, N. L. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.08.004 · Cited by 31 · see citing works
Self-citationQuantitative facial expression analysis revealed the efficacy and time course of oxytocin in autism
Owada, K., Okada, T., Munesue, T., Kuroda, M., Fujioka, T., Uno, Y., Matsumoto, K., Kuwabara, H., Mori, D., Okamoto, Y., et al. (2019) · Brain · doi:10.1093/brain/awz126 · Cited by 29 · see citing works
Early life manipulations of vasopressin-family peptides alter vocal learning
Baran, N. M., Carouso-Peck, S., Kim, T. H., Goldstein, M. H., & Adkins–Regan, E. (2017) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.1114 · Cited by 28 · see citing works
Sexual Differentiation and Sex Differences in Neural Development
Turano, A., Osborne, B. F., & Schwarz, J. M. (2018) · Current topics in behavioral neurosciences · doi:10.1007/7854_2018_56 · Cited by 29 · see citing works
Pournajafi‐Nazarloo, H., Perry, A. N., Partoo, L., Papademeteriou, E., Azizi, F., Carter, C. S., & Cushing, B. S. (2007) · Peptides · doi:10.1016/j.peptides.2007.04.022 · Cited by 28 · see citing works
Baran, N. M., Sklar, N. C., & Adkins–Regan, E. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.10.005 · Cited by 27 · see citing works
Mooney, S. J., & Holmes, M. M. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.11.014 · Cited by 27 · see citing works
Oxytocin receptor binding sites in the periphery of the neonatal mouse
Greenwood, M. A., & Hammock, E. A. D. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172904 · Cited by 27 · see citing works
Perry, A. N., Paramadilok, A., & Cushing, B. S. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.08.021 · Cited by 26 · see citing works
Bakoš, J., Lestanova, Z., Štrbák, V., Havránek, T., & Bačová, Z. (2014) · Neuropeptides · doi:10.1016/j.npep.2014.06.004 · Cited by 24 · see citing works
Pournajafi-Nazarloo, H., Carr, M. S., Papademeteriou, E., Schmidt, J. V., & Cushing, B. S. (2007) · Neuropeptides · doi:10.1016/j.npep.2006.10.002 · Cited by 23 · see citing works
Assentoft, M., Larsen, B. R., Olesen, E. T. B., Fenton, R. A., & MacAulay, N. (2014) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00182.2014 · Cited by 23 · see citing works
Perkeybile, A. M., & Bales, K. L. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.04.024 · Cited by 21 · see citing works
Prato, L. C. D., Zayan, U., Abdallah, D., Point, V., Schaller, F., Pallesi‐Pocachard, E., Montheil, A., Canaan, S., Gaïarsa, J., Muscatelli, F., et al. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01313-5 · Cited by 23 · see citing works
Kelly, A. M., Hiura, L. C., & Ophir, A. G. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1640-2 · Cited by 23 · see citing works
Pohl, M., Shan, Q., Petsch, T., Styp‐Rekowska, B., Matthey, P., Bleich, M., Bachmann, S., & Theilig, F. (2014) · Journal of the American Society of Nephrology · doi:10.1681/asn.2014020148 · Cited by 23 · see citing works
Neuronal morphology alterations in autism and possible role of oxytocin
Falougy, H. E., Filová, B., Ostatníková, D., Bačová, Z., & Bakoš, J. (2019) · Endocrine Regulations · doi:10.2478/enr-2019-0006 · Cited by 22 · see citing works
Lefter, R. M., Ciobica, A. S., Antioch, I., Ababei, D. C., Hrițcu, L. D., & Luca, A.-C. (2020) · Medicina · doi:10.3390/medicina56060267 · Cited by 22 · see citing works
Kasos, E., Kasos, K., Pusztai, F., Polyák, Á., Kovács, K. J., & Varga, K. (2018) · International Journal of Clinical and Experimental Hypnosis · doi:10.1080/00207144.2018.1495009 · Cited by 20 · see citing works
Differential fate between oxytocin and vasopressin cells in the developing mouse brain
Soumier, A., Habart, M., Lio, G., Demily, C., & Angela Sirigu, B. (2021) · iScience · doi:10.1016/j.isci.2021.103655 · Cited by 20 · see citing works
Voles, vasopressin, and infidelity: a molecular basis for monogamy, a platform for ethics, and more?
McKaughan, D. J. (2011) · Biology & Philosophy · doi:10.1007/s10539-011-9303-1 · Cited by 19 · see citing works
γ-Aminobutyric A Receptor (GABAAR) Regulates Aquaporin 4 Expression in the Subependymal Zone
Li, Y., Schmidt-Edelkraut, U., Poetz, F., Oliva, I., Mandl, C., Hölzl‐Wenig, G., Schönig, K., Bartsch, D., & Ciccolini, F. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.618686 · Cited by 19 · see citing works
Neurobiology and the Evolution of Mammalian Social Behavior
Carter, C. S., & Porges, S. W. (2012) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199755059.003.0008 · Cited by 19 · see citing works
Vaidyanathan, R., & Hammock, E. A. D. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12821 · Cited by 20 · see citing works
Feng, T., An, S., Kinden, R., Zhang, X., Jia, R., & Tai, F. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.02.038 · Cited by 18 · see citing works
Monogamy, Motherhood, and Health
Carter, C. S. (2007) · doi:10.1093/acprof:oso/9780195182910.003.0024 · Cited by 17 · see citing works
Baran, N. M., Tomaszycki, M. L., & Adkins–Regan, E. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00058 · Cited by 17 · see citing works
Oxytocin and Social Preference in Female House Mice (Mus musculus domesticus)
Harrison, N., Lopes, P. C., & König, B. (2016) · Ethology · doi:10.1111/eth.12505 · Cited by 17 · see citing works
Borderline personality disorder: current drug treatments and future prospects
Olabi, B., & Hall, J. (2010) · Therapeutic Advances in Chronic Disease · doi:10.1177/2040622310368455 · Cited by 17 · see citing works
- 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
- Social Sciences › Psychology › Social Psychology › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review