Psychoneuroendocrinology
Volume 35, Issue 8 , Pages 1133-1141 , September 2010

Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent–infant contact

Received 10 December 2009 ,Revised 19 January 2010 ,Accepted 20 January 2010.

References 

  1. Ahern TH, Young LJ. 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). Front. Behav. Neurosci. 2009;3:17
  2. Amico JA, Levin SC, Cameron JL. 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. 1989;50:624–632
  3. Bales KL, Kim AJ, Lewis-Reese AD, Sue Carter C. Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles. Horm. Behav. 2004;45:354–361
  4. Beck AT. Beck Depression Inventory. Brace Jovanovich, San Antonio: The Psychological Corporation; 1978;
  5. Bello D, White-Traut R, Schwertz D, Pournajafi-Nazarloo H, Carter CS. An exploratory study of neurohormonal responses of healthy men to massage. J. Altern. Complement. Med. 2008;14:387–394
  6. Bredy TW, Lee AW, Meaney MJ, Brown RE. Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse (Peromyscus californicus). Horm. Behav. 2004;46:30–38
  7. Burri A, Heinrichs M, Schedlowski M, Kruger TH. The acute effects of intranasal oxytocin administration on endocrine and sexual function in males. Psychoneuroendocrinology. 2008;33:591–600
  8. Carter CS. Sex differences in oxytocin and vasopress implications for autism spectrum disorders?. Behav. Brain Res. 2007;176:170–186
  9. In:  Carter CS,  Grossmann KELA,  Hrdy SB,  Lamb ME,  Porges SW,  Sachser N editor. Attachment and Bonding: A New Synthesis. Cambridge, MA; London: MIT Press in cooperation with Dahlem University Press; 2005;
  10. Carter CS, Pournajafi-Nazarloo H, Kramer KM, Ziegler TE, White-Traut R, Bello D, et al. Oxytocin: behavioral associations and potential as a salivary biomarker. Ann. N. Y. Acad. Sci. 2007;1098:312–322
  11. Champagne FA. Epigenetic mechanisms and the transgenerational effects of maternal care. Front. Neuroendocrinol. 2008;29:386–397
  12. Champagne FA, Diorio J, Sharma S, Meaney MJ. Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc. Natl. Acad. Sci. U.S.A. 2001;98:12736–12741
  13. Champagne FA, Francis DD, Mar A, Meaney MJ. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol. Behav. 2003;79:359–371
  14. Champagne DL, Bagot RC, van Hasselt F, Ramakers G, Meaney MJ, de Kloet ER, et al. Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J. Neurosci. 2008;28:6037–6045
  15. Cho MM, DeVries AC, Williams JR, Carter CS. The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav. Neurosci. 1999;113:1071–1079
  16. de Jong TR, Chauke M, Harris BN, Saltzman W. From here to paternity: neural correlates of the onset of paternal behavior in California mice (Peromyscus californicus). Horm. Behav. 2009;56:220–231
  17. Ditzen B, Neumann ID, Bodenmann G, von Dawans B, Turner RA, Ehlert U, et al. Effects of different kinds of couple interaction on cortisol and heart rate responses to stress in women. Psychoneuroendocrinology. 2007;32:565–574
  18. Feldman R. Infant–mother and infant–father synchrony: the coregulation of positive arousal. Infant Ment. Health J. 2003;24:1–23
  19. Feldman R. Parent–infant synchrony and the construction of shared timing: physiological precursors, developmental outcomes, and risk conditions. J. Child Psychol. Psychiatry. 2007;48:329–354
  20. Feldman R, Eidelman AI. Direct and indirect effects of breast milk on the neurobehavioral and cognitive development of premature infants. Dev. Psychobiol. 2003;43:109–119
  21. Feldman R, Eidelman AI. Parent–infant synchrony and the social–emotional development of triplets. Dev. Psychol. 2004;40:1133–1147
  22. Feldman R, Eidelman AI. Maternal postpartum behavior and the emergence of infant–mother and infant–father synchrony in preterm and full-term infants: the role of neonatal vagal tone. Dev. Psychobiol. 2007;49:290–302
  23. Feldman R, Eidelman AI, Sirota L, Weller A. Comparison of skin-to-skin (kangaroo) and traditional care: parenting outcomes and preterm infant development. Pediatrics. 2002;110:16–26
  24. Feldman R, Keren M, Gross-Rozval O, Tyano S. Mother–child touch patterns in infant feeding disorders: relation to maternal, child, and environmental factors. J. Am. Acad. Child Adolesc. Psychiatry. 2004;43:1089–1097
  25. Feldman R, Weller A, Zagoory-Sharon O, Levine A. Evidence for a neuroendocrinological foundation of human affiliation: plasma oxytocin levels across pregnancy and the postpartum period predict mother–infant bonding. Psychol. Sci. 2007;18:965–970
  26. Feldman R, Granat A, Pariente C, Kaneti H, Kuint J, Gilboa-Schechtman E. Maternal affective disorder across the postpartum year and infant social engagement, fear regulation, and stress reactivity. J. Am. Acad. Child Adolesc. Psychiatry. 2009;48:919–927
  27. Feldman R, Singer M, Zagoory O. Touch attenuates infants physiological reactivity to stress. Dev. Sci. 2010;
  28. Francis DD, Champagne FC, Meaney MJ. Variations in maternal behavior are associated with differences in oxytocin receptor levels in the rat. J. Neuroendocrinol. 2000;12:1145–1148
  29. Francis DD, Young LJ, Meaney MJ, Insel TR. Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J. Neuroendocrinol. 2002;14:349–353
  30. Frazier CR, Trainor BC, Cravens CJ, Whitney TK, Marler CA. Paternal behavior influences development of aggression and vasopressin expression in male California mouse offspring. Horm. Behav. 2006;50:699–707
  31. Gordon I, Zagoory-Sharon O, Schneiderman I, Leckman JF, Weller A, Feldman R. Oxytocin and cortisol in romantically unattached young adults: associations with bonding and psychological distress. Psychophysiology. 2008;45:349–352
  32. Gubernick DJ, Winslow JT, Jensen P, Jeanotte L, Bowen J. Oxytocin changes in males over the reproductive cycle in the monogamous, biparental California mouse, Peromyscus californicus. Horm. Behav. 1995;29:59–73
  33. Hake-Brooks SJ, Anderson GC. Kangaroo care and breastfeeding of mother–preterm infant dyads 0–18 months: a randomized, controlled trial. Neonatal Netw. 2008;27:151–159
  34. Holman SD, Goy RW. Experiential and hormonal correlates of care-giving in rhesus macaques. In:  Pryce CR,  Skuse RDMD editor. Motherhood in Human and Nonhuman Primates: Biosocial Determinants. Basel: Karger; 1995;p. 87–93
  35. Holt-Lunstad J, Birmingham WA, Light KC. Influence of a “warm touch” support enhancement intervention among married couples on ambulatory blood pressure, oxytocin, alpha amylase, and cortisol. Psychosom. Med. 2008;70:976–985
  36. Kendrick KM, Keverne EB, Baldwin BA. Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology. 1987;46:56–61
  37. Kotelchuck M. The infant's relationship to the father: experimental evidence. In:  Lamb ME editors. The Role of the Father in Child Development. New York: Wiley & Sons; 1976;
  38. Lamb ME. The role of the father: interactions between 8 month old children and their fathers and mothers. In:  Lamb ME editors. The Role of the Father in Child Development. New York: Wiley & Sons; 1976;
  39. Leckman JF, Feldman R, Swain JE, Eicher V, Thompson N, Mayes LC. Primary parental preoccupation: circuits, genes, and the crucial role of the environment. J. Neural Transm. 2004;111:753–771
  40. Levine A, Zagoory-Sharon O, Feldman R, Weller A. Oxytocin during pregnancy and early postpartum: individual patterns and maternal–fetal attachment. Peptides. 2007;28:1162–1169
  41. Lonstein JS, De Vries GJ. Comparison of the parental behavior of pair-bonded female and male prairie voles (Microtus ochrogaster). Physiol. Behav. 1999;66:33–40
  42. Maestripieri D, Hoffman CL, Anderson GM, Carter CS, Higley JD. Mother–infant interactions in free-ranging rhesus macaques: relationships between physiological and behavioral variables. Physiol. Behav. 2009;96:613–619
  43. March of Dimes . National Center for Health Statistics, Final Natality Data. 2006;http://www.marchofdimes.com/peristats/
  44. Meaney MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 2001;24:1161–1192
  45. Murray L, Halligan SL, Goodyer I, Herbert J. Disturbances in early parenting of depressed mothers and cortisol secretion in offspring: a preliminary study. J. Affect. Disord. 2009;
  46. Neumann ID. Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J. Neuroendocrinol. 2008;20:858–865
  47. Neumann ID. The advantage of social living: brain neuropeptides mediate the beneficial consequences of sex and motherhood. Front. Neuroendocrinol. 2009;30:483–496
  48. Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics. 2008;3:97–106
  49. Parent CI, Meaney MJ. The influence of natural variations in maternal care on play fighting in the rat. Dev. Psychobiol. 2008;50:767–776
  50. Parke RD, Sawin DB. The father's role in infancy: a re-evaluation. Fam. Coord. 1976;25:365–371
  51. Pedersen CA, Boccia ML. Oxytocin antagonism alters rat dams oral grooming and upright posturing over pups. Physiol. Behav. 2003;80:233–241
  52. Pedersen CA, Prange AJ. Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc. Natl. Acad. Sci. U.S.A. 1979;76:6661–6665
  53. Pedersen CA, Caldwell JD, Johnson MF, Fort SA, Prange AJ. Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior. Neuropeptides. 1985;6:175–182
  54. Ross HE, Young LJ. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front. Neuroendocrinol. 2009;30:534–547
  55. Scott SM, Watterberg KL. Effect of gestational age, postnatal age, and illness on plasma cortisol concentrations in premature infants. Pediatr. Res. 1995;37:112–116
  56. Serretti A, Olgiati P, Colombo C. Influence of postpartum onset on the course of mood disorders. BMC Psychiatry. 2006;6:4
  57. Spielberger CD. State-trait Anxiety Inventory: A Comprehensive Bibliography. Palo Alto, CA: Consulting Psychologists Press; 1984;
  58. Strathearn L, Fonagy P, Amico J, Montague PR. Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology. 2009;34:2655–2666
  59. Turner RA, Altemus M, Enos T, Cooper B, McGuinness T. Preliminary research on plasma oxytocin in normal cycling women: investigating emotion and interpersonal distress. Psychiatry. 1999;62:97–113
  60. van der Post JA, van Buul BJ, Hart AA, van Heerikhuize JJ, Pesman G, Legros JJ, et al. Vasopressin and oxytocin levels during normal pregnancy: effects of chronic dietary sodium restriction. J. Endocrinol. 1997;152:345–354
  61. White-Traut R, Watanabe K, Pournajafi-Nazarloo H, Schwertz D, Bell A, Carter CS. Detection of salivary oxytocin levels in lactating women. Dev. Psychobiol. 2009;51:367–373
  62. Wotjak CT, Ganster J, Kohl G, Holsboer F, Landgraf R, Engelmann M. Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: new insights into the secretory capacities of peptidergic neurons. Neuroscience. 1998;85:1209–1222
  63. Wynne-Edwards KE. Hormonal changes in mammalian fathers. Horm. Behav. 2001;40:139–145
  64. Wynne-Edwards KE, Timonin ME. Paternal care in rodents: weakening support for hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care. Horm. Behav. 2007;52:114–121
  65. Young LJ, Lim MM, Gingrich B, Insel TR. Cellular mechanisms of social attachment. Horm. Behav. 2001;40:133–138
  66. Ziegler TE. Hormones associated with non-maternal infant care: a review of mammalian and avian studies. Folia Primatol. (Basel). 2000;71:6–21

PII: S0306-4530(10)00029-6

doi: 10.1016/j.psyneuen.2010.01.013

Psychoneuroendocrinology
Volume 35, Issue 8 , Pages 1133-1141 , September 2010