Skip to main content

Oxytocin and Human Sensitive and Protective Parenting

  • Chapter
  • First Online:
Behavioral Pharmacology of Neuropeptides: Oxytocin

Abstract

In this chapter we review the evidence for the role of oxytocin in parenting, and discuss some crucial but outstanding questions. This is not meant to be a comprehensive review of all studies on oxytocin and parenting in general. Instead, special attention will be paid to a dimension of parenting that has been largely neglected in behavioral and neurobiological research on parental caregiving, namely protection. Parental protection has received considerable attention in animal research but, despite its evolutionary importance, not in studies on humans. It is argued that oxytocin may have specific significance for the protective dimension of parenting. The effects of exogenous oxytocin may be dependent not only on contextual factors, but also on personal characteristics, most notably gender, on endogenous levels of oxytocin, and on early childhood experiences. Examining the contextual, personal, hormonal, neural, genetic, and behavioral mechanisms of protective parenting in tandem is essential for the development of a comprehensive theory of protective parenting, and for the identification of “biomarkers” for insensitive and unprotective parenting that should be taken into account in preventive parenting interventions.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Abraham E, Hendler T, Shapira-Lichter I et al (2014) Father’s brain is sensitive to childcare experiences. Proc Natl Acad Sci U S A 111:9792–9797

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Abramowitz JS, Schwartz SA, Moore KM (2003) Obsessional thoughts in postpartum females and their partners: content, severity, and relationship with depression. J Clin Psychol Med Settings 10(3):157–164

    Article  Google Scholar 

  • Agran PF, Anderson C, Winn D et al (2003) Rates of pediatric injuries by 3-month intervals for children 0 to 3 years of age. Pediatrics 111(6):e683–e692

    Article  PubMed  Google Scholar 

  • Ainsworth MDS (1967) Infancy in Uganda. Johns Hopkins Press, Baltimore

    Google Scholar 

  • Ainsworth MDS, Bell S, Stayton D (1974) Infant-mother attachment and social development. In: Richards MP (ed) The introduction of the child into a social world. Cambridge University Press, Cambridge, pp 99–135

    Google Scholar 

  • Arakawa H, Arakawa K, Deak T (2010) Oxytocin and vasopressin in the medial amygdala differentially modulate approach and avoidance behavior toward illness-related social odor. Neuroscience 171:1141–1151

    Article  PubMed  CAS  Google Scholar 

  • Atzil S, Hendler T, Zagoory-Sharon O et al (2012) Synchrony and specificity in the maternal and the paternal brain: relations to oxytocin and vasopressin. J Am Acad Child Adolesc Psychiatry 51(8):798–811

    Article  PubMed  Google Scholar 

  • Bakermans-Kranenburg MJ, Van IJzendoorn MH (2013) Sniffing around oxytocin: review and meta-analyses of trials in healthy and clinical groups with implications for pharmacotherapy. Transl Psychiatry 3(5):e258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bakermans-Kranenburg MJ, Van IJzendoorn MH (2017) Protective parenting: neurobiological and behavioral dimensions. Curr Opin Psychol 15:45–49

    Article  PubMed  Google Scholar 

  • Bakermans-Kranenburg MJ, Van IJzendoorn MH, Juffer F (2003) Less is more: meta-analyses of sensitivity and attachment interventions in early childhood. Psychol Bull 129(2):195–215

    Article  PubMed  Google Scholar 

  • Bakermans-Kranenburg MJ, Van IJzendoorn MH, Riem MME et al (2012) Oxytocin decreases handgrip force in reaction to infant crying in females without harsh parenting experiences. Soc Cogn Affect Neurosci 7:951–957

    Article  PubMed  Google Scholar 

  • Berg SJ, Wynne-Edwards KE (2002) Salivary hormone concentrations in mothers and fathers becoming parents are not correlated. Horm Behav 42:424–436

    Article  PubMed  CAS  Google Scholar 

  • Bernal J (1972) Crying during the first 10 days of life, and maternal responses. Dev Med Child Neurol 14(3):362–372

    Article  PubMed  CAS  Google Scholar 

  • Bethlehem RAI, Baron-Cohen S, Van Honk J et al (2014) The oxytocin paradox. Front Behav Neurosci 8(48):1–5

    Google Scholar 

  • Bhandari R, Van der Veen R, Parsons CE et al (2014) Effects of intranasal oxytocin administration on memory for infant cues: moderation by childhood emotional treatment. Soc Neurosci 9(5):536–547

    Article  PubMed  Google Scholar 

  • Bick J, Dozier M (2010) Mothers’ and children’s concentrations of oxytocin following close, physical interactions with biological and non-biological children. Dev Psychobiol 52(1):100–107

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bos PA, Hermans EJ, Montoya ER et al (2010) Testosterone administration modulates neural responses to crying infants in young females. Psychoneuroendocrinology 35:114–121

    Article  PubMed  CAS  Google Scholar 

  • Bosch OJ, Meddle SL, Beiderbeck DI et al (2005) Brain oxytocin correlates with maternal aggression: link to anxiety. J Neurosci 25(29):6807–6815

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bowlby J (1969/1982) Attachment, Attachment and loss, vol 1. Penguin Books, Harmondsworth

    Google Scholar 

  • Bugental DB, Lewis JC, Lin E et al (1999) In charge but not in control: the management of teaching relationships by adults with low perceived power. Dev Psychol 35(6):1367

    Article  PubMed  CAS  Google Scholar 

  • Campbell A (2008) Attachment, aggression and affiliation: the role of oxytocin in female social behavior. Biol Psychol 77:1–10

    Article  PubMed  Google Scholar 

  • Carter CS (1998) Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 23:779–818

    PubMed  CAS  Google Scholar 

  • Caughey SD, Klampfl SM, Bishop VR et al (2011) Changes in the intensity of maternal aggression and central oxytocin and vasopressin V1a receptors across the peripartum period in the rat. J Neuroendocrinol 23:1113–1124

    Article  PubMed  CAS  Google Scholar 

  • Champagne FA (2008) Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29(3):386–397

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choleris E, Devidze N, Kavaliers M et al (2008) Steroidal/neuropeptide interactions in hypothalamus and amygdala related to social anxiety. Prog Brain Res 170:291–303

    Article  PubMed  CAS  Google Scholar 

  • Churchland PS, Winkielman P (2012) Modulating social behavior with oxytocin: how does it work? What does it mean? Horm Behav 61(3):392–399

    Article  PubMed  CAS  Google Scholar 

  • Crouch JL, Skowronski JJ, Milner JS et al (2008) Parental responses to infant crying: the influence of child physical abuse risk and hostile priming. Child Abuse Negl 32:702–710

    Article  PubMed  Google Scholar 

  • De Dreu CKW, Greer LL, Handgraag MJ et al (2010) The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science 328(5984):1408–1411

    Article  PubMed  CAS  Google Scholar 

  • De Geest K, Thiery M, Piron-Possuyt G et al (1985) Plasma oxytocin in human pregnancy and parturition. J Perinat Med 13(1):3–13

    Article  PubMed  Google Scholar 

  • De Wolff MS, Van IJzendoorn MH (1997) Sensitivity and attachment: a meta-analysis on parental antecedents of infant attachment. Child Dev 68(4):571–591

    Article  PubMed  Google Scholar 

  • Denson TF, Mehta PH, Tan DH (2013) Endogenous testosterone and cortisol jointly influence reactive aggression in women. Psychoneuroendocrinology 38(3):416–424

    Article  PubMed  CAS  Google Scholar 

  • Depue RA, Morrone-Strupinsky JV (2005) A neurobehavioral model of affiliative bonding: implications for conceptualizing a human trait of affiliation. Behav Brain Sci 28:313–350

    PubMed  Google Scholar 

  • Domes G, Heinrichs M, Glascher J et al (2007) Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol Psychiatry 62:1187–1190

    Article  PubMed  CAS  Google Scholar 

  • Domes G, Lischke A, Berger C et al (2010) Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 35:83–93

    Article  PubMed  CAS  Google Scholar 

  • Dykas MJ, Cassidy J (2011) Attachment and the processing of social information across the life span: theory and evidence. Psychol Bull 137(1):19

    Article  PubMed  Google Scholar 

  • Elmadih A, Wan MW, Numan M et al (2014) Does oxytocin modulate variation in maternal caregiving in healthy new mothers? Brain Res 1580:143–150

    Article  PubMed  CAS  Google Scholar 

  • Elwood RW, Mason C (1994) The couvade and the onset of paternal care: a biological perspective. Ethol Sociobiol 15(3):145–156

    Article  Google Scholar 

  • Fahrbach SE, Morrell JI, Pfaff DW (1984) Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats. Horm Behav 18(3):267–286

    Article  PubMed  CAS  Google Scholar 

  • Fahrbach SE, Morrell JI, Pfaff DW (1985) Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 40(6):526–532

    Article  PubMed  CAS  Google Scholar 

  • Fearon RP, Bakermans-Kranenburg MJ, Van IJzendoorn MH et al (2010) The significance of insecure attachment and disorganization in the development of children’s externalizing behavior: a meta-analytic study. Child Dev 81(2):435–456

    Article  PubMed  Google Scholar 

  • Feinman S (1980) Infant response to race, size, proximity, and movement of strangers. Infant Behav Dev 3:187–204

    Article  Google Scholar 

  • Feldman R, Bakermans-Kranenburg MJ (2017) Oxytocin: a parenting hormone. Curr Opin Psychol 15:13–18

    Article  PubMed  Google Scholar 

  • Feldman R, Weller A, Zagoory-Sharon O et al (2007) Evidence for a neuroendocrinological foundation of human affiliation plasma oxytocin levels across pregnancy and the postpartum period predict mother-infant bonding. Psychol Sci 18:965–970

    Article  PubMed  Google Scholar 

  • Feldman R, Gordon I, Schneiderman I et al (2010) Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 35(8):1133–1141

    Article  PubMed  CAS  Google Scholar 

  • Fessler DMT (2002) Reproductive immunosuppression and diet: an evolutionary perspective on pregnancy sickness and meat consumption. Curr Anthropol 43:19–39

    Article  PubMed  Google Scholar 

  • Flaxman SM, Sherman PW (2000) Morning sickness: a mechanism for protecting mother and embryo. Q Rev Biol 75:113–148

    Article  PubMed  CAS  Google Scholar 

  • Fleming AS, Steiner M, Anderson V (1987) Hormonal and attitudinal correlates of maternal behavior during the early postpartum period. J Reprod Infant Psychol 5:193–205

    Article  Google Scholar 

  • Fleming AS, Steiner M, Corter C (1997) Cortisol, hedonics, and maternal responsiveness in human mothers. Horm Behav 32(2):85–98

    Article  PubMed  CAS  Google Scholar 

  • Fleming AS, Corter C, Stallings J et al (2002) Testosterone and prolactin are associated with emotional responses to infant cries in new fathers. Horm Behav 42:399–413

    Article  PubMed  CAS  Google Scholar 

  • Forbes S (2002) Pregnancy sickness and embryo quality. Trends Ecol Evol 7:115–120

    Article  Google Scholar 

  • Furneaux EC, Langley-Evans AJ, Langley-Evans SC (2001) Nausea and vomiting of pregnancy: endocrine basis and contribution to pregnancy outcome. Obstet Gynecol Surv 56:775–782

    Article  PubMed  CAS  Google Scholar 

  • Galbally M, Lewis AJ, Van IJzendoorn MH et al (2011) The role of oxytocin in mother-infant relations: a systematic review of human studies. Harv Rev Psychiatry 19(1):1–14

    Article  PubMed  Google Scholar 

  • Gettler LT, McDade TW, Feranil AB et al (2011) Longitudinal evidence that fatherhood decreases testosterone in human males. Proc Natl Acad Sci U S A 108:16194–16199

    Article  PubMed  PubMed Central  Google Scholar 

  • Gettler LT, McDade TW, Agustin S et al (2013) Progesterone and estrogen responsiveness to father-toddler interaction. Am J Hum Biol 25(4):491–498

    Article  PubMed  Google Scholar 

  • Gilbert R, Widom CS, Browne K et al (2009) Burden and consequences of child maltreatment in high-income countries. Lancet 373:68–81

    Article  PubMed  Google Scholar 

  • Gilead M, Liberman N (2014) We take care of our own, caregiving salience increases out-group bias in response to out-group threat. Psychol Sci 25:1380–1387

    Article  PubMed  Google Scholar 

  • Gimpl G, Fahrenholz F (2001) The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81:629–683

    Article  PubMed  CAS  Google Scholar 

  • Gordon I, Zagoory-Sharon O, Schneiderman I et al (2008) Oxytocin and cortisol in romantically unattached young adults: associations with bonding and psychological distress. Psychophysiology 45(3):349–352

    Article  PubMed  Google Scholar 

  • Gordon I, Zagoory-Sharon O, Leckman JF et al (2010) Prolactin, oxytocin, and the development of paternal behavior across the first six months of fatherhood. Horm Behav 58(3):513–518

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Groh AM, Roisman GI (2009) Adults’ autonomic and subjective emotional responses to infant vocalizations: the role of secure base script knowledge. Dev Psychol 45(3):889

    Article  PubMed  Google Scholar 

  • Groh AM, Roisman GI, Van IJzendoorn MH et al (2012) The significance of insecure and disorganized attachment for children’s internalizing symptoms: a meta-analytic study. Child Dev 83(2):591–610

    PubMed  Google Scholar 

  • Groh AM, Fearon RP, Bakermans-Kranenburg MJ et al (2014) The significance of attachment security for children’s social competence with peers: a meta-analytic study. Attach Hum Dev 16(2):103–136

    Article  PubMed  PubMed Central  Google Scholar 

  • Grossmann K, Grossmann KE, Kindler H et al (2008) A wider view of attachment and exploration: the influence of mothers and fathers on the development of psychological security from infancy to young adulthood. In: Cassidy J, Shaver PR (eds) Handbook of attachment: theory, research, and clinical applications. Guilford Press, New York, pp 857–879

    Google Scholar 

  • Guastella 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

    Article  PubMed  CAS  Google Scholar 

  • Hahn-Holbrook J, Holbrook C, Bering J (2010) Snakes, spiders, strangers: how the evolved fear of strangers may misdirect efforts to protect children from harm. In: Lampinen JM, Sexton-Radek K (eds) Protecting children from violence: evidence based interventions. Psychology Press, New York, pp 263–289

    Google Scholar 

  • Hahn-Holbrook J, Holbrook C, Hasselton MG (2011a) Parental precaution: neurobiological means and adaptive ends. Neurosci Biobehav Rev 35:1052–1066

    Article  PubMed  Google Scholar 

  • Hahn-Holbrook J, Holt-Lunstad J, Holbrook C et al (2011b) Maternal defense: breast feeding increases aggression by reducing stress. Psychol Sci 22:1288–1295

    Article  PubMed  Google Scholar 

  • Heinrichs M, Domes G (2008) Neuropeptides and social behavior: effects of oxytocin and vasopressin in humans. Prog Brain Res 170:337–350

    Article  PubMed  CAS  Google Scholar 

  • Heinrichs M, Meinlschmidt G, Neumann I et al (2001) Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women. J Clin Endocrinol Metab 86(10):4798–4804

    Article  PubMed  CAS  Google Scholar 

  • Hill K, Hurtado AM (1996) Ache life history: the ecology and demography of a foraging people. Aldine de Gruyter, New York

    Google Scholar 

  • Hrdy SB (1999) Mother nature: a history of mothers, infants and natural selection. Pantheon, New York

    Google Scholar 

  • Hrdy SB (2011) Mothers and others: the evolutionary origins of mutual understanding. Harvard University Press, Cambridge

    Google Scholar 

  • Hurtado AM, Hill K (1992) Parental effect on offspring survivorship among Ache and Hiwi hunter-gathers: implication for modeling pair-bonding stability. In: Hewlett B (ed) Father-child relations: cultural and biosocial contexts. Aldine de Gruyter, New York

    Google Scholar 

  • Insel TR (2010) The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65(6):768–779

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Insel TR, Young LJ (2001) The neurobiology of attachment. Nat Rev Neurosci 2:129–136

    Article  PubMed  CAS  Google Scholar 

  • Jones B, Perrett D, Little A et al (2005) Menstrual cycle, pregnancy and oral contraceptive use alter attraction to apparent health in faces. Proc R Soc Lond B Biol Sci 272:347–354

    Article  CAS  Google Scholar 

  • Kagerbauer SM, Martin J, Schuster T et al (2013) Plasma oxytocin and vasopressin do not predict neuropeptide concentrations in the human cerebrospinal fluid. J Neuroendocrinol 25:668–673

    Article  PubMed  CAS  Google Scholar 

  • Kantrowitz B (1997) Off to a good start. Newsweek 7(129):6–9

    Google Scholar 

  • Kavaliers M, Choleris E, Ågmo A et al (2004) Olfactory-mediated parasite recognition and avoidance: linking genes to behavior. Horm Behav 46:272–283

    Article  PubMed  Google Scholar 

  • Kendrick KM (2000) Oxytocin, motherhood and bonding. Exp Physiol 85:111s–124s

    Article  PubMed  CAS  Google Scholar 

  • Kendrick KM, Da Costa AP, Broad KD et al (1997) Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res Bull 44(4):383–395

    Article  PubMed  CAS  Google Scholar 

  • Keverne EB, Kendrick KM (1992) Oxytocin facilitation of maternal behavior in sheep. Ann N Y Acad Sci 652:83–101

    Article  PubMed  CAS  Google Scholar 

  • Kidscape (1993) How safe are our children? Kidscape, London

    Google Scholar 

  • Kim P, Feldman R, Mayes LC et al (2011) Breastfeeding, brain activation to own infant cry, and maternal sensitivity. J Child Psychol Psychiatry 52:907–915

    Article  PubMed  PubMed Central  Google Scholar 

  • Kringelbach ML (2005) The human orbitofrontal cortex: linking reward to hedonic experience. Nat Rev Neurosci 6(9):691–702

    Article  PubMed  CAS  Google Scholar 

  • Kringelbach ML, Lehtonen A, Squire S et al (2008) A specific and rapid neural signature for parental instinct. PLoS One 3(2):e1664

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumsta R, Hummel E, Chen FS et al (2013) Epigenetic regulation of the oxytocin receptor gene: implications for behavioral neuroscience. Front Neurosci 7(83):1–6

    Google Scholar 

  • Lamb ME, Hwang CP, Frodi AM et al (1982) Security of mother-and father-infant attachment and its relation to sociability with strangers in traditional and nontraditional Swedish families. Infant Behav Dev 5(2):355–367

    Article  Google Scholar 

  • Lane A, Luminet O, Nave G et al (2016) Is there a publication bias in behavioral intranasal oxytocin research on humans? Opening the file drawer of one lab. J Neuroendocrinol Mol Transl Neurobiol 28(4):2–15

    Google Scholar 

  • Leckman JF, Mayes LC, Feldman R et al (1999) Early parental preoccupations and behaviors and their possible relationship to the symptoms of obsessive-compulsive disorder. Acta Psychiatr Scand Suppl 396:1–26

    Article  PubMed  CAS  Google Scholar 

  • LeDoux JE (2000) Emotion circuits in the brain. Ann Rev Neurosci 23:155–184

    Article  PubMed  CAS  Google Scholar 

  • Leerkes EM, Siepak KJ (2006) Attachment linked predictors of women’s emotional and cognitive responses to infant distress. Attach Hum Dev 8(1):11–32

    Article  PubMed  Google Scholar 

  • Leerkes EM, Blankson AN, O’Brien M (2009) Differential effects of maternal sensitivity to infant distress and non-distress on social-emotional functioning. Child Dev 80(3):762–775

    Article  PubMed  PubMed Central  Google Scholar 

  • Leger DW, Thompson RA, Merritt JA et al (1996) Adult perception of emotion intensity in human infant cries: effects of infant age and cry acoustics. Child Dev 67(6):3238–3249

    PubMed  CAS  Google Scholar 

  • Leitman DI, Wolf DH, Ragland JD et al (2010) “It’s not what you say, but how you say it”: a reciprocal temporo-frontal network for affective prosody. Front Hum Neurosci 4:19

    PubMed  PubMed Central  Google Scholar 

  • Macgregor DM (2003) Accident and emergency attendances by children under the age of 1 year as a result of injury. Emerg Med J 20:21–24

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maclean PD (1990) The triune brain in evolution. Role of paleocerebral functions. Plenum Press, New York

    Google Scholar 

  • Mah BL (2016) Oxytocin, postnatal depression, and parenting: a systematic review. Harv Rev Psychiatry 24(1):1–13

    Article  PubMed  Google Scholar 

  • Mah BL, Bakermans-Kranenburg MJ, Van IJzendoorn MH et al (2014) Oxytocin promotes protective behavior in depressed mothers: a pilot study with the enthusiastic stranger paradigm. Depress Anxiety 32(2):76–91

    Article  PubMed  CAS  Google Scholar 

  • McElwain NL, Booth-LaForce C (2006) Maternal sensitivity to infant distress and non-distress as predictors of infant-mother attachment security. J Fam Psychol 20:247–255

    Article  PubMed  Google Scholar 

  • Mehta PH, Josephs RA (2010) Testosterone and cortisol jointly regulate dominance: evidence for a dual-hormone hypothesis. Horm Behav 58(5):898–906

    Article  PubMed  CAS  Google Scholar 

  • Mendes D, Seidl-de-Moura ML, Siqueira JD (2009) The ontogenesis of smiling and its association with mothers’ affective behaviors: a longitudinal study. Infant Behav Dev 32:445–453

    Article  PubMed  Google Scholar 

  • Mezzacappa ES (2004) Breastfeeding and maternal stress response and health. Nutr Rev 67:261–268

    Article  Google Scholar 

  • Mizugaki S, Maehara Y, Okanoya K et al (2015) The power of an infant’s smile: maternal physiological responses to infant emotional expressions. PLoS One 10(6):e0129672

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Naber FBA, Van IJzendoorn MH, Deschamps P et al (2010) Intranasal oxytocin increases fathers’ observed responsiveness during play with their children: a double-blind within-subject experiment. Psychoneuroendocrinology 35:1583–1586

    Article  PubMed  CAS  Google Scholar 

  • Naber FBA, Poslawsky IE, Van IJzendoorn MH et al (2012) Brief report: oxytocin enhances paternal sensitivity to a child with autism: a double-blind within-subject experiment with intranasally administered oxytocin. J Autism Dev Disord 43:224–229

    Article  PubMed Central  Google Scholar 

  • Navarrete CD, Olsson A, Ho AK et al (2009) Fear extinction to an out-group face the role of target gender. Psychol Sci 20(2):155–158

    Article  PubMed  Google Scholar 

  • Neumann ID, Slattery DA (2016) Oxytocin in general anxiety and social fear: a translational approach. Biol Psychiatry 79(3):213–221

    Article  CAS  PubMed  Google Scholar 

  • Nishimori K, Young LJ, Guo Q et al (1996) Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proc Natl Acad Sci U S A 93(21):11699–11704

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Olff M, Frijling JL, Kubzansky LD et al (2013) The role of oxytocin in social bonding, stress regulation and mental health: an update on the moderating effects of context and interindividual differences. Psychoneuroendocrinology 38(9):1883–1894

    Article  PubMed  CAS  Google Scholar 

  • Ostrowski NL (1998) Oxytocin receptor mRNA expression in rat brain: implications for behavioral integration and reproductive success. Psychoneuroendocrinology 23:989–1004

    Article  PubMed  CAS  Google Scholar 

  • Otali E, Gilchrist JS (2006) Why chimpanzee (Pan troglodytes schweinfurthii) mothers are less gregarious than nonmothers and males: the infant safety hypothesis. Behav Ecol Sociobiol 59:561–570

    Article  Google Scholar 

  • Paquette D (2004) Theorizing the father-child relationship: mechanisms and developmental outcomes. Hum Dev 47(4):193–219

    Article  Google Scholar 

  • Pedersen CA, Ascher JA, Monroe YL et al (1982) Oxytocin induces maternal behavior in virgin female rats. Science 216(4546):648–650

    Article  PubMed  CAS  Google Scholar 

  • Pedersen CA, Caldwell JD, Walker C et al (1994) Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 108(6):1163

    Article  PubMed  CAS  Google Scholar 

  • Pepper GV, Roberts SC (2006) Rates of nausea and vomiting in pregnancy and dietary characteristics across populations. Proc R Soc Lond B Biol Sci 273:2675–2679

    Article  Google Scholar 

  • Quintana DS, Guastella AJ, Westlye LT et al (2016) The promise and pitfalls of intranasally administering psychopharmacological agents for the treatment of psychiatric disorders. Mol Psychiatry 21(1):29–38

    Article  PubMed  CAS  Google Scholar 

  • Reijman S, Alink LRA, Compier-de Block LH et al (2014) Autonomic reactivity to infant crying in maltreating mothers. Child Maltreat 19:101–112

    Article  PubMed  Google Scholar 

  • Reijman S, Alink LRA, Compier-de Block LH et al (2015) Salivary α-amylase reactivity to infant crying in maltreating mothers. Child Psychiatry Hum Dev 46(4):589–599

    Article  PubMed  Google Scholar 

  • Reijneveld SA, Van der Wal MF, Brugman E et al (2004) Infant crying and child abuse. Lancet 364:1340–1342

    Article  PubMed  Google Scholar 

  • Riem MME, Bakermans-Kranenburg MJ, Pieper S et al (2011) Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial. Biol Psychiatry 70:291–297

    Article  PubMed  CAS  Google Scholar 

  • Riem MME, Bakermans-Kranenburg MJ, Van IJzendoorn MH et al (2012a) Attachment in the brain: adult attachment representations predict amygdala and behavioral responses to infant crying. Attach Hum Dev 14:533–551

    Article  PubMed  Google Scholar 

  • Riem MME, Van IJzendoorn MH, Tops M et al (2012b) No laughing matter: intranasal oxytocin administration changes functional brain connectivity during exposure to infant laughter. Neuropsychopharmacology 37:1257–1266

    Article  PubMed  CAS  Google Scholar 

  • Riem MME, Voorthuis A, Bakermans-Kranenburg MJ et al (2014) Pity or peanuts? Oxytocin induces different neural responses to the same infant crying labeled as sick or bored. Dev Sci 17:248–256

    Article  PubMed  Google Scholar 

  • Riem MME, Bakermans-Kranenburg MJ, Van IJzendoorn MH (2016) Intranasal administration of oxytocin modulates behavioral and amygdala responses to infant crying in females with insecure attachment representations. Attach Hum Dev 18(3):213–234

    Article  PubMed  Google Scholar 

  • Righetti-Veltema M, Conne-Perreard E, Bousquet A et al (2002) Postpartum depression and mother-infant relationship at 3 months old. J Affect Disord 70(3):291–306

    Article  PubMed  Google Scholar 

  • Rilling JK (2013) The neural and hormonal bases of human parental care. Neuropsychologia 51:731–747

    Article  PubMed  Google Scholar 

  • Rimmele U, Hediger K, Heinrichs M et al (2009) Oxytocin makes a face in memory familiar. J Neurosci 29(1):38–42

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rocchetti M, Radua J, Paloyelis Y et al (2014) Neurofunctional maps of the ‘maternal brain’ and the effects of oxytocin: a multimodal voxel-based meta-analysis. Psychiatry Clin Neurosci 68(10):733–751

    Article  PubMed  CAS  Google Scholar 

  • Sadedin S (2014) War in the womb. Aeon. https://aeon.co/essays/why-pregnancy-is-a-biological-war-between-mother-and-baby. Accessed 5 May 2016

  • Simpson JA, Belsky J (2008) Attachment theory within a modern evolutionary framework: theory, research, and clinical applications. In: Cassidy J, Shaver PR (eds) Handbook of attachment: theory, research, and clinical applications, 2nd edn. Guilford Press, New York, pp 131–157

    Google Scholar 

  • Skarin K (1977) Cognitive and contextual determinants of stranger fear in six-and eleven-month-old infants. Child Dev 48:537–544

    Article  PubMed  CAS  Google Scholar 

  • Sroufe LA, Waters E (1976) The ontogenesis of smiling and laughter: a perspective on the organization of development in infancy. Psychol Rev 83(3):173

    Article  PubMed  CAS  Google Scholar 

  • Stallings J, Fleming AS, Corter C et al (2001) The effects of infant cries and odors on sympathy, cortisol, and autonomic responses in new mothers and nonpostpartum women. Parenting 1(1–2):71–100

    Article  Google Scholar 

  • Storey AE, Walsh CJ, Quinton RL et al (2000) Hormonal correlates of paternal responsiveness in new and expectant fathers. Evol Hum Behav 21:79–95

    Article  PubMed  CAS  Google Scholar 

  • Strathearn L, Fonagy P, Amico J et al (2009) Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology 34:2655–2666

    Article  PubMed  CAS  Google Scholar 

  • Stribley JM, Carter CS (1999) Developmental exposure to vasopressin increases aggression in adult prairie voles. Proc Natl Acad Sci U S A 96:12601–12604

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Striepens N, Scheele D, Kendrick KM et al (2012) Oxytocin facilitates protective responses to aversive social stimuli in males. Proc Natl Acad Sci U S A 109(44):18144–18149

    Article  PubMed  PubMed Central  Google Scholar 

  • Swain JE (2008) Baby stimuli and the parent brain: functional neuroimaging of the neural substrates of parent-infant attachment. Psychiatry 5:28–36

    PubMed  PubMed Central  Google Scholar 

  • Swain JE, Kim P, Spicer J et al (2014) Approaching the biology of human parental attachment: brain imaging, oxytocin and coordinated assessments of mothers and fathers. Brain Res 1580:78–101

    Article  PubMed  CAS  Google Scholar 

  • Takayanagi Y, Yoshida M, Bielsky IF et al (2005) Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc Natl Acad Sci U S A 102(44):16096–16101

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Taylor SE (2002) The tending instinct: how nurturing is essential to who we are and how we live. Holt, New York

    Google Scholar 

  • Taylor SE, Klein LC, Lewis BP (2000) Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol Rev 107:411–429

    Article  PubMed  CAS  Google Scholar 

  • Theodoridou A, Penton-Voak IS, Rowe AC (2013) A direct examination of the effect of intranasal administration of oxytocin on approach-avoidance motor responses to emotional stimuli. PLoS One 8(2):e58113

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thompson RR, George K, Walton JC et al (2006) Sex-specific influences of vasopressin on human social communication. Proc Natl Acad Sci U S A 103(20):7889–7894

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • UNICEF (2013) Levels and trends in child mortality. IGME report 2013

    Google Scholar 

  • Van Anders SM, Tolman RM, Volling BL (2012) Baby cries and nurturance affect testosterone in men. Horm Behav 61(1):31–36

    Article  PubMed  CAS  Google Scholar 

  • Van Hooff JA (1972) A comparative approach to the phylogeny of laughter and smiling. In: Hinde RA (ed) Non-verbal communication. Cambridge University Press, Cambridge, pp 209–241

    Google Scholar 

  • 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 37:438–443

    Article  PubMed  CAS  Google Scholar 

  • Van IJzendoorn MH, Bakermans-Kranenburg MJ (2016) The role of oxytocin in parenting and as augmentative pharmacotherapy; critical issues and bold conjectures. J Neuroendocrinol 28. doi:10.1111/jne.12355

  • Viau V (2002) Functional cross-talk between the hypothalamic-pituitary-gonadal and-adrenal axes. J Neuroendocrinol 14(6):506–513

    Article  PubMed  CAS  Google Scholar 

  • Voorthuis A, Riem MME, Van IJzendoorn MH et al (2014) Reading the mind in the infant eyes: paradoxical effects of oxytocin on neural activity and emotion recognition in watching pictures of infant faces. Brain Res 1580:151–159

    Article  PubMed  CAS  Google Scholar 

  • Weissman O, Zagoory-Sharon O, Feldman R (2014) Oxytocin administration, salivary testosterone, and father-infant social behavior. Prog Neuropsychopharmacol Biol Psychiatry 49:47–52

    Article  CAS  Google Scholar 

  • Williams LM, Kemp AH, Felmingham K et al (2006) Trauma modulates amygdala and medial prefrontal responses to consciously attended fear. NeuroImage 29:347–357

    Article  PubMed  Google Scholar 

  • Wood RM, Gustafson GE (2001) Infant crying and adults’ anticipated caregiving responses: acoustic and contextual influences. Child Dev 72(5):1287–1300

    Article  PubMed  CAS  Google Scholar 

  • Woody EZ, Szechtman H (2011) Adaptation to potential threat: the evolution, neurobiology, and psychopathology of the security motivation system. Neurosci Biobehav Rev 35:1019–1033

    Article  PubMed  Google Scholar 

  • Wright ND, Bahrami B, Johnson E et al (2012) Testosterone disrupts human collaboration by increasing egocentric choices. Proc Biol Sci 279:2275–2280

    Article  PubMed  PubMed Central  Google Scholar 

  • Wynne-Edwards KE, Reburn CJ (2000) Behavioral endocrinology of mammalian fatherhood. Trends Ecol Evol 15:464–468

    Article  PubMed  CAS  Google Scholar 

  • Young LJ, Winslow JT, Wang Z et al (1997) Gene targeting approaches to neuroendocrinology: oxytocin, maternal behavior, and affiliation. Horm Behav 31(3):221–231

    Article  PubMed  CAS  Google Scholar 

  • Zilioli S, Ponzi D, Henry A et al (2014) Testosterone, cortisol and empathy: evidence for the dual-hormone hypothesis. Adapt Hum Behav Physiol 1(4):421–433

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marian J. Bakermans-Kranenburg .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Bakermans-Kranenburg, M.J., van IJzendoorn, M.H. (2017). Oxytocin and Human Sensitive and Protective Parenting. In: Hurlemann, R., Grinevich, V. (eds) Behavioral Pharmacology of Neuropeptides: Oxytocin. Current Topics in Behavioral Neurosciences, vol 35. Springer, Cham. https://doi.org/10.1007/7854_2017_23

Download citation

Publish with us

Policies and ethics