Elsevier

Psychoneuroendocrinology

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

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

https://doi.org/10.1016/j.psyneuen.2010.01.013Get rights and content

Summary

Animal studies have demonstrated that the neuropeptide oxytocin (OT) plays a critical role in processes of parent–infant bonding through mechanisms of early parental care, particularly maternal grooming and contact. Yet, the involvement of OT in human parenting remains poorly understood, no data are available on the role of OT in the development of human fathering, and the links between patterns of parental care and the OT response have not been explored in humans. One hundred and twelve mothers and fathers engaged in a 15-min play-and-contact interaction with their 4–6-month-old infants and interactions were micro-coded for patterns of parental touch. Results showed that baseline levels of plasma and salivary OT in mothers and fathers were similar, OT levels in plasma and saliva were inter-related, and OT was associated with the parent-specific mode of tactile contact. Human mothers who provided high levels of affectionate contact showed an OT increase following mother–infant interaction but such increase was not observed among mothers displaying low levels of affectionate contact. Among fathers, only those exhibiting high levels of stimulatory contact showed an OT increase. These results demonstrate consistency in the neuroendocrine basis of human parental interactions with those seen in other mammals. The findings underscore the need to provide opportunities for paternal care to trigger the biological basis of fatherhood and suggest that interventions that permit social engagement may be recommended in conditions of diminished maternal–infant contact, such as prematurity or postpartum depression.

Introduction

The expression of parenting behavior in mammals is critical for the growth, survival, and adaptation of the young and for the formation of affiliative bonds (Leckman et al., 2004, Carter et al., 2005). The neuropeptide oxytocin (OT) has been shown to play a key role in processes of parent–infant bonding across a range of mammalian species, including rats, prairie voles, sheep, and primates (Kendrick et al., 1987, Holman et al., 1995, Neumann, 2008, Maestripieri et al., 2009). The administration of OT antagonists disrupts the development of maternal behavior (Pedersen et al., 1985, Pedersen and Boccia, 2003), and pregnancy, lactation, and maternal behavior increase OT receptor binding in brain areas central for parenting and the reward parents derive from their infants (Ross and Young, 2009). The oxytocinergic system that supports bond formation in mammals functions as a bio-behavioral feedback loop; maternal–infant touch and contact increase the expression of OT (Francis et al., 2002), while the administration of OT, in turn, leads to the induction of maternal behavior (Pedersen and Prange, 1979). In monogamous species that exhibit biparental care, OT is also associated with fathering and paternal behavior (Gubernick et al., 1995, Cho et al., 1999, Wynne-Edwards, 2001, Bales et al., 2004). Yet, while understanding the neuroendocrine basis of parenting is central for the study of human development, much less is known about the involvement of OT in human parenting, and the mechanisms linking the OT response with the species-typical maternal and paternal behavior or the provision of parent–infant contact have not been explored in human parents.

An important feature of the oxytocinergic system that underlies the formation of affiliative bonds is its modification by early social experience (Meaney, 2001, Champagne et al., 2008). Drawing on natural within-species variations in maternal care, particularly the licking-and-grooming and arched back nursing (LG-ABN) behaviors typical of parturient rat mothers, researchers found that maternal female rats exhibiting high levels of LG-ABN showed greater OT receptor densities in brain areas central for parenting, including the medial preoptic area, the lateral septum, and the paraventricular nucleus of the hypothalamus, as compared to mothers exhibiting low LG-ABN (Francis et al., 2000, Champagne et al., 2001). In rats, the mother's high or low LG style was stable over time and was transmitted from mother to daughter through mechanisms of early experience (Champagne et al., 2001, Champagne et al., 2003). Females bred to a strain of low LG-ABN mothers and reared by high LG-ABN dams showed the high licking-and-grooming parenting pattern toward their own infants and exhibited the brain OT profile typical of the high LG-ABN strain (Francis et al., 2000, Champagne, 2008). Studies in nonhuman primates have similarly demonstrated correlations between plasma OT and the degree of maternal–infant grooming and contact (Maestripieri et al., 2009). Taken together, these findings suggest that both central and peripheral OT is related to individual variations in affectionate contact between mother and young.

Human mothers, like other mammalian mothers, engage in the species-typical forms of affectionate contact. In humans, maternal affectionate contact is expressed in holding the infant in a cradling position and providing affectionate touch, including caresses, soft kisses, light pokes, hugs, and gentle touches that do not serve a specific instrumental purpose. The mother's high or low affectionate contact style is similarly stable over time and contributes to the infant's neurobehavioral, cognitive, and social–emotional growth (Feldman and Eidelman, 2003, Feldman, 2007). Similarly, plasma OT levels in human mothers were found to be individually stable from early pregnancy to the postpartum and to predict the expression of maternal behavior in the postpartum, suggesting a priming effect of OT on the initiation of parenting behaviors (Feldman et al., 2007, Levine et al., 2007). However, it is not known whether the provision of affectionate contact is related to systematic changes in OT. Revealing similar mechanisms in humans may have important implications for the study of human bond formation and for the care of pathological conditions associated with diminished maternal–infant affectionate contact and disrupted bonding, such as premature birth or postpartum depression, each of which impacts approximately 10–15% of current births in industrial societies (March of Dimes, 2006, Serretti et al., 2006).

Research on the neuroendocrine basis of fathering in humans is especially scarce and the mechanisms linking paternal behavior and the oxytocinergic system remain poorly understood. Research in biparental fathers have pointed to the involvement of OT in the development of fathering (Young et al., 2001). Biparental fathers showed an increase in plasma OT during pregnancy (Gubernick et al., 1995), and the degree of paternal exposure to pup stimuli and the amount of paternal care is associated with OT (Ziegler, 2000). Thus, although fathers do not experience pregnancy, birth, or lactation, similar neuroendocrine pathways are thought to mediate the initiation of fathering and mothering in mammals (Wynne-Edwards and Timonin, 2007). The links between OT and the mesolimbic dopaminergic pathways in monogamous fathers suggest that OT modulates paternal reward pathways through attachment-related stimuli from partner and child (Young et al., 2001). In several biparental species fathers exhibit parenting behavior similar to mothers (Bredy et al., 2004, Frazier et al., 2006, Ahern and Young, 2009), yet fathers tend to engage in a specific mode of parental contact. Following separation, monogamous mothers and fathers increased their parenting behavior; however, mothers engaged in licking and contact while fathers provided tactile stimulation, carried the infants in space, and encouraged exploratory behavior (Lonstein and De Vries, 1999). Thus, it is possible that whereas hormones associated with birth, lactation, and affectionate contact may induce hormonal changes in mothers, tactile stimulation and active forms of behavior such as exploration may shape the neuroendocrine basis of fathering.

Like mammals, human fathers engage in interactions that involve proprioceptive and stimulatory contact and their play is often directed toward active exploration of the environment (Lamb, 1976, Parke and Sawin, 1976). Father–child interactions typically take the form of “rough-and-tumble” stimulatory play and have shown to be highly rewarding and to increase the father and child's positive arousal (Feldman, 2003). Consistent with the findings that early experience activates the neuroendocrine basis of parenting, it is thus possible that the species-typical stimulatory play of human fathers induces OT release and natural variations in paternal stimulatory contact would be expressed in systematic changes in paternal OT.

In light of the above, the overall goal of the present study was to assess the involvement of the oxytocinergic system in human mothering and fathering and to address its consistency with parenting in other mammals. First, we sought to examine whether baseline levels of plasma and salivary OT in mothers and fathers are similar during the first months of parenting. Based on studies pointing to similar expressions in males and females of central OT in biparental mammals, no differences in OT levels were expected between mothers and fathers. Second, we examined whether the mechanisms that link the expression of OT with maternal and paternal care in nonhuman mammals are also observed in human parents. Specifically, we tested whether mothers who provide high levels of affectionate contact, but not those showing low affectionate contact, would show an increase in OT levels following mother–infant interaction. Among fathers, we examined whether fathers who display high levels of stimulatory contact, but not those demonstrating low stimulatory contact, would show an increase in OT following an episode of parent–infant interaction. Such findings will demonstrate similar mechanisms in human parents and biparental mammals, pointing to cross-species consistency in the neuroendocrine basis of bonding and its relation to patterns of parental care.

Section snippets

Participants

Participants were 112 parents, including 71 mothers and 41 fathers (not couples) and their 4–6-month-old infants (M = 166.3 days, SD = 12.6). All parents were healthy with at least 12 years of education and were of middle-class SES. Mothers were on average 28.7 years (SD = 5.29), completed on average 15.17 (SD = 2.47) years of education, and 81.3% of the mothers were breastfeeding. Fathers’ age averaged 29.1 years (SD = 4.28) with an average education of 15.50 (SD = 2.73) years. Infants were born at term

Results

Results are organized in six mini-sections according to the study's goals and hypotheses. In the first three sections, we demonstrate similarities and differences between mothers and fathers, inter-relatedness between plasma and salivary OT, and individual stability in OT. The next three sections address the links between OT and the parent-specific mode of tactile contact. Prior to data analysis, we examined correlations between OT and background variables. No correlations were found between OT

Discussion

The present findings point to consistency in the neuroendocrine basis of mammalian and human parenting as well as to similarities and differences between human mothers and fathers during the first postpartum months. Oxytocin – a neuropeptide involved in the formation of parent–infant bonding and in processes of social affiliations throughout life – was first tested here in human fathers in relation to father–infant interactions and paternal contact. The results indicating no differences in

Role of funding source

The NARSAD, ISD, and BSF foundations had no further role in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.

Conflict of interest

None declare.

Acknowledgements

Research is supported by the NARSAD Foundation (independent investigator award), the Israel Science Foundation, and the US–Israel Bi-National Science Foundation.

References (66)

  • C.R. Frazier et al.

    Paternal behavior influences development of aggression and vasopressin expression in male California mouse offspring

    Horm. Behav.

    (2006)
  • D.J. Gubernick et al.

    Oxytocin changes in males over the reproductive cycle in the monogamous, biparental California mouse, Peromyscus californicus

    Horm. Behav.

    (1995)
  • A. Levine et al.

    Oxytocin during pregnancy and early postpartum: individual patterns and maternal–fetal attachment

    Peptides

    (2007)
  • J.S. Lonstein et al.

    Comparison of the parental behavior of pair-bonded female and male prairie voles (Microtus ochrogaster)

    Physiol. Behav.

    (1999)
  • D. Maestripieri et al.

    Mother–infant interactions in free-ranging rhesus macaques: relationships between physiological and behavioral variables

    Physiol. Behav.

    (2009)
  • I.D. Neumann

    The advantage of social living: brain neuropeptides mediate the beneficial consequences of sex and motherhood

    Front. Neuroendocrinol.

    (2009)
  • C.A. Pedersen et al.

    Oxytocin antagonism alters rat dams oral grooming and upright posturing over pups

    Physiol. Behav.

    (2003)
  • C.A. Pedersen et al.

    Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior

    Neuropeptides

    (1985)
  • H.E. Ross et al.

    Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior

    Front. Neuroendocrinol.

    (2009)
  • C.T. Wotjak et al.

    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)
  • K.E. Wynne-Edwards

    Hormonal changes in mammalian fathers

    Horm. Behav.

    (2001)
  • K.E. Wynne-Edwards et al.

    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)
  • L.J. Young et al.

    Cellular mechanisms of social attachment

    Horm. Behav.

    (2001)
  • T.H. Ahern et al.

    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)
  • J.A. Amico et al.

    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)
  • A.T. Beck

    Beck Depression Inventory

    (1978)
  • D. Bello et al.

    An exploratory study of neurohormonal responses of healthy men to massage

    J. Altern. Complement. Med.

    (2008)
  • C.S. Carter et al.

    Oxytocin: behavioral associations and potential as a salivary biomarker

    Ann. N. Y. Acad. Sci.

    (2007)
  • F.A. Champagne et al.

    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)
  • D.L. Champagne 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)
  • M.M. Cho et al.

    The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster)

    Behav. Neurosci.

    (1999)
  • R. Feldman

    Infant–mother and infant–father synchrony: the coregulation of positive arousal

    Infant Ment. Health J.

    (2003)
  • Cited by (473)

    View all citing articles on Scopus
    View full text