Sex Differences in the Embryonic Development of the Central Oxytocin System in Mice
Abstract
Recent studies suggest that oxytocin (OXT) may be important for organising the neural circuitry that underlies adult social behaviour. Although most of the work exploring these effects has focused on early postnatal development, there is evidence that OXT may also be important during foetal development. However, without an understanding of how the OXT system develops, the ability to functionally link OXT in foetal life to adult behaviour is limited. To understand where and when OXT could be acting during embryonic development to affect the organisation of neural substrates, we examined the development of the mouse OXT system from embryonic day (E) 12.5 through postnatal day (PND) 2 using OXT receptor (OXTR) binding and a quantitative polymerase chain reaction. In both males and females, OXTR binding was observed by E16.5 in the ventricular and subventricular zones, as well as the developing amygdala. In males, OXT mRNA was not detectable until PND2, whereas it was detectable by E16.5 in females. OXTR mRNA was detected by E12.5 in both sexes, although females appear to have more OXTR mRNA during foetal development than males. The present study is significant because it is the first to reveal an unexpected sex difference in the development of the OXT system and supports the possibility that OXT during foetal development may contribute to sex differences in adult behaviour.
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?
Sex differences in oxytocin's behavioral effects can be found in rodents.
“Although sex differences in oxytocin and oxytocin receptor distribution have not been reported, sex differences in oxytocin’s behavioral effects can be found in rodents (Miller and Caldwell, 2015; Tamborski et al., 2016; Hammock and Levitt, 2013).”
From Oxytocin neurons mediate the effect of social isolation via the VTA circuits (2022) · cites this paper as Tamborski et al., 2016
Cites
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
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
Lois, C., & Álvarez-Buylla, A. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.5.2074 · Cited by 1,339 · see citing works
Oxytocin in the Medial Amygdala is Essential for Social Recognition in the Mouse
Ferguson, J. N., Aldag, J. M., Insel, T. R., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-20-08278.2001 · Cited by 1,043 · see citing works
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
Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice
Takayanagi, Y., Yoshida, M., Bielsky, I. F., Ross, H. E., Kawamata, M., Onaka, T., Yanagisawa, T., Kimura, T., Matzuk, M. M., Young, L. J., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0505312102 · Cited by 806 · see citing works
Structure and expression of a human oxytocin receptor
Kimura, T., Tanizawa, O., Mori, K., Brownstein, M., & Okayama, H. (1992) · Nature · doi:10.1038/356526a0 · Cited by 631 · see citing works
Tyzio, R., Cossart, R., Khalilov, I., Minlebaev, M., Hübner, C. A., Represa, A., Ben-Ari, Y., & Khazipov, R. (2006) · Science · doi:10.1126/science.1133212 · Cited by 485 · see citing works
Sex 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
Oxytocin and Vasopressin Agonists and Antagonists as Research Tools and Potential Therapeutics
Manning, M., Misicka, A., Olma, A., Bankowski, K., Stoev, S., Chini, B., Durroux, T., Mouillac, B., Corbani, M., & Guillon, G. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2012.02303.x · Cited by 423 · 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
Oxytocin, vasopressin and sociality
CARTER, C., GRIPPO, A., POURNAJAFINAZARLOO, H., RUSCIO, M., & PORGES, S. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00427-5 · Cited by 380 · see citing works
Infant vocalization, adult aggression, and fear behavior of an oxytocin null mutant mouse
Winslow, J. T., Hearn, E. F., Ferguson, J., Young, L. J., Matzuk, M. M., & Insel, T. R. (2000) · Hormones and Behavior · doi:10.1006/hbeh.1999.1566 · Cited by 348 · see citing works
A conditional knockout mouse line of the oxytocin receptor
Lee, H.-J., Caldwell, H. K., Macbeth, A. H., Tolu, S. G., & Young, W. S. (2008) · Endocrinology · doi:10.1210/en.2007-1710 · Cited by 269 · see citing works
Saunders, N. R., Dreifuss, J.-J., Dzięgielewska, K. M., Johansson, P. A., Habgood, M. D., MøllgÃ¥rd, K., & Bauer, H. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00404 · Cited by 261 · 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
Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles
Bales, K. L., Kim, A. J., Lewis-Reese, A. D., & Sue Carter, C. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.01.004 · Cited by 217 · see citing works
Insel, T. R., Gelhard, R., & Shapiro, L. E. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90321-e · Cited by 209 · 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
Dumais, K. M., Bredewold, R., Mayer, T. E., & Veenema, A. H. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.08.012 · Cited by 201 · 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
Developmental Perspectives on Oxytocin and Vasopressin
Hammock, E. A. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.120 · Cited by 177 · see citing works
BARRIER MECHANISMS IN THE BRAIN, II. IMMATURE BRAIN
Saunders, N. R., Habgood, M., & Dziegielewska, K. (1999) · Clinical and Experimental Pharmacology and Physiology · doi:10.1046/j.1440-1681.1999.02987.x · Cited by 173 · see citing works
The blood–CSF barrier explained: when development is not immaturity
Johansson, P. A., Dzięgielewska, K. M., Liddelow, S. A., & Saunders, N. R. (2008) · BioEssays · doi:10.1002/bies.20718 · Cited by 160 · see citing works
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
Bales, K. L., & Carter, C. S. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.4.854 · Cited by 155 · see citing works
Atlas of the developing mouse brain at E 17.5, P0, and P6
Paxinos, G., Halliday, G. M., WATSON, C. R. R., Koutcherov, Y., & Wang, H. (2007) · Elsevier eBooks · Cited by 143 · see citing works
Quick sex determination of mouse fetuses
Lambert, J., Benoit, B. O., Colvin, G. A., Carlson, J. E., Delville, Y., & Quesenberry, P. J. (2000) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(99)00157-0 · Cited by 139 · see citing works
Reduced aggressive behaviour in mice with targeted disruption of the oxytocin gene
DeVries, A. C., Young III, W. S., & Nelson, R. J. (1997) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1997.t01-1-00589.x · Cited by 134 · see citing works
Ramos, L., Hicks, C., Kevin, R., Caminer, A., Narlawar, R., Kassiou, M., & McGregor, I. S. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.125 · Cited by 128 · see citing works
Oxytocin in the Amygdala Facilitates Maternal Aggression
Ferris, C. F., FOOTE, K. B., Meltser, H., PLENBY, M. G., Smith, K. L., & Insel, T. R. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34382.x · Cited by 123 · see citing works
Sexually dimorphic expression of oxytocin binding sites in forebrain and spinal cord of the rat
Uhl-Bronner, S., Waltisperger, E., Martínez-Lorenzana, G., Condes Lara, M., & Freund-Mercier, M. J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.025 · Cited by 123 · see citing works
Buijs, R. M., Velis, D. N., & Swaab, D. F. (1980) · Peptides · doi:10.1016/0196-9781(80)90009-1 · Cited by 121 · see citing works
Hammock, E. A. D. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00195 · Cited by 115 · see citing works
Song, Z., McCann, K. E., McNeill, J. K., Larkin, T. E., Huhman, K. L., & Albers, H. E. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.08.005 · Cited by 111 · see citing works
Impairments in the Initiation of Maternal Behavior in Oxytocin Receptor Knockout Mice
Rich, M. E., deCárdenas, E. J., Lee, H.-J., & Caldwell, H. K. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098839 · Cited by 105 · see citing works
Sex and species differences in plasma oxytocin using an enzyme immunoassay
Kramer, K. M., Cushing, B. S., Carter, C. S., Wu, J., & Ottinger, M. A. (2004) · Canadian Journal of Zoology · doi:10.1139/z04-098 · Cited by 99 · see citing works
Macbeth, A. H., Stepp, J. E., Lee, H.-J., Young, W. S., & Caldwell, H. K. (2010) · Behavioral Neuroscience · doi:10.1037/a0020799 · Cited by 98 · see citing works
Self-citationStructure and expression of the mouse oxytocin receptor gene
Kubota, Y., Kimura, T., Hashimoto, K., Tokugawa, Y., Nobunaga, K., Azuma, C., Saji, F., & Murata, Y. (1996) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(96)03923-8 · Cited by 93 · see citing works
Antiaggressive activity of central oxytocin in male rats
Calcagnoli, F., de Boer, S. F., Althaus, M., den Boer, J. A., & Koolhaas, J. M. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3124-7 · Cited by 90 · see citing works
Schambra, U. B. (2008) · Springer eBooks · doi:10.1007/978-0-387-47093-1 · Cited by 83 · see citing works
Neuroendocrinology of social behavior
Adkins-Regan, E. (2009) · ILAR Journal · doi:10.1093/ilar.50.1.5 · Cited by 81 · see citing works
Krémarik, P., Freund‐Mercier, M. J., & Stoeckel, M. E. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903330304 · Cited by 80 · 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
Tribollet, E., Barberis, C., & Arsenijévic, Y. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00591-x · Cited by 76 · 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
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
Scala-Guenot, D. D., & Strosser, M. T. (1992) · Biochemical Journal · doi:10.1042/bj2840491 · Cited by 59 · see citing works
Caldwell, H. K. (2012) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4614-1704-0_12 · Cited by 58 · 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
Behavioural studies using temporal and spatial inactivation of the oxytocin receptor
LEE, H., CALDWELL, H., MACBETH, A., & YOUNGIII, W. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00407-x · Cited by 49 · see citing works
Self-citationMittaud, P., Labourdette, G., Zingg, H. H., & Guénot, D. (2001) · Glia · doi:10.1002/glia.10029 · 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
Ontogeny of the vasopressin and oxytocin RNAs in the mouse hypothalamus
Jing, X., Ratty, A. K., & Murphy, D. (1998) · Neuroscience Research · doi:10.1016/s0168-0102(98)00017-0 · Cited by 39 · 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
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
Social dominance in male vasopressin 1b receptor knockout mice
Caldwell, H. K., Dike, O. E., Stevenson, E. L., Storck, K. E., & Young, W. S. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.008 · Cited by 34 · see citing works
Caldwell, H. K., & Albers, H. E. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01086.x · Cited by 33 · see citing works
Photoperiodic regulation of vasopressin receptor binding in female Syrian hamsters
Caldwell, H. K., & Albers, H. E. (2004) · Brain Research · doi:10.1016/j.brainres.2003.12.025 · 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
Oxytocin, vasopressin and their interplay with gonadal steroids
Dhakar, M. B., Stevenson, E. L., & Caldwell, H. K. (2013) · Oxytocin, Vasopressin and Related Peptides in the Regulation of Behavior · doi:10.1017/cbo9781139017855.003 · Cited by 20 · see citing works
Self-citationVeinante, P., & Freund-Mercier, M.-J. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970707)383:3
Flagged first, then by citations
Cited by
Sorted by citations
Sheng, J. A., Bales, N. J., Myers, S. A., Bautista, A. I., Roueinfar, M., Hale, T. M., & Handa, R. J. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.601939 · Cited by 418 · see citing works
Oxytocin and vasopressin: powerful regulators of social behavior
Caldwell, H. K. (2017) · The Neuroscientist · doi:10.1177/1073858417708284 · Cited by 216 · see citing works
Self-citationMolecular Mechanisms of Oxytocin Signaling at the Synaptic Connection
Bakos, J., Srancikova, A., Havranek, T., & Bacova, Z. (2018) · Neural Plasticity · doi:10.1155/2018/4864107 · Cited by 104 · 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 and behavior: lessons from knockout mice
Caldwell, H. K., Aulino, E. A., Freeman, A. R., Miller, T. V., & Witchey, S. K. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22431 · Cited by 79 · see citing works
Oxytocin neurons mediate the effect of social isolation via the VTA circuits
Musardo, S., Contestabile, A., Knoop, M., Baud, O., & Bellone, C. (2022) · eLife · doi:10.7554/elife.73421 · Cited by 77 · 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
Oxytocin and sex differences in behavior
Caldwell, H. K. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.02.002 · Cited by 64 · 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
Baracz, S. J., Everett, N. A., & Cornish, J. L. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.08.014 · Cited by 52 · 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
Witchey, S. K., Fuchs, J., & Patisaul, H. B. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.06.007 · Cited by 40 · see citing works
Harshaw, C., Leffel, J. K., & Alberts, J. R. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.12.007 · Cited by 39 · see citing works
Prounis, G. S., Thomas, K., & Ophir, A. G. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24450 · Cited by 36 · 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
An association of intrapartum synthetic oxytocin dosing and the odds of developing autism
Soltys, S., Scherbel, J. R., Kurian, J. R., Diebold, T., Wilson, T. S., Hedden, L., Groesch, K. A., Díaz‐Sylvester, P., Botchway, A., Campbell, P., et al. (2020) · Autism · doi:10.1177/1362361320902903 · Cited by 33 · see citing works
Schmidt, M., Braun, K., Brandwein, C., Rossetti, A. C., Ciurana, S. G., Riva, M. A., Deuschle, M., Bock, J., Gass, P., & Gröger, N. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.06.027 · Cited by 33 · see citing works
The Role of Oxytocin in Abnormal Brain Development: Effect on Glial Cells and Neuroinflammation
Knoop, M. S., Possovre, M.-L., Jacquens, A., Charlet, A., Baud, O., & Darbon, P. (2022) · Cells · doi:10.3390/cells11233899 · Cited by 31 · see citing works
Meng, X., Grandjean, J., Sbrini, G., Schipper, P., Hofwijks, N., Stoop, J., Calabrese, F., & Homberg, J. R. (2022) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.2c00448 · Cited by 32 · 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
Morais, L. H., Golubeva, A. V., Casey, S., Scott, K. A., Costa, A. P., Moloney, G. M., Dinan, T. G., & Cryan, J. F. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01040-3 · Cited by 22 · see citing works
Saad, A. K., Akour, A. A., Mahboob, A. A., Aburuz, S., & Sadek, B. S. (2022) · Pharmaceuticals · doi:10.3390/ph15050612 · 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
Baracz, S. J., Robinson, K. J., Wright, A. L., Turner, A. J., McGregor, I. S., Cornish, J. L., & Everett, N. A. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01336-y · Cited by 23 · see citing works
Sex differences in chronic pain-induced mental disorders: Mechanisms of cerebral circuitry
Shen, Z., Li, W., Chang, W., Yue, N., & Yu, J. M. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1102808 · Cited by 21 · see citing works
Vaidyanathan, R., & Hammock, E. A. D. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12821 · Cited by 20 · see citing works
Neonatal oxytocin gives the tempo of social and feeding behaviors
Muscatelli, F., Matarazzo, V. A., & Chini, B. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1071719 · Cited by 17 · see citing works
Subtle sex differences in vasopressin mRNA expression in the embryonic mouse brain
Aulino, E. A., & Caldwell, H. K. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12835 · Cited by 14 · see citing works
Xie, S., Hu, Y., Fang, L., Chen, S., Botchway, B. O. A., Tan, X., Fang, M., & Hu, Z. (2021) · Reviews in the Neurosciences · doi:10.1515/revneuro-2020-0128 · Cited by 14 · see citing works
Raymond, J. S., Rehn, S., James, M. H., Everett, N. A., & Bowen, M. T. (2024) · Biology of Sex Differences · doi:10.1186/s13293-024-00612-4 · Cited by 12 · see citing works
Taylor, J. H., Cavanaugh, J., & French, J. A. (2017) · Developmental Psychobiology · doi:10.1002/dev.21533 · Cited by 10 · see citing works
Cesarean section delivery is a risk factor of autism-related behaviors in mice
Nagano, M., Saitow, F., Higo, S., Uzuki, M., Mikahara, Y., Akimoto, T., Ozawa, H., Nishimori, K., & Suzuki, H. (2021) · Scientific Reports · doi:10.1038/s41598-021-88437-8 · Cited by 9 · see citing works
Freeman, A. R., Hare, J. F., & Caldwell, H. K. (2019) · Journal of Neuroscience Research · doi:10.1002/jnr.24400 · Cited by 10 · see citing works
Harshaw, C., Lanzkowsky, J., Tran, A.-Q. D., Bradley, A. R., & Jaime, M. (2021) · Hormones and Behavior · doi:10.1016/j.yhbeh.2021.104981 · Cited by 10 · see citing works
PVN-mPFC OT projections modulate pup-directed pup care or attacking in virgin mandarin volesPreprint
Li, L., Li, Y., Huang, C.-H., Hou, W.-J., Lv, Z., Zhang, L.-Z., Qu, Y., Sun, Y., Huang, K., Han, X., et al. (2024) · eLife · doi:10.7554/elife.96543 · Cited by 7 · see citing works
Rethinking the Architecture of Attachment: New Insights into the Role for Oxytocin Signaling
Berendzen, K. M., & Manoli, D. S. (2022) · Affective Science · doi:10.1007/s42761-022-00142-5 · Cited by 9 · see citing works
Aulino, E. A., & Caldwell, H. K. (2021) · Hormones and Behavior · doi:10.1016/j.yhbeh.2021.105026 · Cited by 6 · see citing works
Ramlall, E. K., Hall, M. A. L., Forger, N. G., & Castillo‐Ruiz, A. (2021) · Hormones and Behavior · doi:10.1016/j.yhbeh.2021.105080 · Cited by 4 · see citing works
Effah, F., Nidadavolu, P., Silva, N. K. D. G. T., Wojtowicz, M., Camarini, R., Zimmer, A., & Bailey, A. (2024) · European Journal of Neuroscience · doi:10.1111/ejn.16578 · Cited by 4 · see citing works
Chlorpyrifos and neuroendocrine function: Concerns for research with free-living mammal populations
Mitzel, K. M., & Freeman, A. R. (2025) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2025.114807 · Cited by 3 · see citing works
TPH2 knockout male rats are aggressive, show less anxiety, and exhibit an altered oxytocin systemPreprint
Meng, X., Grandjean, J., Sbrini, G., Schipper, P., Hofwijks, N., Calabrese, F., & Homberg, J. R. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.08.499134 · Cited by 3 · see citing works
Knoop, M. S., Trak, E., Possovre, M.-L., van de Looij, Y., Schirmbeck, G. H., Ceyzériat, K., Pitetti, J.-L., Sanches, E. F., Musardo, S., Millet, P., et al. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106293 · Cited by 2 · see citing works
Ontogenesis of Hypothalamic Neurons in Mammals
Bouret, S. G., & Muscatelli, F. (2021) · Masterclass in neuroendocrinology · doi:10.1007/978-3-030-86630-3_1 · Cited by 1 · see citing works
L’ocytocine, dès la naissance, conditionne le comportement alimentaire et social d’un individu
Muscatelli, F. (2022) · Biologie Aujourd hui · doi:10.1051/jbio/2022017 · Cited by 2 · see citing works
Social Processes in Animals: Individual Differences in Affiliative Capacity
Brown, J., & Hammock, E. A. D. (2025) · Springer eBooks · doi:10.1007/978-3-031-77967-1_11 · Cited by 1 · see citing works
Sommer, E., & Caldwell, H. K. (2025) · Neuroscience Letters · doi:10.1016/j.neulet.2025.138409 · Cited by 1 · see citing works
Oxytocin, Vasopressin, and Development of Social Behavior in Primates
Bales, K. L. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-804042-3.00094-4
Social Living and Rethinking the Concept of “Prosociality”
Caldwell, H. K., & Albers, H. E. (2021) · Cambridge University Press eBooks · doi:10.1017/9781108671187.008
Wilczynski, W., & Brosnan, S. F. (2021) · Cambridge University Press eBooks · doi:10.1017/9781108671187.007
PVN-mPFC OT projections modulates pup-directed pup care or attacking in virgin mandarin volesPreprint
Li, L., He, Z., Yin, L., Huang, C., Hou, W., Lv, Z., Zhang, L., Qu, Y., Sun, Y., Huang, K., et al. (2024) · eLife · doi:10.7554/elife.96543.1
PVN-mPFC OT projections modulates pup-directed pup care or attacking in virgin mandarin volesPreprint
Li, L., Li, Y., Huang, C., Hou, W., Lv, Z., Zhang, L., Qu, Y., Sun, Y., Huang, K., Han, X., et al. (2024) · eLife · doi:10.7554/elife.96543.2
Knoop, M. S., Trak, E., Possovre, M.-L., van de Looij, Y., Schirmbeck, G. H., Ceyzériat, K., Pitetti, J.-L., Sanches, E. F., Musardo, S., Millet, P., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.02.652172
Knoop, M. S., Possovre, M.-L., Trak, E., Pitetti, J.-L., van de Looij, Y., Sanches, E. F., Tsartsalis, S., Pansiot, J., Schirmbeck, G. H., & Baud, O. (2025) · Neurobiology of Disease · doi:10.1016/j.nbd.2025.107250
Bertoni, A. (2019) · theses.fr (ABES) · doi:10.70675/d43fcf44zc66ez47a1zae43zd20439e2b233
- Authors
- Tamborski, S., Mintz, E. M., & Caldwell, H. K.
- Affiliations
- Kent State University (US)
- Corresponding author
- Caldwell, H. K.
- Venue
- Journal of Neuroendocrinology
- Publisher
- Wiley
- Published
- 2016-04
- Volume
- 28
- Issue
- 4
- ISSN
- 0953-8194 (ISSN-L)
- 1365-2826
- OpenAlex
- W2236417990
- Cited by
- 55
- References
- 62
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 5 · 2023: 1 · 2022: 9 · 2021: 12 · 2020: 2 · 2019: 5 · 2018: 7 · 2017: 5 · 2016: 3
- FWCI
- 10.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- NSF IOS (1353859, 1021957)
- Department of Biological Sciences at Kent State University
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- oxytocin, oxytocin receptor, sex differences, embryonic development, fetal development, amygdala, mice
- MeSH terms
- Amygdala, Animals, Cerebral Ventricles, Female, Male, Pregnancy, Radioligand Assay, Sex Characteristics, Time Factors, Receptors, Oxytocin, Embryonic Development, Mice
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