Abstract
Recent work suggests that key aspects of sensitive parenting (e.g., warmth, emotional attunement) may be shaped in part by biology, specifically the neuropeptide oxytocin. However, some studies have found that oxytocin may not act in expected ways in higher-risk populations (e.g., those with postnatal depression or borderline personality disorder). This study examined the relation between oxytocin and parenting among mothers with varying levels of early life stress. Forty low-income mothers and their 34- to 48-month-old child participated in this study. Mother-child dyads were observed in an interaction task in their home, and videos of these interactions were later coded for parenting behaviors. Mothers’ oxytocin production before and after the interaction task was assessed through saliva. Mothers’ early stress was assessed via the Adverse Childhood Experiences Scale (ACES; Felitti et al. Am J Prev Med 14:245–258, 1998). For mothers with low ACEs, higher oxytocin secretion was associated with more positive parenting. For mothers with high ACEs, higher oxytocin secretion was associated with lower levels of positive parenting. Oxytocin may be operating differently for mothers who experienced harsh early social environments, supporting more defensive behaviors and harsh parenting than anxiolytic and prosocial behaviors.
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References
Amico JA, Levin SC, Cameron JL (2008) Circadian rhythm of oxytocin in the cerebrospinal fluid of rhesus and cynomolgus monkeys: effects of castration and adrenalectomy and presence of a caudal-rostral gradient. Neuroendocrinology 50(6):624–632. https://doi.org/10.1159/000125291
Bakermans-Kranenburg MJ, van IJzendoorn MH, Riem MME, Tops M, Alink LRA (2012) Oxytocin decreases handgrip force in reaction to infant crying in females without harsh parenting experiences. Soc Cogn Affect Neurosci 7(8):951–957. https://doi.org/10.1093/scan/nsr067
Banyard VL (1997) The impact of childhood sexual abuse and family functioning on four dimensions of women’s later parenting. Child Abuse Negl 21(11):1095–1107. https://doi.org/10.1016/S0145-2134(97)00068-9
Barrett J, Fleming AS (2011) Annual research review: all mothers are not created equal: neural and psychobiological perspectives on mothering and the importance of individual differences. J Child Psychol Psychiatry and Allied Disciplines 52(4):368–397. https://doi.org/10.1111/j.1469-7610.2010.02306.x
Bartz JA, Zaki J, Ochsner KN, Bolger N, Kolevzon A, Ludwig N, Lydon JE (2010) Effects of oxytocin on recollections of maternal care and closeness. Proc Natl Acad Sci U S A 107(50):21371–21375. https://doi.org/10.1073/pnas.1012669107
Bartz JA, Simeon D, Hamilton H, Kim S, Crystal S, Braun A et al (2011a) Oxytocin can hinder trust and cooperation in borderline personality disorder. Soc Cogn Affect Neurosci 6(5):556–563. https://doi.org/10.1093/scan/nsq085
Bartz JA, Zaki J, Bolger N, Ochsner KN (2011b) Social effects of oxytocin in humans: context and person matter. Trends Cogn Sci 15(7):301–309. https://doi.org/10.1016/j.tics.2011.05.002
Booth CL, Rose-Krasnor L, McKinnon J-A, Rubin KH (1994) Predicting social adjustment in middle childhood: the role of preschool attachment security and maternal style. Soc Dev 3(3):189–204. https://doi.org/10.1111/j.1467-9507.1994.tb00040.x
Brophy-Herb HE, Stansbury K, Bocknek E, Horodynski MA (2012) Modeling maternal emotion-related socialization behaviors in a low-income sample: relations with toddlers’ self-regulation. Early Child Res Q 27(3):352–364. https://doi.org/10.1016/j.ecresq.2011.11.005
Carter CS (2014) Oxytocin pathways and the evolution of human behavior. Annu Rev Psychol 65(1):17–39. https://doi.org/10.1146/annurev-psych-010213-115110
Carter CS, Pournajafi-Nazarloo H, Kramer KM, Ziegler TE, White-Traut R, Bello D, Schwertz D (2007) Oxytocin: behavioral associations and potential as a salivary biomarker. Ann N Y Acad Sci 1098(1):312–322. https://doi.org/10.1196/annals.1384.006
Champagne F, Meaney MJ (2001) Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 133:287–302. https://doi.org/10.1016/S0079-6123(01)33022-4
Cohen J (1992) A power primer. Psychol Bull 112(1):155–159. https://doi.org/10.1037/0033-2909.112.1.155
Davis MC, Lee J, Horan WP, Clarke AD, McGee MR, Green MF, Marder SR (2013) Effects of single dose intranasal oxytocin on social cognition in schizophrenia. Schizophr Res 147(2–3):393–397. https://doi.org/10.1016/j.schres.2013.04.023
Ditzen B, Schaer M, Gabriel B, Bodenmann G, Ehlert U, Heinrichs M (2009) Intranasal oxytocin increases positive communication and reduces cortisol levels during couple conflict. Biol Psychiatry 65(9):728–731. https://doi.org/10.1016/j.biopsych.2008.10.011
Dwyer CM (2008) Individual variation in the expression of maternal behaviour: a review of the neuroendocrine mechanisms in the sheep. J Neuroendocrinol 20(4):526–534. https://doi.org/10.1111/j.1365-2826.2008.01657.x
Eckstein M, Scheele D, Weber K, Stoffel-Wagner B, Maier W, Hurlemann R (2014) Oxytocin facilitates the sensation of social stress. Hum Brain Mapp 35(9):4741–4750. https://doi.org/10.1002/hbm.22508
Eiden RD, Edwards EP, Leonard KE (2007) A conceptual model for the development of externalizing behavior problems among kindergarten children of alcoholic families: role of parenting and children’s self-regulation. Dev Psychol 43(5):1187–1201. https://doi.org/10.1037/0012-1649.43.5.1187
Enns MW, Cox BJ, Clara I (2002) Parental bonding and adult psychopathology: results from the US National Comorbidity Survey. Psychol Med 32(6):997–1008. https://doi.org/10.1017/S0033291702005937
Febo M, Numan M, Ferris CF (2005) Functional magnetic resonance imaging shows oxytocin activates brain regions associated with mother–pup bonding during suckling. J Neurosci 25(50):11637–11644. https://doi.org/10.1523/JNEUROSCI.3604-05.2005
Feldman R, Gordon I, Schneiderman I, Weisman O, Zagoory-Sharon O (2010) Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 35(8):1133–1141. https://doi.org/10.1016/j.psyneuen.2010.01.013
Feldman R, Gordon I, Zagoory-Sharon O (2011) Maternal and paternal plasma, salivary, and urinary oxytocin and parent-infant synchrony: considering stress and affiliation components of human bonding. Dev Sci 14(4):752–761. https://doi.org/10.1111/j.1467-7687.2010.01021.x
Felitti VJ, Anda RF, Nordenberg D, Williamson DF, Spitz AM, Edwards V et al (1998) Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) Study. Am J Prev Med 14(4):245–258. https://doi.org/10.1016/S0749-3797(98)00017-8
Flinn MV, Ward CV, Noone RJ (2015) Hormones and the human family. In: The handbook of evolutionary psychology. John Wiley & Sons, Inc., Hoboken, pp 552–580. https://doi.org/10.1002/9780470939376.ch19
Forsling ML, Montgomery H, Halpin D, Windle RJ, Treacher DF (1998) Daily patterns of secretion of neurohypophysial hormones in man: effect of age. Exp Physiol 83(3):409–418. https://doi.org/10.1113/expphysiol.1998.sp004124
Galbally M, Lewis AJ, van IJzendoorn MH, Permezel M (2011) The role of oxytocin in mother-infant relations: a systematic review of human studies. Harvard Rev Psychiatry 19(1):1–14. https://doi.org/10.3109/10673229.2011.549771
Graustella AJ, MacLeod C (2012) A critical review of the influence of oxytocin nasal spray on social cognition in humans: evidence and future directions. Horm Behav 61(3):410–418. https://doi.org/10.1016/j.yhbeh.2012.01.002
Guastella AJ, Einfeld SL, Gray KM, Rinehart NJ, Tonge BJ, Lambert TJ, Hickie IB (2010) Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biol Psychiatry 67(7):692–694. https://doi.org/10.1016/j.biopsych.2009.09.020
Gunnar MR, Vazquez DM (2001) Low cortisol and a flattening of expected daytime rhythm: potential indices of risk in human development. Dev Psychopathol 13(3):515–538. https://doi.org/10.1017/S0954579401003066
Huffmeijer R, Alink LRA, Tops M, Grewen KM, Light KC, Bakermans-Kranenburg MJ, van IJzendoorn MH (2013) The impact of oxytocin administration and maternal love withdrawal on event-related potential (ERP) responses to emotional faces with performance feedback. Horm Behav 63(3):399–410. https://doi.org/10.1016/j.yhbeh.2012.11.008
Knutson JF (1995) Psychological characteristics of maltreated children: putative risk factors and consequences. Annu Rev Psychol 46(1):401–431. https://doi.org/10.1146/annurev.ps.46.020195.002153
Kochanska G, Boldt LJ, Kim S, Yoon JE, Philibert RA (2015) Developmental interplay between children’s biobehavioral risk and the parenting environment from toddler to early school age: prediction of socialization outcomes in preadolescence. Dev Psychopathol 27(3):775–790. https://doi.org/10.1017/S0954579414000777
Levine A, Zagoory-Sharon O, Feldman R, Weller A (2007) Oxytocin during pregnancy and early postpartum: individual patterns and maternal-fetal attachment. Peptides 28(6):1162–1169. https://doi.org/10.1016/j.peptides.2007.04.016
Lucassen N, Kok R, Bakermans-Kranenburg MJ, Van Ijzendoorn MH, Jaddoe VWV, Hofman A et al (2015) Executive functions in early childhood: the role of maternal and paternal parenting practices. Br J Dev Psychol 33(4):489–505. https://doi.org/10.1111/bjdp.12112
Lunkenheimer ES, Olson SL, Hollenstein T, Sameroff AJ, Winter C (2011) Dyadic flexibility and positive affect in parent-child coregulation and the development of child behavior problems. Dev Psychopathol 23(2011):577–591. https://doi.org/10.1017/S095457941100006X
Lyons-Ruth K, Block D (1996) The disturbed caregiving system: relations among childhood trauma, maternal caregiving, and infant affect and attachment. Infant Mental Health J 17(3):257–275. https://doi.org/10.1002/(SICI)1097-0355(199623)17:3<257::AID-IMHJ5>3.0.CO;2-L
Maestripieri D (2005) Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proc Natl Acad Sci U S A 102(27):9726–9729. https://doi.org/10.1073/pnas.0504122102
Mah BL, Van IJzendoorn MH, Smith R, Bakermans-Kranenburg MJ (2013) Oxytocin in postnatally depressed mothers: its influence on mood and expressed emotion. Prog Neuro-Psychopharmacol Biol Psychiatry 40(1):267–272. https://doi.org/10.1016/j.pnpbp.2012.10.005
Matthiesen A-S, Ransjo-Arvidson A-B, Nissen E, Uvnas-Moberg K (2001) Postpartum maternal oxytocin release by newborns: effects of infant hand massage and sucking. Birth 28(1):13–19. https://doi.org/10.1046/j.1523-536x.2001.00013.x
Miller AL, Rosenblum KL, Retzloff LB, Lumeng JC (2016) Observed self-regulation is associated with weight in low-income toddlers. Appetite 105:705–712. https://doi.org/10.1016/j.appet.2016.07.007
Moehler E, Biringen Z, Poustka L (2007) Emotional availability in a sample of mothers with a history of abuse. Am J Orthopsychiatry 77(4):624–628. https://doi.org/10.1037/0002-9432.77.4.624
Neumann ID (2007) Stimuli and consequences of dendritic release of oxytocin within the brain. Biochem Soc Trans 35(5):1252–1257. https://doi.org/10.1042/BST0351252
Patterson GR (1998) Continuities—a search for causal mechanisms: comment on the special section. Dev Psychol 34(6):1263–1268. https://doi.org/10.1037/0012-1649.34.6.1263
Pedersen CA, Boccia ML (2002) Oxytocin links mothering received, mothering bestowed and adult stress responses. Stress (Amsterdam, Netherlands) 5(4):259–267. https://doi.org/10.1080/1025389021000037586
Raby KL, Roisman GI, Fraley RC, Simpson JA (2015) The enduring predictive significance of early maternal sensitivity: social and academic competence through age 32 years. Child Dev 86(3):695–708. https://doi.org/10.1111/cdev.12325
Rose J, Roman N, Mwaba K, Ismail K (2017) The relationship between parenting and internalizing behaviours of children: a systematic review. Early Child Dev Care 4430(March):1–19. https://doi.org/10.1080/03004430.2016.1269762
Serbin L, Karp J (2003) Intergenerational studies of parenting and the transfer of risk from parent to child. Curr Dir Psychol Sci 12(4):138–142. https://doi.org/10.1111/1467-8721.01249
Strathearn L, Fonagy P, Amico JA, Montague PR (2009) Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 34(13):2655–2666. https://doi.org/10.1038/npp.2009.103
Uvnäs-Moberg K (1998) Antistress pattern induced by oxytocin. News in Physiol Sci: An Int J Physiol Prod Joint Int Union Physiol Sci Am Physiol Soc 13(1):22–25. https://doi.org/10.1016/0304-3940(95)11335-t
Van Ijzendoorn MH (1992) Intergenerational transmission of parenting: a review of studies in nonclinical populations. Dev Rev 12(1):76–99. https://doi.org/10.1016/0273-2297(92)90004-L
Van IJzendoorn MH, Bakermans-Kranenburg MJ (2012) A sniff of trust: meta-analysis of the effects of intranasal oxytocin administration on face recognition, trust to in-group, and trust to out-group. Psychoneuroendocrinology 37(3):438–443. https://doi.org/10.1016/j.psyneuen.2011.07.008
Wismer Fries AB, Ziegler TE, Kurian JR, Jacoris S, Pollak SD (2005) Early experience in humans is associated with changes in neuropeptides critical for regulating social behavior. Proc Natl Acad Sci 102(47):17237–17240. https://doi.org/10.1073/pnas.0504767102
Zahn-Waxler C, Duggal S, Gruber R (2002) Parental psychopathology. In: Bornstein MH (ed) Handbook of parenting. 2, vol 3. Lawrence Erlbaum Associates, Mahwah, pp 295–327
Zheng J, Babygirija R, Bülbül M, Cerjak D, Ludwig K, Takahashi T (2010) Hypothalamic oxytocin mediates adaptation mechanism against chronic stress in rats. Am J Physiol Gastrointest Liver Physiol 299(4):G946–G953. https://doi.org/10.1152/ajpgi.00483.2009
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The content of this article is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. We thank the families for their participation in our research and to our research team at the University of Michigan for their assistance with data collection and coding.
Funding
This research was supported by Eunice Kennedy Shriver National Institute of Child Health and Human Development grants 1R01HD069179 (PIs JC Lumeng, AL Miller), T32 HD079350 (PI: JC Lumeng), F32HD088029 (PI: JR Doom), National Institute of Diabetes and Digestive Kidney Diseases grant T32 DK071212 (PI: DM Vazquez), and National Institutes of Health CTSA pilot grant UL1TR000433 (PI: AL Miller).
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This study was approved by the [redacted for blind review] Institutional Review Board (protocol number [redacted for blind review]). Mothers provided written informed consent.
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Julian, M.M., Rosenblum, K.L., Doom, J.R. et al. Oxytocin and parenting behavior among impoverished mothers with low vs. high early life stress. Arch Womens Ment Health 21, 375–382 (2018). https://doi.org/10.1007/s00737-017-0798-6
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DOI: https://doi.org/10.1007/s00737-017-0798-6