The neurohormonal basis of social attachment: oxytocin in regulating pair and maternal bonds
DOI:
https://doi.org/10.47611/jsrhs.v12i2.4203Keywords:
pair bonds, maternal bonds, oxytocin, prairie voles, monogamyAbstract
Humans are highly social creatures that form intricate relationships, which makes studying social attachment an important part of behavioral neuroscience. These social relationships can reinforce positive well-being, but also inflict psychological damage when broken. Monogamous species form pair bonds, which are uncommon in the predominantly polygamous mammalian kingdom. Using the prairie vole (Microtus orchogaster), an extensively studied model organism, this review will focus on the role of oxytocin (OT) in both regulating and manipulating systems important for these bonds and discuss the possible consequences of changes to these systems. Because of the nature of these bonds, and how OT regulates the associated neural circuits, this research has important therapeutic value.
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Ahern, T. H., & Young, L. J. (2009). The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (microtus ochrogaster). Frontiers in behavioral neuroscience, 3, 17. https://doi.org/10.3389/neuro.08.017.2009
Ahern, T. H., Hammock, E. A., & Young, L. J. (2011). Parental division of labor, coordination, and the effects of family structure on parenting in monogamous prairie voles (Microtus ochrogaster). Developmental psychobiology, 53(2), 118–131. https://doi.org/10.1002/dev.20498
Argiolas, A., Collu, M., D'Aquila, P., Gessa, G. L., Melis, M. R., & Serra, G. (1989). Apomorphine stimulation of male copulatory behavior is prevented by the oxytocin antagonist d(CH2)5 Tyr(Me)-Orn8-vasotocin in rats. Pharmacology, biochemistry, and behavior, 33(1), 81–83. https://doi.org/10.1016/0091-3057(89)90433-4
Arias Del Razo, R., & Bales, K. L. (2016). Exploration in a dispersal task: Effects of early experience and correlation with other behaviors in prairie voles (Microtus ochrogaster). Behavioural processes, 132, 66–75. https://doi.org/10.1016/j.beproc.2016.10.002
Bales, K. L., van Westerhuyzen, J. A., Lewis-Reese, A. D., Grotte, N. D., Lanter, J. A., & Carter, C. S. (2007). Oxytocin has dose-dependent developmental effects on pair-bonding and alloparental care in female prairie voles. Hormones and behavior, 52(2), 274–279. https://doi.org/10.1016/j.yhbeh.2007.05.004
Bales, K. L., Ardekani, C. S., Baxter, A., Karaskiewicz, C. L., Kuske, J. X., Lau, A. R., Savidge, L. E., Sayler, K. R., & Witczak, L. R. (2021). What is a pair bond?. Hormones and behavior, 136, 105062. https://doi.org/10.1016/j.yhbeh.2021.105062
Bales, K. L., & Saltzman, W. (2016). Fathering in rodents: Neurobiological substrates and consequences for offspring. Hormones and behavior, 77, 249–259. https://doi.org/10.1016/j.yhbeh.2015.05.021
Baracz, S. J., Everett, N. A., Robinson, K. J., Campbell, G. R., & Cornish, J. L. (2020). Maternal separation changes maternal care, anxiety-like behaviour and expression of paraventricular oxytocin and corticotrophin-releasing factor immunoreactivity in lactating rats. Journal of neuroendocrinology, 32(6), e12861. https://doi.org/10.1111/jne.12861
Beery A. K. (2021). Familiarity and Mate Preference Assessment with the Partner Preference Test. Current protocols, 1(6), e173. https://doi.org/10.1002/cpz1.173
Bielsky, I. F., Hu, S. B., Ren, X., Terwilliger, E. F., & Young, L. J. (2005). The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron, 47(4), 503–513. https://doi.org/10.1016/j.neuron.2005.06.031
Blocker, T. D., & Ophir, A. G. (2016). A preference to bond? Male prairie voles form pair bonds even in the presence of multiple receptive females. Animal behaviour, 122, 89–97. https://doi.org/10.1016/j.anbehav.2016.10.007
Bosch, O. J., Dabrowska, J., Modi, M. E., Johnson, Z. V., Keebaugh, A. C., Barrett, C. E., Ahern, T. H., Guo, J., Grinevich, V., Rainnie, D. G., Neumann, I. D., & Young, L. J. (2016). Oxytocin in the nucleus accumbens shell reverses CRFR2-evoked passive stress-coping after partner loss in monogamous male prairie voles.
Psychoneuroendocrinology, 64, 66–78. https://doi.org/10.1016/j.psyneuen.2015.11.011
Carcea, I., Caraballo, N. L., Marlin, B. J., Ooyama, R., Riceberg, J. S., Mendoza Navarro, J. M., Opendak, M., Diaz, V. E., Schuster, L., Alvarado Torres, M. I., Lethin, H., Ramos, D., Minder, J., Mendoza, S. L., Bair-Marshall, C. J., Samadjopoulos, G. H., Hidema, S., Falkner, A., Lin, D., Mar, A., … Froemke, R. C. (2021). Oxytocin neurons enable social transmission of maternal behaviour. Nature, 596(7873), 553–557. https://doi.org/10.1038/s41586-021-03814-7
Carter, C. S., & Getz, L. L. (1993). Monogamy and the prairie vole. Scientific American, 268(6), 100–106. https://doi.org/10.1038/scientificamerican0693-100
Champagne, F., Diorio, J., Sharma, S., & Meaney, M. J. (2001). Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proceedings of the National Academy of Sciences of the United States of America, 98(22), 12736–12741. https://doi.org/10.1073/pnas.221224598
Cho, M. M., DeVries, A. C., Williams, J. R., & Carter, C. S. (1999). The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behavioral neuroscience, 113(5), 1071–1079. https://doi.org/10.1037//0735-7044.113.5.1071
Curtis J. T. (2010). Does fertility trump monogamy?. Animal behaviour, 80(2), 319–328. https://doi.org/10.1016/j.anbehav.2010.05.014
Cushing, B. S., & Carter, C. S. (2000). Peripheral pulses of oxytocin increase partner preferences in female, but not male, prairie voles. Hormones and behavior, 37(1), 49–56. https://doi.org/10.1006/hbeh.1999.1558
Domes, G., Heinrichs, M., Michel, A., Berger, C., & Herpertz, S. C. (2007). Oxytocin improves "mind-reading" in humans. Biological psychiatry, 61(6), 731–733. https://doi.org/10.1016/j.biopsych.2006.07.015
Francis, D. D., Champagne, F. C., & Meaney, M. J. (2000). Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. Journal of neuroendocrinology, 12(12), 1145–1148. https://doi.org/10.1046/j.1365-2826.2000.00599.x
Francis, D. D., Young, L. J., Meaney, M. J., & Insel, T. R. (2002). Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. Journal of neuroendocrinology, 14(5), 349–353. https://doi.org/10.1046/j.0007-1331.2002.00776.x
Getz, L. L., Carter, C. S., & Gavish, L. (1981). The Mating System of the Prairie Vole, Microtus ochrogaster: Field and Laboratory Evidence for Pair-Bonding. Behavioral Ecology and Sociobiology, 8(3), 189–194. http://www.jstor.org/stable/4599380
Guastella, A. J., Gray, K. M., Rinehart, N. J., Alvares, G. A., Tonge, B. J., Hickie, I. B., Keating, C. M., Cacciotti-Saija, C., & Einfeld, S. L. (2015). The effects of a course of intranasal oxytocin on social behaviors in youth diagnosed with autism spectrum disorders: a randomized controlled trial. Journal of child psychology and psychiatry, and allied disciplines, 56(4), 444–452. https://doi.org/10.1111/jcpp.12305
Guastella, A. J., Mitchell, P. B., & Dadds, M. R. (2008). Oxytocin increases gaze to the eye region of human faces. Biological psychiatry, 63(1), 3–5. https://doi.org/10.1016/j.biopsych.2007.06.026
Harbert, K. J., Pellegrini, M., Gordon, K. M., & Donaldson, Z. R. (2020). How prior pair-bonding experience affects future bonding behavior in monogamous prairie voles. Hormones and behavior, 126, 104847. https://doi.org/10.1016/j.yhbeh.2020.104847
He, F., Wang, Z., & Guo, G. (2018). Postnatal separation prevents the development of prenatal stress-induced anxiety in association with changes in oestrogen receptor and oxytocin immunoreactivity in female mandarin vole (Microtus mandarinus) offspring. The European journal of neuroscience, 47(1), 95–108. https://doi.org/10.1111/ejn.13788
Heinrichs, M., Baumgartner, T., Kirschbaum, C., & Ehlert, U. (2003). Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biological psychiatry, 54(12), 1389–1398. https://doi.org/10.1016/s0006-3223(03)00465-7
Heinrichs, M., von Dawans, B., & Domes, G. (2009). Oxytocin, vasopressin, and human social behavior. Frontiers in neuroendocrinology, 30(4), 548–557. https://doi.org/10.1016/j.yfrne.2009.05.005
Hinde, K., Muth, C., Maninger, N., Ragen, B. J., Larke, R. H., Jarcho, M. R., Mendoza, S. P., Mason, W. A., Ferrer, E., Cherry, S. R., Fisher-Phelps, M. L., & Bales, K. L. (2016). Challenges to the Pair Bond: Neural and Hormonal Effects of Separation and Reunion in a Monogamous Primate. Frontiers in behavioral neuroscience, 10, 221. https://doi.org/10.3389/fnbeh.2016.00221
Insel, T. R., & Hulihan, T. J. (1995). A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behavioral neuroscience, 109(4), 782–789. https://doi.org/10.1037//0735-7044.109.4.782
Keebaugh, A. C., & Young, L. J. (2011). Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults. Hormones and behavior, 60(5), 498–504. https://doi.org/10.1016/j.yhbeh.2011.07.018
Keebaugh, A. C., Barrett, C. E., Laprairie, J. L., Jenkins, J. J., & Young, L. J. (2015). RNAi knockdown of oxytocin receptor in the nucleus accumbens inhibits social attachment and parental care in monogamous female prairie voles. Social neuroscience, 10(5), 561–570. https://doi.org/10.1080/17470919.2015.1040893
Kelly, A. M., Hiura, L. C., & Ophir, A. G. (2018). Rapid nonapeptide synthesis during a critical period of development in the prairie vole: plasticity of the paraventricular nucleus of the hypothalamus. Brain structure & function, 223(6), 2547–2560. https://doi.org/10.1007/s00429-018-1640-2
Kenkel, W. M., Perkeybile, A. M., Yee, J. R., & Carter, C. S. (2019). Rewritable fidelity: How repeated pairings and age influence subsequent pair-bond formation in male prairie voles. Hormones and behavior, 113, 47–54. https://doi.org/10.1016/j.yhbeh.2019.04.015
Kleiman D. G. (1977). Monogamy in mammals. The Quarterly review of biology, 52(1), 39–69. https://doi.org/10.1086/409721
Kohlhoff, J., Karlov, L., Dadds, M., Barnett, B., Silove, D., & Eapen, V. (2022). The contributions of maternal oxytocin and maternal sensitivity to infant attachment security. Attachment & human development, 24(4), 525–540. https://doi.org/10.1080/14616734.2021.2018472
Kojima, S., & Alberts, J. R. (2011). Oxytocin mediates the acquisition of filial, odor-guided huddling for maternally-associated odor in preweanling rats. Hormones and behavior, 60(5), 549–558. https://doi.org/10.1016/j.yhbeh.2011.08.003
Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., & Fehr, E. (2005). Oxytocin increases trust in humans. Nature, 435(7042), 673–676. https://doi.org/10.1038/nature03701
Lieberwirth, C., & Wang, Z. (2014). Social bonding: regulation by neuropeptides. Frontiers in neuroscience, 8, 171. https://doi.org/10.3389/fnins.2014.00171
Liu, Y., & Wang, Z. X. (2003). Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience, 121(3), 537–544. https://doi.org/10.1016/s0306-4522(03)00555-4
Lu, Q., Lai, J., Du, Y., Huang, T., Prukpitikul, P., Xu, Y., & Hu, S. (2019). Sexual dimorphism of oxytocin and vasopressin in social cognition and behavior. Psychology research and behavior management, 12, 337–349. https://doi.org/10.2147/PRBM.S192951
Marlin, B. J., Mitre, M., D'amour, J. A., Chao, M. V., & Froemke, R. C. (2015). Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature, 520(7548), 499–504. https://doi.org/10.1038/nature14402
Meyer-Lindenberg, A., Domes, G., Kirsch, P., & Heinrichs, M. (2011). Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nature reviews. Neuroscience, 12(9), 524–538. https://doi.org/10.1038/nrn3044
Naderi, A., Soltanmaohammadi, E., Kaza, V., Barlow, S., Chatzistamou, I., & Kiaris, H. (2021). Persistent effects of pair bonding in lung cancer cell growth in monogamous Peromyscus californicus. eLife, 10, e64711. https://doi.org/10.7554/eLife.64711
Nagasawa, M., Okabe, S., Mogi, K., & Kikusui, T. (2012). Oxytocin and mutual communication in mother-infant bonding. Frontiers in human neuroscience, 6, 31. https://doi.org/10.3389/fnhum.2012.00031
Nardou, R., Lewis, E. M., Rothhaas, R., Xu, R., Yang, A., Boyden, E., & Dölen, G. (2019). Oxytocin-dependent reopening of a social reward learning critical period with MDMA. Nature, 569(7754), 116–120. https://doi.org/10.1038/s41586-019-1075-9
Numan, M., & Young, L. J. (2016). Neural mechanisms of mother-infant bonding and pair bonding: Similarities, differences, and broader implications. Hormones and behavior, 77, 98–112. https://doi.org/10.1016/j.yhbeh.2015.05.015
Olazábal, D. E., & Young, L. J. (2006). Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum. Hormones and behavior, 49(5), 681–687. https://doi.org/10.1016/j.yhbeh.2005.12.010
Olazábal, D. E., & Young, L. J. (2006). Oxytocin receptors in the nucleus accumbens facilitate "spontaneous" maternal behavior in adult female prairie voles. Neuroscience, 141(2), 559–568. https://doi.org/10.1016/j.neuroscience.2006.04.017
Orpen, B. G., & Fleming, A. S. (1987). Experience with pups sustains maternal responding in postpartum rats. Physiology & behavior, 40(1), 47–54. https://doi.org/10.1016/0031-9384(87)90184-3
Pedersen, C. A., & Prange, A. J., Jr (1979). Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proceedings of the National Academy of Sciences of the United States of America, 76(12), 6661–6665. https://doi.org/10.1073/pnas.76.12.6661
Perkeybile, A. M., Griffin, L. L., & Bales, K. L. (2013). Natural variation in early parental care correlates with social behaviors in adolescent prairie voles (Microtus ochrogaster). Frontiers in behavioral neuroscience, 7, 21. https://doi.org/10.3389/fnbeh.2013.00021
Pitkow, L. J., Sharer, C. A., Ren, X., Insel, T. R., Terwilliger, E. F., & Young, L. J. (2001). Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole. The Journal of neuroscience : the official journal of the Society for Neuroscience, 21(18), 7392–7396. https://doi.org/10.1523/JNEUROSCI.21-18-07392.2001
Pournajafi-Nazarloo, H., Kenkel, W., Mohsenpour, S. R., Sanzenbacher, L., Saadat, H., Partoo, L., Yee, J., Azizi, F., & Carter, C. S. (2013). Exposure to chronic isolation modulates receptors mRNAs for oxytocin and vasopressin in the hypothalamus and heart. Peptides, 43, 20–26. https://doi.org/10.1016/j.peptides.2013.02.007
Renfro, C. A., Pesek, D. W., Bobeck, K., & Solomon, N. G. (2009). Does time after pair bond disruption affect subsequent reproduction in the socially monogamous woodland vole (Microtus pinetorum)?. Behavioural processes, 81(1), 60–64. https://doi.org/10.1016/j.beproc.2009.01.008
Ross, H. E., Cole, C. D., Smith, Y., Neumann, I. D., Landgraf, R., Murphy, A. Z., & Young, L. J. (2009). Characterization of the oxytocin system regulating affiliative behavior in female prairie voles. Neuroscience, 162(4), 892–903. https://doi.org/10.1016/j.neuroscience.2009.05.055
Ross, H. E., Freeman, S. M., Spiegel, L. L., Ren, X., Terwilliger, E. F., & Young, L. J. (2009). Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles. The Journal of neuroscience : the official journal of the Society for Neuroscience, 29(5), 1312–1318. https://doi.org/10.1523/JNEUROSCI.5039-08.2009
Rutigliano, G., Rocchetti, M., Paloyelis, Y., Gilleen, J., Sardella, A., Cappucciati, M., Palombini, E., Dell'Osso, L., Caverzasi, E., Politi, P., McGuire, P., & Fusar-Poli, P. (2016). Peripheral oxytocin and vasopressin: Biomarkers of psychiatric disorders? A comprehensive systematic review and preliminary meta-analysis. Psychiatry research, 241, 207–220. https://doi.org/10.1016/j.psychres.2016.04.117
Shi, D.D. et al. (2021). Predictable maternal separation confers adult stress resilience via the medial prefrontal cortex oxytocin signaling pathway in rats. Molecular Psychiatry 26, 7296–7307. https://doi.org/10.1038/s41380-021-01293-w
Sikich, L. et al. (2021). Intranasal Oxytocin in Children and Adolescents with Autism Spectrum Disorder. The New England journal of medicine, 385(16). pp. 1462-1473. https://doi.org/10.1056/nejmoa2103583
Smith, A. S., & Wang, Z. (2014). Hypothalamic oxytocin mediates social buffering of the stress response. Biological psychiatry, 76(4), 281–288. https://doi.org/10.1016/j.biopsych.2013.09.017
Smith, A. S., & Wang, Z. (2012). Salubrious effects of oxytocin on social stress-induced deficits. Hormones and behavior, 61(3), 320–330. https://doi.org/10.1016/j.yhbeh.2011.11.010
Sun, P., Smith, A. S., Lei, K., Liu, Y., & Wang, Z. (2014). Breaking bonds in male prairie vole: long-term effects on emotional and social behavior, physiology, and neurochemistry. Behavioural brain research, 265, 22–31. https://doi.org/10.1016/j.bbr.2014.02.016
Tickerhoof, M. C., & Smith, A. S. (2017). Vasopressinergic Neurocircuitry Regulating Social Attachment in a Monogamous Species. Frontiers in endocrinology, 8, 265. https://doi.org/10.3389/fendo.2017.00265
Tripp, J. A. et al. (2021). Comparative neurotranscriptomics reveal widespread species differences associated with bonding. BMC genomics, 22(1), 399. https://doi.org/10.1186/s12864-021-07720-0
Wang, Z., Smith, W., Major, D. E., & De Vries, G. J. (1994). Sex and species differences in the effects of cohabitation on vasopressin messenger RNA expression in the bed nucleus of the stria terminalis in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus). Brain research, 650(2), 212–218. https://doi.org/10.1016/0006-8993(94)91784-1
Wang, Z., Young, L. J., Liu, Y., & Insel, T. R. (1997). Species differences in vasopressin receptor binding are evident early in development: comparative anatomic studies in prairie and montane voles. The Journal of comparative neurology, 378(4), 535–546.
Williams, J. R., Carter, C. S., & Insel, T. (1992). Partner preference development in female prairie voles is facilitated by mating or the central infusion of oxytocin. Annals of the New York Academy of Sciences, 652, 487–489. https://doi.org/10.1111/j.1749-6632.1992.tb34393.x
Williams, J. R., Catania, K. C., & Carter, C. S. (1992). Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience. Hormones and behavior, 26(3), 339–349. https://doi.org/10.1016/0018-506x(92)90004-f
Yamasue, H., Okada, T., Munesue, T., Kuroda, M., Fujioka, T., Uno, Y., Matsumoto, K., Kuwabara, H., Mori, D., Okamoto, Y., Yoshimura, Y., Kawakubo, Y., Arioka, Y., Kojima, M., Yuhi, T., Owada, K., Yassin, W., Kushima, I., Benner, S., Ogawa, N., … Kosaka, H. (2020). Effect of intranasal oxytocin on the core social symptoms of autism spectrum disorder: a randomized clinical trial. Molecular psychiatry, 25(8), 1849–1858. https://doi.org/10.1038/s41380-018-0097-2
Young, K. A., Liu, Y., & Wang, Z. (2008). The neurobiology of social attachment: A comparative approach to behavioral, neuroanatomical, and neurochemical studies. Comparative biochemistry and physiology. Toxicology & pharmacology : CBP, 148(4), 401–410. https://doi.org/10.1016/j.cbpc.2008.02.004
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