Oxytocin, cortisol, and triadic family interactions
Ilanit Gordona, Orna Zagoory-Sharonb, James F. Leckmanc, Ruth Feldmana,b,c,⁎
aDepartment of Psychology, Bar-Ilan University, Ramat-Gan, Israel
bGonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan, Israel
cYale University Medical School, Child Study Center, 230 South Frontage Rd. New Haven, CT 06520, USA
a b s t r a c ta r t i c l e i n f o
Received 9 June 2010
Received in revised form 21 July 2010
Accepted 10 August 2010
The neuropeptide oxytocin (OT) supports the development of parenting in mammals primarily through its
impact on parent–infant proximity and touch behaviors; however, much less is known about the links
between OT and parental touch and contact in humans. In this study, we examined the relations between
maternal and paternal OT and patterns of touch and contact in the family unit during triadic interactions.
Thirty-seven parents and their firstborn child were seen twice: during the 2nd and 6th postpartum month.
Plasma OT and salivary cortisol (CT) were assessed with ELISA methods. At six months, triadic mother–
father–infant interactions were videotaped and micro-coded for patterns of proximity, touch, and gaze
behavior. Triadic synchrony, defined as moments of coordination between physical proximity and
affectionate touch between the parents as well as between parent and infant while both parent and child
are synchronizing their social gaze, was predicted by both maternal and paternal OT. Among mothers, triadic
synchrony was also independently related to lower levels of CT. Results highlight the role of OT in the early
formation of the family unit at the transition to parenthood.
© 2010 Elsevier Inc. All rights reserved.
Oxytocin (OT), named for quick delivery  and known for its
involvement in uterine contractions during birth and lactation , has
long been considered a maternal mammalian hormone. Animal research
has shown that central OT injections rapidly induce maternal behavior
[3,4] and studies have pointed to the role of maternal touch and contact
patterns, such as licking-and-grooming behavior, in the consolidation of
the brain OT system in both mother and infant [5–8]. Studies have
similarly underscored the importance of touch and contact in the cross-
generation transmission of OT in mammals [9–13]. In humans, OT has
been implicated in a variety of skills related to social affiliation, including
fearful social cues , and improved ability to infer the mental states of
betweenOT andtriadicfamilyinteractions,thefirstsocialgroup inwhich
the human infant takes part.
has recently become an area of interest. Research has indicated that
mothers exposed to infant stimuli showed an increased fMRI BOLD
response in brain areas rich in OT receptors . An increase in maternal
plasma OT from the first to the third trimester of pregnancy was
associated with maternal bonding to the fetus , and higher levels of
maternal plasma OT in the first trimester predicted more maternal
behavior in the postpartum, including greater amounts of maternal
affectionate touch . Similar levels of plasma OT concentrations were
and OT levels were related to the parent-specific behavioral repertoire
including positive affect, “motherese” vocalizations, and affectionate
touch in mothers and stimulatory contact and exploratory behavior in
fathers . Finally, following a session of parent–infant contact, an
increase in parental OT levels was found only among mothers who
provided high levels of affectionate touch and among fathers who
provided high levels of stimulatory contact but not among those who
exhibited low levels of the parent-specific pattern of touch and contact
. Taken together, these studies point to the relations between OT and
development of the whole-family process has not yet been assessed.
Research on the development of parent–infant bonding has mainly
the development of triadic mother–father–infant interactions received
less attention. Several studies addressed the development of the whole-
family process during the transition to parenthood [23–25]. For instance,
four-month-old infants were found to be capable of responding to subtle
social signals between their parents and shift their focus of social gaze
following change in the co-parental behavior . Researchers have
life that enables infants to function within a multi-person triadic context
. Parents and their four-month-old firstborn child were found to
Physiology & Behavior 101 (2010) 679–684
⁎ Corresponding author. Department of Psychology and the Gonda Brain Sciences
Center, Bar-Ilan University, Ramat-Gan, Israel 52900. Tel.: +972 3 531 7943; fax: +972
3 535 0267.
E-mail address: firstname.lastname@example.org (R. Feldman).
0031-9384/$ – see front matter © 2010 Elsevier Inc. All rights reserved.
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lower infantnegativeemotionality,less maternalanxietyand depression,
and higher paternal involvement and support. Similarly, higher family-
level cohesiveness was shaped by the nature of the interactions between
each parent and the child during parent–child sessions, with more
reciprocal parent–child interactions leading to more synchronous triadic
sessions . Based on dynamic systems' theory applied to the study of
family systems, the construct of “triadic synchrony” [25,28] implies that
there is coordination between the various sub-systems in the family and
that the spousal, mothering, and fathering sub-systems cohere into a
unified higher-order process that is marked by synchrony and cohesive-
In humans as well as in other mammals, mother–infant proximity
and touch play a critical role in infant development, regulating
adaptive physiological and psychological functions [34–36]. Attach-
ment theory  emphasizes the role of the caregiver's touch in
establishing a secure bond that enables the internalization of a sense
of securityandfreedom to exploretheenvironment.Animalresearch
has shown that maternal touch patterns, such as licking and
grooming and arched-back nursing, carry epigenetic effects and
lead to the cross generational transmission of OT and parenting
behavior [5,10,38]. Among premature infants, maternal infant skin-
to-skin contact (Kangaroo Care) during the immediate postpartum
period was found to result in higher maternal and paternal
affectionate touch at three months and in an increase in the degree
of proximity and touch between spouses during triadic family
interactions . Guided by the family system's approach, the
present study focused on the role of maternal and paternal OT in
shaping the parents' capacity to engage in a synchronous and
coherent triadic interaction that coordinates higher levels of touch
and contact among spouses with greater contact between each
parent and the child into the mutually-responsive multi-person
An additional hormone that is considered a part of the neuro-
endocrine system that supports the parent–infant bond is cortisol
(CT). Cortisol is the end product of the HPA axis that plays a central
role in stress reactivity as well as in a range of social and affiliative
behavior . In humans, elevated levels of CT have been reported
during periods of social bonding, such as falling in love or at the
transition to parenthood [40,41]. CT has been consistently
implicated in human maternal behavior and responsiveness to
the infant [42–45], however, the associations between CT and
parenting have shown to be complex, depending on multiple
factors including maternal age, prior experience, and feeding
patterns . The transition to parenthood is among the most
stressful life transitions for an individual and thus, CT was
measured in addition to OT, in order to assess the effects of stress
on the development of the family process and to examine the
associations between hormonal indices of stress and affiliation and
the nature of triadic interactions. In general, the relationships
between OT and CT are complex and not yet fully understood. On
the one hand, OT is considered to be an anti-stress hormone,
mediating anxiolytic and relaxing effects that are associated with
the calm state of breastfeeding [47–49]. On the other hand,
negative [50–53], positive [54–57], and non-significant [19,58]
correlations have been reported between OT and CT, suggesting
that the inter-relationship between the functioning of these two
systems is not yet fully understood.
In light of the above, the present study examined the links
between triadic family interactions and maternal and parental OT
and CT. Consistent with previous research [20,27], we expected that
OT would be related to more touch and contact in the family context
whereas CT would be negatively related to triadic synchrony and
that each hormone would explain unique variance in the prediction
of triadic synchrony. As the transition to parenthood is more
stressful for mothers than fathers, we expected closer links between
CT and triadic synchrony among mothers as compared to fathers.
Thirty-seven cohabitating couples and their firstborn infant (22
girls and 15 boys) participated in this study (overall: n=111
participants), which was part of a larger project on the transition to
parenthood. All infants were healthy firstborns. Parents were seen
twice, at the second month after the child's birth (M=6.97 weeks,
SD=2.35) and again when the infant was approximately 6 months
old (M=25.49 weeks, SD=4.61). Families were all of middle class
and all parents were married. Mothers age averaged 26.26 years
(SD=3.94) and fathers' age averaged 28.81 years (SD=4.73).
Parents all completed at least high-school education and the
average education was 15.35 years for men (SD=3.27) and
15.96 years for women (SD=2.29). Families were recruited through
ads posted in the university and surrounding area and in parenting
message boards online. The study was approved by the Institutional
Review Board and conducted according to ethical standards. All
participants signed informed consent forms prior to participation.
Families were visited at home twice during the evening hours
(4–8 PM). Mothers and fathers first completed self-report measures
assessing a range of demographic and health variables (e.g., weight,
height, and smoking). Next, blood was drawn for OT analysis and
interactions were videotaped between each parent and the child.
On the second home visit, families were videotaped in a free-play
triadic interaction. To allow for an ecologically valid observation of
the family process, parents were instructed that the two of them
play together with the infant as they normally do and no specific
position or toys were required. Parents were then given tubes for
collecting saliva for CT.
1.3.1. Plasma OT
Blood for OTanalysiswas drawnfrom antecubital veinsinto a 9 mL
chilled vacutainer tube containing that were supplemented with
400 KIU of Trasylol (Trasylol — Bayer, Germany) per 1 mL blood.
Samples were kept ice-chilled for up to two hours before being
centrifuged at 4 °C at 1000×g for 15 min. Supernatants were collected
and storedat −70 °C until assayed.Fathers were asked to refrainfrom
food intake for at least 30 min prior to blood draw. Determination of
OT was performed using a commercial OT ELISA kit (Assay Design, MI,
USA) as described in earlier studies [19,20,58,59]. Measurements
were performed in duplicate and the concentrations of samples were
calculated by using MatLab-7 according to relevant standard curves.
The intra-assay and inter-assay coefficient were less than 12.4 and
1.3.2. Salivary cortisol
Saliva for CT analysis was sampled on a single day during the
2 weeks following each of the home visits. In order to assess diurnal
CT levels, parents were given 3 rolls of cotton (Salivettes — Sarstedt,
Rommelsdorft, Germany) and were asked to place them in their
mouthsandchewonthemfora minuteuntil theybecamesaturatedat
three time-points during a single day. The first assessment was upon
waking, the second assessment was 30 min later, and the third
assessment was upon going to sleep at night. As CT displays diurnal
change patterns across the day, two CT morning samples were
I. Gordon et al. / Physiology & Behavior 101 (2010) 679–684
collected upon wakening and 30 min after wake-up in order to assess
the awakening CT response. The third assessment before going to bed
measures the diurnal HPA axis activity at its lowest level throughout
the day and this measurement time-point reflects the ability of CT to
unbind from receptors and drop significantly in order to allow for
the calm state that enables sleep (for review see  ). Research has
shown that dysregulated basal CT levels are correlated with distress,
pathology, illness and early life adversity [61–64]. As data was not
collected in predetermined hours across the day, since waking and
bedtime occurred at different hours for each individual, the typical
assessment of CT under the curve, which reflects cortisol activity
throughout the day could not be computed. In addition, the expected
CT awakening response was not found in this study, either due to the
parents' not being able to collect saliva exactly at awakening or
because of a blunted morning stress response associated with the
disrupted sleep of new parents in the first period after childbirth
[Gunnar M., personal communication, June 15, 2010]. In light of
these limitations regarding morning CT levels, only the evening
measure of CT was analyzed in this study. This evening measure was
considered to reflect basal non-reactive cortisol levels that most
appropriately match basal OT levels assessed in this research as well
as the stable parental behaviors that emerge during a free triadic
play which were not intended to elicit stress or examine stress
CT salivettes were kept ice-chilled in parents' freezers at home,
until being collected and broughtto the lab chilled. Upon arrival to the
lab, sampleswere centrifuged at 4 °Cat 1000×g for15 min. Saliva was
collected and stored at −20 °C until assayed. Free CT levels were
assayed using a commercial ELISA kit (Assay Design). Measurements
were performed according to the kit's instructions. CT levels were
calculated by using MatLab-7 according to relevant standard curves.
The intra-assay and inter-assay coefficients are less than 10.5% and
1.4. Triadic interactions
Interactions were micro-coded by trained graduate students of
psychology on a computerized system (The Observer, Noldus, The
Vaggenigen, Netherlands) consistent with previous research on
triadic interactions in infancy that used the same coding system
[35,65–67]. Interactions were coded in three passes for each sub-
system in the family: spousal, mother–child, and father–child.
Consistent with previous research, infant–mother and infant–father
episodes within a triadic interaction were considered moments in
which each parent and the infant were looking at each other (e.g.,
infant gazes at father and father gazes at infant). For each sub-
system we coded four behavioral categories of each partner: gaze,
affect, proximity position, and touch and each category included a
set of mutually-exclusive codes (an “uncodable” code was added to
each category to address moments when codes could not be
determined). Categories and codes for each sub-system were as
(a) The parent–infant sub-system
Parent Gaze — to partner, to infant, to object or aspects of the
environment, gaze aversion (gaze is not directed to partner,
infant, or objects). Parent Affect — positive, neutral, withdrawn,
negative; Proximity — infant in parent's hands or on parent's
lap, infant is positioned within the parent's arms' reach, infant
is far and out of parent's arms' reach. Parental Touch —
affectionate touch (e.g., hugging, kissing, and stroking), touch
of infant extremities, functional touch, proprioceptive touch
(i.e., changing infant position in space), touch with another
object, stimulatory touch, passive touch, none.
Infant Gaze— to mother,to father, to object or the environment,
gaze aversion; Infant Affect — positive, neutral, withdrawn,
negative; Infant Touch — touching father, touching mother,
touching both parents, no touch. Infant Proximity Position — on
parents' shoulders or in parents' hands, on parents' lap, in an
infant-seat chair, free (on couch, carpet, etc.).
(b) The spousal sub-system (coded for both mother and father)
Proximity — parents in close physical contact, parents within
arms' reach, parents far from each other's arms' reach. Touch —
affectionate touch, functional touch, accidental touch, none.
Inter-rater reliability was conducted for 10% of the interactions
and averaged 98% (kappa=.84). For each behavior, we computed
the proportions of time out of the entire interaction this behavior
had occurred and the mean durations of each episode for this
To create the composite of triadic synchrony, conditional proba-
bilities were computed which assessed the proportion of time a
behavior occurs given a certain baseline state. On the basis of our a-
prior hypotheses and previous [20,25,66–68] Triadic Synchrony was
computed for each parent as the proportions of time mothers and
father were in co-parental proximity (contact between parents) and
provided affectionate touch to each other given the infant was either
in physical contact with the father, the mother, or both and mutual
gaze was observed between the infant and one of the parents. This
behavioral composite was intended to portray the degree of
synchrony within the triadic family context that integrates compo-
nents of proximity and contact between all family members into a
communication system that includes mutual social gaze and tactile
contact intothe family system.This construct of triadic synchrony was
based on our previous studies showing that such proximity and touch
between mother, father, and infant differentiated infants who
received early tactile contact (Kangaroo Care) from those not
receiving such contact . Similarly, we found in previous work
that triadic synchrony related to micro-level patterns of touch and
contact in infancy predicted children's social competence at the
kindergarten during the preschool years , and this measure was
thus selected to index triadic synchrony.
2.1. Plasma oxytocin and salivary cortisol
Levels of OT and evening CT at the first and second assessments are
presentedinTable1. Asingle outlier higherthan3 SDs above meanwas
removed from the first assessment and 2 outliers were removed from
the second assessments. OT levels in parents showed high individual
stability across the study period. Pearson correlations between the two
assessments were, r=.61, pb.001 for mothers and, r=.78, pb.001 for
Plasma oxytocin and salivary cortisol concentrations in mothers and fathers at the
second and sixth months postpartum.
I. Gordon et al. / Physiology & Behavior 101 (2010) 679–684
fathers. Plasma OT levels in fathers and mothers were comparable at
both time-points. Overall there was a marginal increase in OT levels
betweenboth time-points: t(60)=−1.957, p=.055. Paired comparison
t tests to compare paternal and maternal levels were non-significant in
pN.1 for TIME 2. Considering the high correlations between TIME 1 and
TIME 2 measures of OT, for all following analyses OT levels across
assessments were averaged into a single score.
Evening CT levels similarly showed high individual stability:
fathers, r=.69, pb.001 and mothers, r=.47, pb.01. Paired compar-
ison t tests revealed that for fathers there was no significant change
in evening CT levels from TIME 1 to TIME 2: t(26)=.63, pN.1. On the
other hand, for mothers there was a significant rise in evening CT
levels from TIME 1 to TIME 2, t(25)=2.85, pb.05. Paired comparison
t test revealed that in the first assessment there were no differences
between maternal and paternal evening CT levels: t(37)=−.014,
pN.1. However, by the 6th postpartum month mothers had higher
evening CT levels compared to fathers, t(25)=−3.38, pb.005.
Plasma OT and Salivary Evening CT were unrelated in fathers and
mothers at the two time-points of the study.
Considering the high associations between TIME 1 and TIME 2 in
measures of CT, TIME 1 and TIME 2 CT levels were averaged into a
single score from which 3 outliers higher than 2 SDs over the mean
level were removed.
2.2. Correlations between hormones and triadic interaction
Paired comparison t tests revealed that triadic synchrony was
comparable in mothers and fathers: t(36)=1.02, pN.1 (mothers:
M=5.95, SD=11.06; fathers: M=8.37, SD=15.81), suggesting that
infants divide their time evenly in social focus to mother and father
during triadic interactions. Paternal and maternal triadic synchrony
scores were highly correlated: r=.82, pb.001. This high correlation is
due in part to the fact that the composite includes proximity
behaviors between spouses that are the same for both parents. The
mean duration of an episode of parent–infant contact during family
interactions was 22.35 s (SD=43.83) and ranged from 0 to 192.12 s.
2.3. Predicting triadic synchrony
Finally, two hierarchical multiple regression equations were
computed to predict triadic synchrony, once from maternal variables
and once from paternal variables. In the first block, the averaged
parental OT levels were entered, and in the second block the averaged
parental evening CT was entered. In the third block the interaction
between both hormones was entered. Results are presented in
As can be seen, both regression models were significant and
explained approximately 20% of the variance in triadic synchrony.
Among mothers, OT was an independent positive predictor and CT
was an independent negative predictor of triadic synchrony. It
appears that in mothers more OT and less CT predict more triadic
synchrony. For fathers, only OT independently predicted triadic
synchrony and no relations were found between paternal CT and
synchrony in the family triad, indicating that higher paternal OT
predicted higher levels of triadic synchrony. The interaction of OT and
CT did not predict additional variance above and beyond the two
hormones in both mothers and fathers.
Results of the present study provide the first data on the
associations between plasma OT and family interaction patterns
during triadic sessions between parents and their 6-month-old
firstborn child. The findings point to similarities between OT levels
in mothers and fathers and show that OT is associated with the degree
of proximity and affectionate contact between all members of the
family system — among spouses and between parents and child.
Finally, the findings also indicate that evening CT levels in mothers,
but not in fathers are negatively related to the level of synchrony with
the family triad.
In this study, OT and CT did not show significant correlations at
both the first post-birth period and at 6 months postpartum.
However, among mothers each hormone was uniquely predictive
of triadic synchrony, suggesting that each hormone specified a
unique neuro-endocrine channel to the development of touch and
contact in the family context. Previous research on the antenatal
predictors of maternal postpartum behavior demonstrated that
although OT and CT were unrelated across pregnancy and the
postpartum, they were each independently predictive of the amount
of maternal behavior, such as gaze to infants' face, “motherese”
vocalizations, affectionate touch, and positive maternal affect during
mother–infant interactions in the postpartum. Specifically, more OT
and less CT were each independently predictive of more such
maternal behaviors . These previous results support the present
findings by pointing to a potential integration of the stress and
affiliation neuro-endocrine systems in the formation of parenting
and the functioning of the family triad with OT indexing aspects of
bonding and affiliation while CT assessing stress levels. The findings
suggest that the mother's ability to engage in a synchronous and
coherent family process is likely shaped by the interplay between
these two hormonal systems.
Maternal CT was related to lower triadic synchrony but such
associations were not found for fathers. These findings are consistent
with theories suggesting that the experience of stress triggers a
relationship-related affiliation response in women termed “tend-and-
befriend” to counteract stress whereas men use “fight or flight”
strategies to manage stress . CT is associated with the develop-
ment of maternal behavior during the early postpartum period and
has been associated with maternal caregiving, attraction to the
newborn's body odor , and better discrimination of infant cry .
However, by six months of age, increased CT levels have shown to
predict negative indices of maternal behavior, such as intrusiveness
and controlling maternal behavior . Similarly, at 6 months touch
synchrony – the coordination of affectionate with the mother and
child's mutual gaze – was found to correlate with lower baseline CT in
mothers and infants . It is also possible that the greater
physiological demands following childbirth, the physiological burden
of breastfeeding, and the sleep deprivation that may be more
pronounced in mothers may have contributed to the negative
correlations between CT and triadic synchrony among mothers and
not among fathers. The rise in evening CT concentrations found only
in mothers from the 2nd to the 6th postpartum month may also
represent increased stress experienced by mothers during this period.
The findings indicate that by six months postpartum, maternal
evening CT was higher than paternal CT and this difference may
Regression models predicting triadic synchrony from maternal and paternal plasma
oxytocin and evening salivary cortisol.
BetaR2changeF changeBetaR2changeF change
R2total=.20, F (3, 34)=4.34,
R2total=.22, F (3, 34)=3.25,
I. Gordon et al. / Physiology & Behavior 101 (2010) 679–684
have accounted for the specific relations betweenmaternal CT and the
cohesive family process. Future research is required to further assess
the exact interplay of CT and OT as biomarkers of the stress and
affiliation systems in mothers and fathers and their differential impact
on parenting behavior in dyadic and triadic contexts. It is also
important to note that the current study focused on basal measures of
both CT and OT and further research is required to explore whether
reactive hormonal patterns may be involved in shaping the family-
level interaction patterns.
The findings indicate that despite the traditional associations with
maternal bonding, basal plasma OT levels are similar in mothers and
fathers. These findings are in line with research showing similarities
in women's and men's plasma  and cerebrospinal fluid OT levels
. Recent findings have pointed to the role of OT in the
development of paternalbehaviorduring the transitionto parenthood
and demonstrated links between paternal OT and patterns of paternal
touch [21,73]. Similarly, research assessing micro-level patterns of
proximity and touch in the family triad found no differences in the
proportions or frequencies of maternal and paternal affectionate
touch to the infant, as well as in their level of gaze, vocalizations, and
positive affect during triadic interactions . The present findings
contribute to this line of work by showing that touch patterns in the
triad, as expressed by both mother and father, are supported by
maternal and paternal OT. Our data echoes the work of Meaney and
colleagues' in animal models [5,7,9,10], which highlights the role of
OT in maternal touch patterns, and extend this model to human
parents, to fathers, and to whole-family process during the transition
In this study, hormonal biomarkers were sampled peripherally
from plasma and saliva. Contrary to the abundant literature on
salivary CT in humans, the relatively scant reports on OT in human
plasma using ELISA methodology and the ethical and practical
limitations in measuring central activity in humans should be
considered in the interpretation of the findings. Nevertheless, animal
studies point to a coordination between central and peripheral
measures of OT [74,75] as well as some reports on higher peripheral
levels following intranasal OT administration in humans . The
high stability of plasma OT levels across time reported here and
elsewhere and the growing number of reports on peripheral OT in
humans (for instance [77–79] support our reliance on peripheral
measures. Yet, this issue should be considered a study limitation and
requires much further research.
Parental touch during the first months of life is critical for the
infant's growth and survival and the neuro-endocrine pathways that
support parental touch behaviors in humans are thus of central
importance in healthy families and in families of high risk to the
parent–infant bond, such as following premature birth or when
mothers suffer postpartum depression. The current study lends
support to models that underscore the involvement of OT in these
pathways  and expands these models to the family social “group”.
Research on OT in humans has pointed to the role of OT in initiating
the “touch circuitry” between parents and infants and among couples.
Warm contact and touch between couples was associated with
increased OT levels [80–82]; infant tactile stimulation of the mother's
nipples during breastfeeding resulted in increased maternal OT
release ; and intense parental touch during parent–infant
interactions correlated with an increase in maternal and paternal OT
. These findings, combined with the present results, point to the
need to further assess the role of proximity and close contact between
attachment partners and its contribution to the consolidation of
affiliative bonds.Futurestudies are alsoneededtoexaminetheimpact
of parent–infant, spousal, and whole-family contact on the infant's
later social–emotional growth. Finally, it is important to assess
whether touch-related interventions initiate the OT bio-behavioral
feedback loop and function to increase OT levels under conditions of
disruption to the parent–infant bond.
The study was supported by the US–Israel Bi-National Science
Foundation (# 2005-273).
 Ivell R, Russell JA. Oxytocin: cellular and molecular approaches in medicine and
research. Rev Reprod 1996;1:13–8.
 Gimpl G, Fahrenholz F. The oxytocin receptor system: structure, function, and
regulation. Physiol Rev 2001;81:629–83.
 Keverne EB, Kendrick KM. Oxytocin facilitation of maternal behavior in sheep. Ann
NY Acad Sci 1992;652:83–101.
 Pedersen CA, Prange Jr AJ. Induction of maternal behavior in virgin rats after
intracerebroventricular administration of oxytocin. Proc Natl Acad Sci USA
 Francis DD, Champagne FC, Meaney MJ. Variations in maternal behavior are
associated with differences in oxytocin receptor levels in the rat. J Neuroendo-
 Champagne F, 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 USA 2001;98:12736–41.
 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;14:349–53.
 Shahrokh DK, Zhang TY, Diorio J, Gratton A, Meaney MJ. Oxytocin–dopamine
interactions mediate variations in maternal behavior in the rat. Endocrinology
 Meaney MJ. Maternal care, gene expression, and the transmission of individual
differences in stress reactivity across generations. Annu Rev Neurosci 2001;24:
 Champagne F, Meaney MJ. Like mother, like daughter: evidence for non-genomic
transmission of parental behavior and stress responsivity. Prog Brain Res
 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;79:359–71.
 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.
 Champagne FA. Epigenetic mechanisms and the transgenerational effects of
maternal care. Front Neuroendocrinol 2008;29:386–97.
 Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E. Oxytocin increases trust in
humans. Nature 2005;435:673–6.
 Ditzen B, Schaer M, Gabriel B, Bodenmann G, Ehlert U, Heinrichs M. Intranasal
oxytocin increases positive communication and reduces cortisol levels during
couple conflict. Biol Psychiatry 2009;65:728–31.
 Petrovic P, Kalisch R, Singer T, Dolan RJ. Oxytocin attenuates affective evaluations
of conditioned faces and amygdala activity. J Neurosci 2008;28:6607–15.
 Domes G, Heinrichs M, Michel A, Berger C, Herpertz SC. Oxytocin improves “mind-
reading” in humans. Biol Psychiatry 2007;61:731–3.
 Strathearn L, Fonagy P, Amico J, Montague PR. Adult attachment predicts maternal
brain and oxytocin response to infant cues. Neuropsychopharmacology 2009;34:
 Levine A, Zagoory-Sharon O, Feldman R, Weller A. Oxytocin during pregnancy and
early postpartum: individual patterns and maternal–fetal attachment. Peptides
 Feldman R, Weller A, Zagoory-Sharon O, Levine A. Evidence for a neuroendocri-
nological foundation of human affiliation: plasma oxytocin levels across
pregnancy and the postpartum period predict mother–infant bonding. Psychol
 Gordon I, Zagoory-Sharon O, Leckman JF, Feldman R. Oxytocin and the
development of parenting in humans. Biol Psychiatry 2010.
 Feldman R, Gordon I, Schneiderman I, Weisman O, Zagoory-Sharon O. Natural
variations in maternal and paternal care are associated with systematic changes in
oxytocin following parent–infant contact. Psychoneuroendocrinology 2010.
 McHale JP. Charting the bumpy road of coparenthood: understanding the
challenges of family life. Washington, DC: Zero To Three; 2007.
 McHale J, Fivaz-Depeursinge E, Dickstein S, Robertson J, Daley M. New evidence
for the social embeddedness of infants' early triangular capacities. Fam Process
 Gordon I, Feldman R. Synchrony in the triad: a microlevel process model of
coparenting and parent–child interactions. Fam Process 2008;47:465–79.
 Fivaz-Depeursinge E, Corboz-Warnery A. The primary triangle: a developmental
systems view of mothers, fathers, and infants. New York: Basic Books; 1999.
 Feldman R. Maternal versus child risk and the development of parent–child and
family relationships in five high-risk populations. Dev Psychopathol 2007;19:
 Feldman R, Masalha S. Parent–child and triadic antecedents of children's social
competence: cultural specificity, shared process. Dev Psychol 2010;46:455–67.
 Cox MJ, Paley B. Families as systems. Annu Rev Psychol 1997;48:243–67.
 Katz LF, Woodin EM. Hostility, hostile detachment, and conflict engagement in
marriages: effects on child and family functioning. Child Dev 2002;73:636–51.
I. Gordon et al. / Physiology & Behavior 101 (2010) 679–684
 Feldman R, Masalha S, Alony D. Microregulatory patterns of family interactions: Download full-text
cultural pathways to toddlers' self-regulation. J Fam Psychol 2006;20:614–23.
 Keren M, Feldman R, Namdari-Weinbaum I, Spitzer S, Tyano S. Relations between
parents' interactive style in dyadic and triadic play and toddlers' symbolic
capacity. Am J Orthopsychiatry 2005;75:599–607.
 Kitzmann KM. Effects of marital conflict on subsequent triadic family interactions
and parenting. Dev Psychol 2000;36:3–13.
 Hofer MA. Hidden regulators: implications for a new understanding of
attachment, separation, and loss. In: Golberg RM S, Kerr J, editors. Attachment
theory: social, developmental, and clinical perspectives. Hillsdale, NJ: Analytic
Press; 1995. p. 203–30.
 Feldman R, Weller A, Sirota L, Eidelman AI. Testing a family intervention
hypothesis: the contribution of mother–infant skin-to-skin contact (kangaroo
care) to family interaction, proximity, and touch. J Fam Psychol 2003;17:
 Stack DM, Muir DW. Adult tactile stimulation during face-to-face interactions
modulates five-month-olds' affect and attention. Child Dev 1992;63:1509–25.
 Bowlby J. Attachment and loss. New York: Basic Books; 1969.
 Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, et al.
Epigenetic programming by maternal behavior. Nat Neurosci 2004;7:847–54.
 DeVries AC, Glasper ER, Detillion CE. Social modulation of stress responses. Physiol
 Carter CS. Neuroendocrine perspectives on social attachment and love.
 Marazziti D, Canale D. Hormonal changes when falling in love. Psychoneuroen-
 Fleming AS, Steiner M, Corter C. Cortisol, hedonics, and maternal responsiveness
in human mothers. Horm Behav 1997;32:85–98.
 Fleming AS, Corter C, Franks P, Surbey M, Schneider B, Steiner M. Postpartum
factors related to mother's attraction to newborn infant odors. Dev Psychobiol
 Stallings, J., Fleming, A. S., Corter, C., Worthman, C., & Steiner, M. The effects of
infant cries and odors on sympathy, cortisol, and autonomic responses in new
mothers and nonpostpartum women. Parenting 2001;1:71–100.
 Maestripieri D. Biological bases of maternal attachment. Current Directions in
Psychological Science 2001;10:79–83.
 Krpan KM, Coombs R, Zinga D, Steiner M, Fleming AS. Experiential and hormonal
correlates of maternal behavior in teen and adult mothers. Horm Behav 2005;47:
 Uvnas-Moberg K. Oxytocin linked antistress effects—the relaxation and growth
response. Acta Physiol Scand Suppl 1997;640:38–42.
 Uvnas-Moberg K. Antistress pattern induced by oxytocin. News Physiol Sci
 Neumann ID. Brain oxytocin: a key regulator of emotional and social behaviours in
both females and males. J Neuroendocrinol 2008;20:858–65.
 Altemus M, Deuster PA, Galliven E, Carter CS, Gold PW. Suppression of
hypothalmic–pituitary–adrenal axis responses to stress in lactating women. J
Clin Endocrinol Metab 1995;80:2954–9.
 Heinrichs M, Gaab J. Neuroendocrine mechanisms of stress and social interaction:
implications for mental disorders. Curr Opin Psychiatry 2007;20:158–62.
 Heinrichs M, Baumgartner T, Kirschbaum C, Ehlert U. Social support and oxytocin
interact to suppress cortisol and subjective responses to psychosocial stress. Biol
 Meinlschmidt G, Heim C. Sensitivity to intranasal oxytocin in adult men with early
parental separation. Biol Psychiatry 2007;61:1109–11.
 Hoge EA, Pollack MH, Kaufman RE, Zak PJ, Simon NM. Oxytocin levels in social
anxiety disorder. CNS Neurosci Ther 2008;14:165–70.
 Marazziti D, Dell'Osso B, Baroni S, Mungai F, Catena M, Rucci P, et al. A relationship
between oxytocin and anxiety of romantic attachment. Clin Pract Epidemol Ment
 Taylor SE, Gonzaga GC, Klein LC, Hu P, Greendale GA, Seeman TE. Relation of
oxytocin to psychological stress responses and hypothalamic–pituitary–adreno-
cortical axis activity in older women. Psychosom Med 2006;68:238–45.
 Tops M, van Peer JM, Korf J, Wijers AA, Tucker DM. Anxiety, cortisol, and
attachment predict plasma oxytocin. Psychophysiology 2007;44:444–9.
 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;45:349–52.
 Carter CS. Sex differences in oxytocin and vasopressin: implications for autism
spectrum disorders? Behav Brain Res 2007;176:170–86.
 Kudielka BM, Wust S. Human models in acute and chronic stress: assessing
determinants of individual hypothalamus–pituitary–adrenal axis activity and
reactivity. Stress 2010;13:1–14.
 Aziz NA, Pijl H, Frolich M, van der Graaf AW, Roelfsema F, Roos RA. Increased
hypothalamic–pituitary–adrenal axis activity in Huntington's disease. J Clin
Endocrinol Metab 2009;94:1223–8.
 Nicolson NA, Davis MC, Kruszewski D, Zautra AJ. Childhood maltreatment and
diurnal cortisol patterns in women with chronic pain. Psychosom Med 2010;72:
 Gunnar MR, Quevedo KM. Early care experiences and HPA axis regulation in
children: a mechanism for later trauma vulnerability. Prog Brain Res 2008;167:
 Dozier M, Manni M, Gordon MK, Peloso E, Gunnar MR, Stovall-McClough KC, et al.
Foster children's diurnal production of cortisol: an exploratory study. Child
 Feldman R, Eidelman AI, Rotenberg N. Parenting stress, infant emotion regulation,
maternal sensitivity, and the cognitive development of triplets: a model for parent
and child influences in a unique ecology. Child Dev 2004;75:1774–91.
 Feldman R, Eidelman AI. Direct and indirect effects of breast milk on the
neurobehavioral and cognitive development of premature infants. Dev Psychobiol
 Feldman R, Eidelman AI. Parent–infant synchrony and the social–emotional
development of triplets. Dev Psychol 2004;40:1133–47.
 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.
 Taylor SE, Klein LC, Lewis BP, Gruenewald TL, Gurung RA, Updegraff JA.
Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-
flight. Psychol Rev 2000;107:411–29.
 Mills-Koonce WR, Propper C, Gariepy JL, Barnett M, Moore GA, Calkins S, et al.
Psychophysiological correlates of parenting behavior in mothers of young
children. Dev Psychobiol 2009;51:650–61.
 Feldman R, Singer M, Zagoory O. Touch attenuates infants' physiological reactivity
to stress. Dev Sci 2010;13:271–8.
 Leckman JF, Goodman WK, North WG, Chappell PB, Price LH, Pauls DL, et al.
Elevated cerebrospinal fluid levels of oxytocin in obsessive–compulsive disorder.
Comparison with Tourette's syndrome and healthy controls. Arch Gen Psychiatry
 Gordon I, Zagoory-Sharon O, Leckman JF, Feldman R. Prolactin, oxytocin, and the
development of paternal behavior across the first six months of fatherhood. Horm
 Ross HE, Young LJ. Oxytocin and the neural mechanisms regulating social
cognition and affiliative behavior. Front Neuroendocrinol 2009;30:534–47.
 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;85:1209–22.
 Burri A, Heinrichs M, Schedlowski M, Kruger TH. The acute effects of intranasal
oxytocin administration on endocrine and sexual function in males. Psychoneur-
 Andari E, Duhamel JR, Zalla T, Herbrecht E, Leboyer M, Sirigu A. Promoting social
behavior with oxytocin in high-functioning autism spectrum disorders. Proc Natl
Acad Sci USA 2010;107:4389–94.
 Barraza JA, Zak PJ. Empathy toward strangers triggers oxytocin release and
subsequent generosity. Ann NY Acad Sci 2009;1167:182–9.
 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:
 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;70:976–85.
 Grewen KM, Girdler SS, Amico J, Light KC. Effects of partner support on resting
oxytocin, cortisol, norepinephrine, and blood pressure before and after warm
partner contact. Psychosom Med 2005;67:531–8.
 Light KC, Grewen KM, Amico JA. More frequent partner hugs and higher oxytocin
levels are linked to lower blood pressure and heart rate in premenopausal women.
Biol Psychol 2005;69:5–21.
 Matthiesen AS, Ransjo-Arvidson AB, Nissen E, Uvnas-Moberg K. Postpartum
maternal oxytocin release by newborns: effects of infant hand massage and
sucking. Birth 2001;28:13–9.
I. Gordon et al. / Physiology & Behavior 101 (2010) 679–684