Psychoneuroendocrinology (2010) 35, 1133—1141 available at www.sciencedirect.com journal homepage: www.elsevier.com/locate/psyneuen Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent—infant contact Ruth Feldman *, Ilanit Gordon, Inna Schneiderman, Omri Weisman, Orna Zagoory-Sharon Bar-Ilan University, Israel Received 10 December 2009; received in revised form 19 January 2010; accepted 20 January 2010 KEYWORDS Summary Animal studies have demonstrated that the neuropeptide oxytocin (OT) plays a Oxytocin; critical role in processes of parent—infant bonding through mechanisms of early parental care, Parent—infant bonding; particularly maternal grooming and contact. Yet, the involvement of OT in human parenting Mothering; remains poorly understood, no data are available on the role of OT in the development of human Fathering; fathering, and the links between patterns of parental care and the OT response have not been Touch; explored in humans. One hundred and twelve mothers and fathers engaged in a 15-min play-and- Attachment 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 interac- tions with those seen in other mammals. The findings underscore the need to provide oppor- tunities 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. # 2010 Elsevier Ltd. All rights reserved. 1. Introduction the formation of affiliative bonds (Leckman et al., 2004; Carter et al., 2005). The neuropeptide oxytocin (OT) has The expression of parenting behavior in mammals is critical been shown to play a key role in processes of parent—infant for the growth, survival, and adaptation of the young and for bonding across a range of mammalian species, including rats, prairie voles, sheep, and primates (Kendrick et al., 1987; * Corresponding author at: Department of Psychology and The Holman et al., 1995; Neumann, 2008; Maestripieri et al., Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan 2009). The administration of OT antagonists disrupts the 52900, Israel. Tel.: +972 3 531 7943; fax: +972 3 535 0267. development of maternal behavior (Pedersen et al., 1985; E-mail address: [email protected] (R. Feldman). Pedersen and Boccia, 2003), and pregnancy, lactation, and 0306-4530/$ — see front matter # 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.psyneuen.2010.01.013 1134 R. Feldman et al. maternal behavior increase OT receptor binding in brain implications for the study of human bond formation and for areas central for parenting and the reward parents derive the care of pathological conditions associated with dimin- from their infants (Ross and Young, 2009). The oxytocinergic ished maternal—infant affectionate contact and disrupted system that supports bond formation in mammals functions bonding, such as premature birth or postpartum depression, as a bio-behavioral feedback loop; maternal—infant touch each of which impacts approximately 10—15% of current and contact increase the expression of OT (Francis et al., births in industrial societies (March of Dimes, 2006; Serretti 2002), while the administration of OT, in turn, leads to the et al., 2006). induction of maternal behavior (Pedersen and Prange, 1979). Research on the neuroendocrine basis of fathering in In monogamous species that exhibit biparental care, OT is humans is especially scarce and the mechanisms linking also associated with fathering and paternal behavior (Guber- paternal behavior and the oxytocinergic system remain nick et al., 1995; Cho et al., 1999; Wynne-Edwards, 2001; poorly understood. Research in biparental fathers have Bales et al., 2004). Yet, while understanding the neuroendo- pointed to the involvement of OT in the development of crine basis of parenting is central for the study of human fathering (Young et al., 2001). Biparental fathers showed an development, much less is known about the involvement of increase in plasma OT during pregnancy (Gubernick et al., OT in human parenting, and the mechanisms linking the OT 1995), and the degree of paternal exposure to pup stimuli and response with the species-typical maternal and paternal the amount of paternal care is associated with OT (Ziegler, behavior or the provision of parent—infant contact have 2000). Thus, although fathers do not experience pregnancy, not been explored in human parents. birth, or lactation, similar neuroendocrine pathways are An important feature of the oxytocinergic system that thought to mediate the initiation of fathering and mothering underlies the formation of affiliative bonds is its modification in mammals (Wynne-Edwards and Timonin, 2007). The links by early social experience (Meaney, 2001; Champagne et al., between OT and the mesolimbic dopaminergic pathways in 2008). Drawing on natural within-species variations in mater- monogamous fathers suggest that OT modulates paternal nal care, particularly the licking-and-grooming and arched reward pathways through attachment-related stimuli from back nursing (LG-ABN) behaviors typical of parturient rat partner and child (Young et al., 2001). In several biparental mothers, researchers found that maternal female rats exhi- species fathers exhibit parenting behavior similar to mothers biting high levels of LG-ABN showed greater OT receptor (Bredy et al., 2004; Frazier et al., 2006; Ahern and Young, densities in brain areas central for parenting, including the 2009), yet fathers tend to engage in a specific mode of medial preoptic area, the lateral septum, and the paraven- parental contact. Following separation, monogamous tricular nucleus of the hypothalamus, as compared to mothers and fathers increased their parenting behavior; mothers exhibiting low LG-ABN (Francis et al., 2000; Cham- however, mothers engaged in licking and contact while pagne et al., 2001). In rats, the mother’s high or low LG style fathers provided tactile stimulation, carried the infants in was stable over time and was transmitted from mother to space, and encouraged exploratory behavior (Lonstein and daughter through mechanisms of early experience (Cham- De Vries, 1999). Thus, it is possible that whereas hormones pagne et al., 2001, 2003). Females bred to a strain of low LG- associated with birth, lactation, and affectionate contact ABN mothers and reared by high LG-ABN dams showed the may induce hormonal changes in mothers, tactile stimulation high licking-and-grooming parenting pattern toward their and active forms of behavior such as exploration may shape own infants and exhibited the brain OT profile typical of the neuroendocrine basis of fathering. the high LG-ABN strain (Francis et al., 2000; Champagne, Like mammals, human fathers engage in interactions that 2008). Studies in nonhuman primates have similarly demon- involve proprioceptive and stimulatory contact and their play strated correlations between plasma OT and the degree of is often directed toward active exploration of the environ- maternal—infant grooming and contact (Maestripieri et al., ment (Lamb, 1976; Parke and Sawin, 1976). Father—child 2009). Taken together, these findings suggest that both cen- interactions typically take the form of ‘‘rough-and-tumble’’ tral and peripheral OT is related to individual variations in stimulatory play and have shown to be highly rewarding and affectionate contact between mother and young. to increase the father and child’s positive arousal (Feldman, Human mothers, like other mammalian mothers, engage 2003). Consistent with the findings that early experience in the species-typical forms of affectionate contact. In activates the neuroendocrine basis of parenting, it is thus humans, maternal affectionate contact is expressed in hold- possible that the species-typical stimulatory play of human ing the infant in a cradling position and providing affection- fathers induces OT release and natural variations in paternal ate touch, including caresses, soft kisses, light pokes, hugs, stimulatory contact would be expressed in systematic and gentle touches that do not serve a specific instrumental changes in paternal OT. purpose. The mother’s high or low affectionate contact style In light of the above, the overall goal of the present study is similarly stable over time and contributes to the infant’s was to assess the involvement of the oxytocinergic system in neurobehavioral, cognitive, and social—emotional growth human mothering and fathering and to address its consis- (Feldman and Eidelman, 2003; Feldman, 2007). Similarly, tency with parenting in other mammals. First, we sought to plasma OT levels in human mothers were found to be indi- examine whether baseline levels of plasma and salivary OT in vidually stable from early pregnancy to the postpartum and