Maternal and paternal plasma, salivary, and urinary oxytocin
and parent–infant synchrony: considering stress and affiliation
components of human bonding
Ruth Feldman, Ilanit Gordon and Orna Zagoory-Sharon
Department of Psychology and the Gonda Brain Sciences Center, Bar-Ilan University, Israel
Studies in mammals have implicated the neuropeptide oxytocin (OT) in processes of bond formation and stress modulation, yet
the involvement of OT in human bonding throughout life remains poorly understood. We assessed OT in the plasma, saliva, and
urine of 112 mothers and fathers interacting with their 4–6-month-old infants. Parent–infant interactions were micro-coded for
parent and child’s social behaviors and for the temporal coordination of their socio-affective cues. Parents were interviewed
regarding their attachment to the infant and reported on bonding to own parents, romantic attachment, and parenting stress.
Results indicated that OT in plasma (pOT) and saliva (sOT) were inter-related and were unrelated to OT in urine (uOT). pOT
and sOT in mothers and fathers were associated with parent and child’s social engagement, affect synchrony, and positive
communicative sequences between parent and child. uOT was related to moments of interactive stress among mothers only,
indexed by the co-occurrence of infant negative engagement and mother re-engagement attempts. pOTand sOT were associated
with mothers’ and fathers’ attachment relationships throughout life: to own parents, partner, and infant, whereas uOTcorrelated
with relationship anxiety and parenting stress among mothers only. Similar to other mammals, OT is involved in human
attachment and contingent parenting. The dual role of OT in stress and affiliation underscores its complex involvement in
processes of social bonding throughout life.
The parent–infant bond provides the primary relation-
ship in mammals that supports growth and development
and buffers against physiological and social stress
(Carter, 2005; Kendrick, Keverne & Baldwin, 1987;
Maestripieri, Hoffman, Anderson, Carter & Higley,
2009; Pedersen & Prange, 1979). Research across mam-
malian species has shown that the neuropeptide oxytocin
(OT) plays a key role in processes of bond formation and
functions to reduce stress, enhance social competence,
initiate maternal behavior, and promote social affiliation
throughout life (Francis, Champagne & Meaney, 2000;
Gimpl & Fahrenholz, 2001; Keverne & Kendrick, 1992;
Pedersen, 2004; Ross, Cole, Smith, Neumann, Landgraf,
Murphy & Young, 2009; Waldherr, Nyuyki, Malamby,
Bosch & Neumann, 2010; Winslow, Hearn, Ferguson,
Young, Matzuk & Insel, 2000). Among the central fea-
tures of the OT system is its openness to early social
experience (Ahern & Young, 2009; Champagne, Bagot,
van Hasselt, Ramakers, Meaney, de Kloet, Joels &
Krugers, 2008) and the effects of OT on brain organi-
zation are shaped early in life through the provision of
well-timed maternal behavior (Meaney, 2010). Young
mammals who received more maternal grooming and
contact exhibited higher OT receptor densities in brain
areas central for social affiliation, benefited more from
environmental enrichment, were better equipped to
handle stress, and provided more optimal parenting to
their own infants (Champagne, 2008; Champagne &
Meaney, 2007). Yet, in contrast to the abundance of
research on OT and bond formation in mammals, the
role of OT in human attachment has attracted less research.
To date, no study has addressed the relations between OT
and contingent parenting or the individual’s attachment
relationships throughout life. Understanding such links
may be important for uncovering the biological basis of
human attachment and assessing its consistency with
Oxytocin in plasma, saliva, and urine and attachment-
Research on OT and attachment-related processes in
humans has mainly examined plasma OT (pOT). For
instance, assessing OT repeatedly from early pregnancy
to the postpartum, pOT levels were individually stable
and predicted the amount of maternal postpartum
Address for correspondence: Ruth Feldman, Department of Psychology and the Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan, Israel
52900; e-mail: firstname.lastname@example.org
? 2010 Blackwell Publishing Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden, MA 02148, USA.
Developmental Science 14:4 (2011), pp 752–761 DOI: 10.1111/j.1467-7687.2010.01021.x
behavior, including gaze at infant, ‘motherese’ vocaliza-
tions, positive affect, and affectionate touch, pointing to
a priming effect of OT across pregnancy on the devel-
opment of mothering (Feldman, Weller, Zagoory-Sharon
& Levine, 2007). Mothers with secure attachment rep-
resentations showed pOT increases following mother–
infant interactions and greater BOLD fMRI response in
brain areas rich in OT receptors, such as the medial
preoptic area, lateral septum, and paraventricular
nucleus of the hypothalamus (Strathearn, Fonagy, Amico
& Montague, 2009). pOT increased in response to the
initiation of breastfeeding (Jonas, Johansson, Nissen,
Ejdeback, Ransjo-Arvidson & Uvnas-Moberg, 2009),
and newborn suckling and touch stimulated pOT release
Moberg, 2001). In addition, pOT has been linked with
processes of bonding throughout life. Adults with higher
pOTreported more optimal bonding to their own parents
(Gordon, Zagoory-Sharon, Schneiderman, Leckman,
Weller & Feldman, 2008) and secure attachment to
romantic partners (Tops, van Peer, Korf, Wijers &
Tucker, 2007). Similarly, non-verbal displays of love
between romantic partners correlated with pOT increase
(Gonzaga, Turner, Keltner, Campos & Altemus, 2006),
underscoring the role of OT in the individual’s lifetime
attachments: to parents, partners, and infants.
OT measured in saliva and urine has similarly been
associated with processes of social affiliation. Carter and
colleagues (2007) showed that salivary OT (sOT) is a
reliable biomarker of peripheral OT, and research has
demonstrated the presence of an OT receptor in the
human salivary gland (Forsyth & Neville, 2009). sOTwas
found to increase immediately before breastfeeding
(White-Traut, Watanabe, Pournajafi-Nazarloo, Schwertz,
Bell & Carter, 2009), after massage in adults (Carter,
Bello & Schwertz, 2007), and following touch-related
(Holt-Lunstad, Birmingham & Light, 2008). Following
parent–infant interaction, an increase in sOT was found
in parents who provided more tactile contact to their
infants, but not among those who displayed low levels of
touch (Feldman, Gordon, Schneiderman, Weisman &
Zagoory-Sharon, 2010). Similarly, urinary OT (uOT)
increased after mother–daughter conversation following
a stressful laboratory paradigm (Seltzer, Ziegler &
Pollak, 2010). These studies provide initial evidence for
the involvement of OT in bonding-related processes as
measured in plasma, saliva, and urine; yet no study to
date has assessed the correlations between OT measured
in these three peripheral systems at the same time.
The dual role of oxytocin in stress and affiliation
The anxiolytic effects of OT and its role in attenuating
the stress response are observed in both humans and
other mammals (Heinrichs & Gaab, 2007; Neumann,
2008). Authors have pointed to several mechanisms as
mediating the effects of OT on stress (Lee, Macbeth,
Pagani & Young, 2009). These include the enhancement
of neural activity in brain areas central for emotion and
cognitive processing while reducing activity in areas
controlling autonomic and visceral responses (Febo,
Shields, Ferris & King, 2009); modulating the release of
(Yoshida, Takayanagi, Inoue, Kimura, Young, Onaka &
Nishimori, 2009); and the role of variations in the OT
receptor gene in regulating anxiety (Costa, Pini, Martini,
Abelli, Gabelloni, Ciampi, Muti, Gesi, Lari, Cardini,
Mucci, Bucci, Lacacchini & Cassano, 2009). Yet, human
studies on the relations of OT and stress have yielded
mixed results. Whereas some found links between OT
and higher cortisol, an index of the stress response
(Marazziti, Dell’Osso, Baroni, Mungai, Catena, Rucci,
Albanese, Giannaccini, Betti, Fabbrini, Italiani, Del
Debbio, Lucacchini & Dell’Osso, 2006), others reported
correlations between OT and lower levels of stress
(Heinrichs & Gaab, 2007).
One reason for the inconsistent findings may relate to
the gender-specific effects of OT on stress. Carter and
colleagues (2009) suggested that the effects of early
rearing experiences on the oxytocinergic system is sexu-
ally dimorphic. Both acute and chronic OT manipula-
tions in animals bred for high and low anxiety showed
different effects in females and males (Slattery & Neu-
mann, 2010). Similarly, OT was related to relationship
distress in women, but not in men (Taylor, Saphire-
Bernstein & Seeman, 2010). It has been theorized that
since women use the formation of social bonds for the
management of stress, the links between OT and stress
are tighter in women (Taylor et al., 2000). It is thus
possible that among mothers OT would be more closely
related to stress, particularly stress within close rela-
tionships, due to its role as a signal to the mother to
form, maintain, nourish, and repair close bonds as a
means for regulating stress.
Oxytocin and parent–infant synchrony
Parent–infant synchrony, which describes the temporal
coordination between the parent and infant’s affective
behavior, is an important component of sensitive par-
enting that contributes to infant development (Feldman,
2007). Nelson and Panksepp (1998) suggest that hor-
monal changes in the mother across gestation, particu-
larly in OT and prolactin, prime the initiation of
maternal behavior following birth and provide the basis
for the development of contingent parenting.
Synchronous interactions are organized in repetitive-
rhythmic sequences that consist of matched affective
behaviors in the gaze, vocal, facial expression, and
touch modalities. Such moments of affect synchrony are
important for the maturation of the infant’s physio-
logical systems and shape the individual’s attachment
relationships throughout life (Feldman, 2010). Syn-
chronous exchanges may come in three forms according
Oxytocin and parent–infant synchrony 753
? 2010 Blackwell Publishing Ltd.
to the timed relationships between the parent and
child’s social behavior. Concurrent synchronous rela-
tions indicate that the parent and child coordinate their
affective behavior, and positive affective expressions
co-occur in the two partners. Sequential synchronous
relations imply that positive affective behaviors in one
partner are followed by similar positive behaviors in the
Finally, communications systems are dynamic in nature
and are underlaid by patterned cross-correlations be-
tween the partners’ behaviors that include a time-lag of
responsivity, for instance, when one partner becomes
more positive and the other follows by increasing po-
sitive engagement within a time-lag. Inherent in such
moments of synchrony are repeated episodes of mis-
match and repair, for instance, when the infant displays
negative affect and the parent attempts to re-establish
moments are likely to increase the parent’s stress, par-
ticularly among mothers who are more attentive to
mismatch within the relationship (Feldman, 2003) and
use social relationships for the management of stress
(Taylor, Klein, Lewis, Gruenewald, Gurung & Updeg-
The current study
In light of the above, the current study had three goals.
First, we examined similarities and differences between
maternal and paternal OTas expressed in plasma, saliva,
and urine. Although much less research examined OT
and fathering, OT in biparental fathers has been asso-
ciated with paternal behavior and pup exposure (Ziegler,
2000), and similar neuroendocrine pathways are theo-
rized to mediate the initiation of fathering and mothering
in mammals (Wynne-Edwards & Timonin, 2007). Thus,
similar levels of pOT, sOT, and uOT were expected in
mothers and fathers.
The second goal aimed to assess the relations
between OT and synchronous parent–infant interac-
tions. Both moments of concurrent affect synchrony
and sequences of positive engagement were expected to
correlate with OT in both mothers and fathers. The
degree of stress inherent in synchronous interactions,
indexed by the co-occurrence of infant negative emo-
tions and the parent’s re-engagement attempts, was
expected to correlate with higher maternal, but not
The final goal was to test the relations between OT in
the three fractions and the parent’s attachment rela-
tionships throughout life, including bonding to own
parents, romantic attachment, and attachment to infant.
Human bonds include components of both stress and
affiliation: romantic attachment involves anxieties for the
exclusivity of the relationship and parental attachment
involves biologically based preoccupations and worries
with regard to infant safety (Leckman, Feldman, Swain,
Eicher, Thompson & Mayes, 2004). Based on the dual
role of OT, we expected that indices of both stress and
affiliation would correlate with OT but that the links
between OT and stress would be more notable among
Participants were 112 parents and their infants, including
71 mothers and 41 fathers (not couples) and their 4–6-
month-old infants (M = 166.3 days, SD = 12.6). Parents
were of middle-class SES, healthy, and with at least
12 years of education. Mothers’ age was, M = 28.7,
SD = 5.29 years, and education, M = 15.17, SD =
2.47 years, and 81.3% were breastfeeding. Fathers’ age
M = 29.1,
SD = 4.28 years
M = 15.50, SD = 2.73 years. Infants were born at term
M = 3319.4
(96.3%) by vaginal delivery, received an Apgar score of
9.40 (SD = 1.56), and 55% were firstborns. Infants were
healthy since birth, and parents were screened for
depression and anxiety. Fathers reported at least med-
ium-level participation in childcare on a scale of 1–5,
which assessed how much parents shared childcare
responsibilities in terms of both time spent with child
and types of activities performed (e.g. bathing, feeding,
diapering, doctor’s visits). The study was approved by
the Institutional Review Board and all parents signed
SD = 452.1),mainly
Parents and infants arrived at the lab during the early
acquainting period when no touch or parent–child
interaction occurred (parent completed questionnaires
and RA took care of the infant), provided baseline
plasma, saliva, and urine samples in consecutive order.
Assessments were arranged to take place at least half
an hour after breastfeeding and to end at least half an
hour before breastfeeding, in light of White-Traut et al.
(2009), who showed that following a peak in OT
during the period surrounding breastfeeding, OT in
breastfeeding mothers returns to baseline levels. Then
parent and child entered an observation room with an
infant-seat mounted on a table and were filmed from
an adjoining room by two cameras that were integrated
into a single frame using a split-screen generator.
Parents were asked to engage in a 15-minute interac-
tion that would include any type of touch they typi-
cally use. Fifteen minutes after play, post-interaction
saliva and urine samples were collected. Blood was
drawn only once at baseline as our pilot study indi-
cated that multiple draws created high levels of stress.
Parents were then interviewed and completed self-
754Ruth Feldman et al.
? 2010 Blackwell Publishing Ltd.
Hormone collection and analysis
Blood was drawn from antecubital veins into 9 mL
chilled vacutainer tubes containing lithium heparin that
was supplemented with 400 KIU of Trasylol (Trasylol–
Bayer, Germany) per 1 mL blood. Blood samples were
kept ice-chilled for up to 2 hours before being centri-
fuged at 4?C at 1000 · g for 15 minutes. Supernatants
were collected and stored at )80?C until assayed.
sOTwas collected by Sallivatte (Sarstedt, Rommelsdorft,
Germany). Parents were asked to chew a roll of cotton
for 40 seconds. Salivettes were kept ice-chilled for up to
1 hour before being centrifuged at 4?C at 1500 · g for
15 minutes. The liquid samples were stored at )80?C. To
concentrate the samples by 3 or 4 times, the liquid
samples were lyophilized overnight and kept at )20?C
until assayed. The dry samples were reconstructed in the
assay buffer immediately before analysis by Oxytocin
EIA commercial kit, consistent with previous research
(Carter et al., 2007).
The method for OT extraction was taken from the kit
insert, with the following modifications to adjust the low
concentration of uOT. Two ml of urine were loaded on
HBL extraction cartridge 3 cc⁄60 mg (Waters Oasis,
MA, USA). The cartridges were washed twice with 0.1%
TFA and 10% acetonitrile solution. Samples were eluted
by 0.1% TFA and 80% acetonitrile solution, dried by
speed-vac, and kept at )20?C until assayed. For each
urine collection the process was repeated twice. The dry
samples were reconstructed in the assay buffer immedi-
ately before analysis by OT EIA commercial Kit.
Determination of oxytocin
OT was determined using a commercial OT ELISA kit
(Assay Design, MI, USA) consistent with previous
research (Carter et al., 2007; Feldman et al., 2007).
Measurements were performed in duplicate and the
concentrations of samples were calculated by using
MatLab-7 according to relevant standard curves. The
observed intra-assay and inter-assay coefficients were <
12.4% and 14.5%, respectively.
Coding of parent–infant interaction
Interactions were micro-coded on a computerized system
(Noldus, The Vaggenigen, Netherlands), consistent with
Eidelman, 2004, 2007). Four non-verbal categories of
behavior were coded and each category included a set of
mutually exclusive codes (an ‘uncodable’ code was added
be determined). Categories and codes were as follows:
Parent Gaze: This category assessed the direction of
parent gaze and included the following codes: gaze to
infant’s face, gaze to infant’s body; gaze to object or
environment; and gaze aversion, indicating that parent
gazes away from the infant but gaze is not focused on
other objects or the environment. Parent Affect: Parent’s
expressed affect was coded on the basis of facial
expressions, body tone, movements, and other non-ver-
bal signals and included positive, neutral, and negative
affective expression. Parent Vocalizations: The parent’s
vocal output was coded along four codes: ‘motherese’
vocalizations, which are infant-directed speech that is
high pitched and typically includes sing-song vocaliza-
tions; ‘typical’ adult speech to the infant in a normal
range and regular rhythm; adult speech to other adult;
and no speech. Parent Touch included six codes: affec-
tionate touch – loving touch such as hugging, kissing,
stroking, or light pokes; touch of infant extremities –
touch of infant’s hands or feet often with another object;
functional touch – touch that has a functional goal such
as wiping the infant’s mouth; proprioceptive touch –
includes touch that changes the infant’s position in
space, for instance, pulling the infant to a sitting posi-
tion; stimulatory touch – indicating touch that intends to
stimulate and increase arousal; and no touch.
Infant Gaze was coded similar to parent’s gaze along the
following codes: gaze to parent, gaze to object or envi-
ronment, and gaze aversion. Infant Affect was similarly
coded as positive, neutral, or negative. Infant Vocaliza-
tions: included positive vocalizations, such as positive
babbling, cooing, or giggles, negative vocalizations,
including fussing and crying. Infant Touch included
intentional, accidental, and no touch. Inter-rater reli-
ability was computed for 15 interactions and reliability
kappas averaged .84 (range = .76–.93)
The following composites were computed as the sum
proportions of several codes: Parent Positive Engagement
included parent gaze to infant, positive affect, and
‘motherese’ vocalizations. Infant Positive Engagement
included infant gaze to parent, positive affect, and
positive vocalizations. Infant Negative Engagement in-
cluded fuss-cry vocalizations and gaze aversion.
Two variables were created as measures of synchrony: (1)
Affect Synchrony – conditional probability indicated the
proportion of time parent and child coordinated their
Oxytocin and parent–infant synchrony 755
? 2010 Blackwell Publishing Ltd.
positive engagement. Using the median split, parents
were divided into High and Low Affect Synchrony
groups (median = .25).(2)
Sequences were computed using lag sequential analysis
and indicated the number of times the infant’s positive
affective engagement was followed by the parent’s posi-
Interactive Stress was the conditional probability of the
proportion of time the infant was in negative engagement
while the parent attempted to re-engage the child by
positive affect or ‘motherese’ vocalizations.
Measures of stress and affiliation in the parent’s
Parental attachment to infant and parenting preoccupa-
tions and worries
The adapted Yale Inventory of Parent Thought and
Action (YIPTA; Feldman, Weller, Leckman, Kuint &
Eidelman, 1999) is an instrument that assesses parent–
measure. Both the interview and the self-report consider
nine topics pertaining to the parent’s thoughts, worries,
feelings, attachment behaviors, and attachment-related
thoughts in the postpartum months, and the instrument
has been validated in several studies of healthy and high-
risk infants (Feldman et al., 2007; Feldman et al., 1999;
Leckman et al., 1999). A clinician interviewed the parent
for 30–45 minutes and first probed the parent’s free nar-
rative on each topic. Narratives were audiotaped, tran-
scribed, and coded by two coders on a scale from 1 (little)
to 5 (a lot) for each topic, with an inter-rater reliability
performed on 10 interviews averaging 95% (intraclass
r = .93). Next, parents completed questionnaires orga-
nized by the same topics. Two composites were included.
the self-report questionnaire, and the coded preoccupa-
tion score (alpha = .87). Attachment Representations was
the average of four items on the self-report questionnaire
and the parallel narrative attachment score (alpha = .86).
The Adult Attachment Style (Brennan & Shaver, 1998)
defines two dimensions of adult romantic attachment:
anxiety and avoidance, each measured with a reliable and
valid 18-item scale. Low anxiety and avoidance index
attachment security. High attachment anxiety indicates
stress within romantic relationships.
Bonding to parents
Tupling & Brown, 1979) includes 25 questions for
Parental Bonding Instrument(PBI; Parker,
mother and father. The average of mother and father
care scores indexed bonding to own parents and was
The Parenting Stress Index (PSI; Abidin, 1983) is a
36-item questionnaire measuring the magnitude of stress
in the parent–child system with good reliability and
Mean levels of OT and interactive behaviors in mothers
Prior to data analysis, Pearson correlations were com-
puted to test potential relationships between OT and
background variables. No correlations were found
between OT in plasma, saliva, and urine and demo-
graphic variables, including parent age, height, weight,
body mass index, smoking, use of medications, and
time of last meal. Maternal OT was unrelated to men-
strual cycle phase, contraceptive intake, mode of deliv-
ery (vaginal vs. c-section), feeding style (breastfeeding
vs. bottle-feeding), postpartum interval (weeks from
birth to date of assessment), or the interval from prior
breastfeeding. No differences in maternal OT level in
either fraction were observed between breastfeeding and
non-breastfeeding women, consistent with previous
research which found that when OT is not sampled
during breastfeeding, no differences are found between
breastfeeding and non-breastfeeding women (Feldman
et al., 2010; Gordon, Zagoory, Leckman & Feldman,
Descriptive statistics for baseline OT in the three
fractions and interactive behavior are presented in
Table 1 and show no differences between mothers and
fathers in OT levels, parent and child’s Positive and
Negative Engagement, and Affect Synchrony. Mothers
showed more Interactive Stress and more Positive
Communicative Sequences during play. All following
correlation and regression analyses were conducted with
baseline OT measures.
Significant correlations emerged between pOT and
sOT, r = .41, p < .001, indicating some degree of con-
cordance between the two measures, and the correlations
were of similar magnitudes in mothers and fathers. uOT
was unrelated to pOT, r = ).06, ns, or sOT, r = ).03, ns,
in the combined parents groups and were of similar
magnitudes in mothers and fathers.
Assessing differences in baseline OT between the
high- and low-Affect Synchrony groups, differences
between the high- and low-Affect Synchrony groups
were found for pOT, F(1, 111) = 6.24, p < .01, Effect
Size (ES) = .11, and sOT, F(1, 111) = 4.76, p < .05,
ES = .06 (Figure 1).
756 Ruth Feldman et al.
? 2010 Blackwell Publishing Ltd.
Relations between OT and parent–infant interactive
Pearson correlations between pOT, sOT, and uOT and
parent–infant interactive behavior appear in Table 2. As
seen, pOT and sOT correlated with parent Positive
Engagement, Affect Synchrony, and Positive Communi-
cative Sequences between parent and child. Infant Posi-
tive Engagement was related to parent pOT and
marginally to sOT. These correlations were significant for
both mothers and fathers. However, correlations between
uOT and any interactive variable were significant among
mothers only. uOT correlated with the infant’s Negative
Engagement with mother and with the mother’s Inter-
active Stress (Figure 2).
Relations between OT and indices of stress and
Oxytocin was associated with the parent’s attachment
representations of the infant. pOT and sOT correlated
with the parent’s Attachment Representations, r = .30,
p < .01, r = .26, p < .05, respectively. sOTalso correlated
with Parental Preoccupations, r = .29, p < .01.
Bonding to parents
Bonding to own parents correlated with pOT, r = .30,
p < .01.
sOT correlated with attachment security as indexed by
low attachment anxiety, r = ).28, p < .05, and low
avoidance, r = ).32, p < .01.
The correlations reported for pOT and sOT were
for the entire sample of parents but were significant
Table 1 Plasma, salivary, and urinary OT and interactive behavior among mothers and fathers
Plasma OT – pOT (pg⁄ml)
Salivary OT – sOT (pg⁄ml)
Urinary OT – uOT (pg⁄ml)
Parent Positive Engagement
Infant Positive Engagement
Infant Negative Engagement
Positive Communicative Sequences
*p < .05
Note: Numbers represent baseline OT levels.
and fathers high and low on affect synchrony.
Baseline plasma and salivary oxytocin in mothers
plasma, saliva, and urine and parent–infant interaction
Correlations between oxytocin in parents’ baseline
Parent Positive Engagement
Infant Positive Engagement
Infant Negative Engagement
Positive Communicative Sequences
+p < .10; *p < .05; **p < .01.
Note: Correlations with uOT are reported for mothers only.
Correlation between urinary oxytocin and mothers’
Oxytocin and parent–infant synchrony 757
? 2010 Blackwell Publishing Ltd.
As hypothesized, uOT was related to relationship-related
stress among mothers only: to romantic attachment
anxiety, r = .29, p < .05, and parenting stress, r = .34,
p < .01.
Predicting Affect Synchrony and Interactive Stress
Two regression equations were computed predicting
Affect Synchrony and Interactive Stress from measures
of stress and affiliation. In light of the gender-specific
correlations reported above, the model predicting Inter-
active Stress included mothers only, whereas the model
predicting Affect Synchrony included both mothers and
fathers. Each model contained six predictor variables.
The first was the parent’s OT (pOT was entered for
Affect Synchrony and uOT for Interactive Stress). The
next two predictors included Parental Preoccupations
and Attachment Representations of the parent–child
relationship, followed by bonding to own parents,
attachment anxiety, and parenting stress. Results appear
in Table 3. As seen, pOT, Attachment Representations,
and bonding to own parents each explained unique
variance in Affect Synchrony. Interactive Stress was
uniquely predicted by uOT, maternal preoccupations,
and parenting stress, with marginal beta for attachment
anxiety among mothers. Overall, these physiological and
psychological variables explained 22% of the variance in
Affect Synchrony and Interactive Stress.
OT is the most abundant brain neuropeptide that pro-
vides the foundation for the capacity to form close
relationships (Gimpl & Fahrenholz, 2001). The present
study utilized a broad perspective on the relations of OT
and human bonding by analyzing OT in three peripheral
systems, using diverse methodologies such as micro-
analysis of non-verbal social cues and in-depth inter-
views, focusing on the parent’s multiple attachments
throughout life, and assessing indices of both stress and
affiliation within each relationship. Results demonstrated
the involvement of OT in micro-level processes of par-
ent–infant synchrony; in the parent’s attachments to his
or her own parents, partner, and infant; and in mothers’,
but not fathers’ relationship distress within the spousal
relationship, the parenting role, and the parent–infant
interaction. The study is also the first to compare OT
levels in plasma, saliva, and urine. Overall, the findings
point to substantial consistencies between human and
mammalian parenting and bonding-related processes,
and suggest that OTsupports bond formation in humans
similar to its role in other mammals. The comparable
levels of pOT, sOT, and uOT in mothers and fathers
similarly accord with animal research on the role of OT
in the development of paternal behavior in biparental
species (Ziegler, 2000). Notwithstanding cross-species
consistency, the relations between OT and micro-level
synchrony of visuo-affective facial signals and the par-
ent’s mental representations of attachment relationships
highlight the unique features of attachment in humans
and their specific links with the OT system.
Synchrony is a concept coined by the first researchers
on parenting in social animals that describes the coor-
dination of hormonal, behavioral, and physiological
stimuli between parent and infant during social contact,
providing critical inputs for growth and development of
the young. Through such bio-behavioral synchrony,
mammalian mothers adapt their physiological systems to
those of the infants and the process facilitates physio-
logical maturation and social adaptation (Fleming,
O’Day & Kraemer, 1999). In humans, parent–infant
synchrony appears in a species-typical form that involves
the coordination of visual, vocal, and affective signals,
and this experience similarly organizes the infant’s
physiology and socialization and supports later devel-
opment (Feldman, 2007). The present findings point to
similarities between humans and other mammals and
suggest that the species-typical form of well-adapted
parenting in humans is similarly supported by the OT
system and is likely to carry a similar organizing impact
on infant growth (Champagne, 2008).
that representational models of attachment and their
built onthe assumption
Table 3 Predicting Affect Synchrony and Interactive Stress
Affect Synchrony Interactive Stress
Bonding to Parents
R2Total = .22, F(6, 103) = 2.94, p < .01; .23, F(6, 63) = 3.11, p < .01.
+p > .10; *p < .05; **p < .01.
Note: Model for Affect Synchrony included both mothers and fathers. Model for Interactive Stress was conducted for mothers only.
Plasma oxytocin was entered in the first step predicting Affect Synchrony, whereas urinary oxytocin was entered in the prediction of Interactive Stress.
758 Ruth Feldman et al.
? 2010 Blackwell Publishing Ltd.
behavioral and physiological underpinnings are formed
early in life through the experience of sensitive parenting,
continue with the individual’s romantic attachment, and
culminate in the capacity to provide adequate parenting
to the next generation (Bowlby, 1969). Cross-fostering
animal studies show that the cross-generation transmis-
sion of maternal behavior rides on mechanisms of early
experience and shapes the organization of brain OT
(Meaney, 2010). The present findings indicate that OT is
related to the entire constellation of attachment in
humans, including the parent’s experience of being cared
for as a child, attachment to romantic partner, and the
ability to provide optimal parenting to the next genera-
tion, as expressed in developmentally adequate preoc-
cupations and worries regarding infant well-being, clear
and coherent representations of the parent–infant
attachment, and the ability to engage in positive, well-
timed synchronous interactions with the child.
Unlike the cross-gender associations of OT and syn-
chrony, the correlations between OT and markers of
relationship distress were specific to women, consistent
with the findings for mammals (Neumann, 2008). The
data indicate that maternal uOT was related to moments
of interactive stress, maternal attachment anxiety, and
stress in the maternal role, in line with theories suggest-
ing that women are more sensitive to relationship distress
and utilize close relationships as a strategy for stress
regulation (Taylor et al., 2000). Possibly, relationship
distress functions to increase OT production through its
impact on HPA functioning (Pedersen, 2004), consistent
with recent findings on the effects of stress on the
expression of magnocellular neurons and their secreted
neurohypophysial peptides in the hypothalamic para-
ventricular nucleus (Herman, Flak & Jankord, 2008). OT
increase during moments of stress may activate a feed-
back loop that up-regulates the woman’s employment of
affiliative processes and social behavior in the service
of well-being, calmness, and physical health (Uvnas-
Interestingly, the associations between the stress
components of bonding and OT were expressed in
urine, whereas the links with the affiliation components
emerged in plasma and saliva. OT plays a complex role
in urination. Like vasopressin, OT functions as an
anti-diuretic hormone via the kidney vasopressin type-
2 receptor (Chou, DiGiovanni, Luther, Lolait &
Knepper, 1995). Moreover, micturition is partially
regulated by neurological pathways sending inputs to
the limbic system, including preoptic regions, the cen-
tral nucleus of the amygdala, bed nucleus of the stria
terminalis, and hypothalamic nuclei, particularly the
PVN where OT is produced (Holstege, 2005). Future
research is required to assess the role of OT in psycho-
physiological processes leading to micturition. The
differential relations of pOT and uOT with markers
of affiliation and stress may also accord with the
bi-phasic theory of OT (Lancel, Kromer & Neumann,
2003), which suggests that when physiological systems
are in a calm state, OT functions as a soporific agent
that reduces central activity and induces calmness,
while under conditions of stress OT acts as a stimulant
and increases social vigilance and active social behav-
It must be emphasized, however, that there are cur-
rently no comprehensive explanations for the specific
associations between OT in urine and indices of
maternal stress. Similarly, the lack of correlations
between OT in saliva and plasma and OT in urine are
not fully understood. One possibility may relate to the
longer time it takes OT to be expressed in urine as
compared to the other peripheral systems. This is the
first study to assess OT in plasma, saliva, and urine
simultaneously and assess
observed behavior and indices of stress and affiliation
research is required to examine the conditions under
which OT levels measured in these three systems
converge or diverge and the differential associations
between the various markers of OT with parenting
behavior and attachment experiences.
A central limitation of the present study is the
peripheral measure of OT, which is unavoidable in
humans. Although the relations between central and
peripheral OT are not fully understood, studies in
animals (Carter et al., 2007) and humans (Strathearn et
al., 2009) as well as theoretical accounts of the func-
tioning of the oxytocinergic system (Ross & Young,
2009) suggest that central and peripheral levels are
coordinated. The consistency between the present find-
ings – which show associations between bonding-related
processes and peripheral OT as measured in various
fractions – and those observed centrally and peripherally
in other mammals provides further evidence for the
utility of assessing peripheral OT. However, much further
research is required to uncover the involvement of OT in
processes of human attachment and understand the
behavioral indicators, physiological correlates, genetic
expressions, brain structures, and meta-representational
models that contribute to the human capacity to form
selective and enduring attachments throughout life.
their relationships with
Research at Dr Feldman’s lab during the study period
was supportedby theIsrael
(#1318⁄08), the US-Israel Bi-National Science Founda-
tion (2005-273), the NARSAD foundation (Independent
Investigator Award 2006, 2008), and the Irving B. Harris
Abidin, R.R. (1983). Parenting stress and the utilization of
pediatric services. Child Health Care, 11, 70–73.
Oxytocin and parent–infant synchrony759
? 2010 Blackwell Publishing Ltd.
Ahern, T.H., & Young, L.J. (2009). The impact of early life
family structure on adult social attachment, alloparental
behavior, andthe neuropeptide
affiliative behaviorsin the
(microtus ochrogaster). Frontiers in Behavioral Neurosci-
ence, 3, 17.
Bowlby, J. (1969). Attachment and loss. New York: Basic Books.
Brennan, K.A., & Shaver, P.R. (1998). Attachment styles and
personality disorders: their connections to each other and
to parental divorce, parental death, and perceptions of
parental caregiving. Journal of Personality Disorders, 66,
Carter, C.S. (2005). Attachment and bonding: A new synthesis.
Cambridge, MA: MIT Press.
Carter, C.S., Boone, E.M., Pournajafi-Nazarloo, H., & Bales,
K.L. (2009). Consequences of early experiences and exposure
to oxytocin and vasopressin are sexually dimorphic. Devel-
opmental Neuroscience, 31, 332–341.
Carter, C.S., Pournajafi-Nazarloo, H., Kramer, K.M., Ziegler,
T.E., White-Traut, R., Bello, D., & Schwertz, D. (2007).
Oxytocin: behavioral associations and potential as a salivary
biomarker. Annals of the New York Academy of Sciences,
Champagne, F.A. (2008). Epigenetic mechanisms and the
transgenerational effects of maternal care. Frontiers in Neu-
roendocrinology, 29, 386–397.
Champagne, D.L., Bagot, R.C., van Hasselt, F., Ramakers, G.,
Meaney, M.J., de Kloet, E.R., Joels, M., & Krugers, H.
(2008). Maternal care and hippocampal plasticity: evidence
for experience-dependent structural plasticity, altered syn-
aptic functioning, and differential responsiveness to gluco-
corticoids and stress. Journal of Neuroscience, 28, 6037–6045.
Champagne, F.A., & Meaney, M.J. (2007). Transgenerational
effects of social environment on variations in maternal care
and behavioral response to novelty. Behavioral Neuroscience,
121 (6), 1353–1363.
Chou, C.L., DiGiovanni, S.R., Luther, A., Lolait, S.J., &
Knepper, M.A. (1995). Oxytocin as an antidiuretic hormone.
II. Role of V2 vasopressin receptor. American Journal of
Physiology, 269, F78–F85.
Costa, B., Pini, S., Martini, C., Abelli, M., Gabelloni, P.,
Ciampi, O., Muti, M., Gesi, C., Lari, L., Cardini, A., Mucci,
A., Bucci, P., Lucacchini, A., & Cassano, G.B. (2009).
Mutation analysis of oxytocin gene in individuals with adult
separation anxiety. Psychiatry Research, 168, 87–93.
Febo, M., Shields, J., Ferris, C.F., & King, J.A (2009). Oxy-
tocin modulates unconditioned fear response in lactating
dams: an fMRI study. Brain Research, 1302, 183–193.
Feldman, R. (2003). Infant–mother and infant–father syn-
chrony: the coregulation of positive arousal. Infant Mental
Health Journal, 24, 1–23.
Feldman, R. (2007). Parent–infant synchrony and the con-
struction of shared timing; physiological precursors, devel-
opmental outcomes, and risk conditions. Journal of Child
Psychology and Psychiatry, 48, 329–354.
Feldman, R. (2010). Parent–infant synchrony: a bio-behavioral
model of mutual influences in the formation of social affili-
ation. Monographs of the Society for Research in Child
Feldman, R., & Eidelman, A.I. (2004). Parent–infant syn-
chrony and the social-emotional development of triplets.
Developmental Psychology, 40 (6), 1133–1147.
Feldman, R., & Eidelman, A.I. (2007). 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. Developmental Psychology, 49, 290–302.
Feldman, R., Gordon, I., Schneiderman, I., Weisman, O, &
Zagoory-Sharon, O. (2010). Natural variations in maternal
and paternal care are associated with systematic changes in
oxytocin following parent–infant contact. Psychoneuroendo-
crinology, 35, 1133–1141.
Feldman, R., Weller, A., Leckman, J.F., Kuint, J., & Eidelman,
A.I. (1999). The nature of the mother’s tie to her infant:
maternal bonding under conditions of proximity, separation,
and potential loss. Journal of Child Psychology and Psychia-
try, 40, 929–939.
Feldman, R., Weller, A., Zagoory-Sharon, O., & Levine, A.
(2007). Evidence for a neuroendocrinological foundation of
human affiliation: plasma oxytocin levels across pregnancy
and the postpartum period predict mother–infant bonding.
Psychological Science, 18, 965–970.
Fleming, A.S., O’Day, D.H., & Kraemer, G.W. (1999).
Neurobiology of mother–infant interaction: experience and
central nervous system plasticity across development and
generations. Neuroscience and Biobehavioral Review, 23, 673–
Forsyth, I.A., & Neville, M.C. (2009). Introduction: the myo-
epithelial cell and milk letdown; entrance to the multifunc-
tional role of oxytocin. Journal of Mammary Gland Biology
and Neoplasia, 14, 221–222.
Francis, D.D., Champagne, F.C., & Meaney, M.J. (2000).
Variations in maternal behaviour are associated with differ-
ences in oxytocin receptor levels in the rat. Journal of Neu-
roendocrinology, 12, 1145–1148.
Gimpl, G., & Fahrenholz, F. (2001). The oxytocin receptor
system: structure, function, and regulation. Physiological
Revues, 81, 629–683.
Gonzaga, G.C., Turner, R.A., Keltner, D., Campos, B., &
Altemus, M. (2006). Romantic love and sexual desire in close
relationships. Emotion, 6, 163–179.
Gordon, I., Zagoory-Sharon, O., Schneiderman, I., Leckman,
J.F., Weller, A., & Feldman, R. (2008). Oxytocin and cortisol
in romantically unattached young adults: associations with
bonding and psychological distress. Psychophysiology, 45,
Gordon, I., Zagoory, O., Leckman, J.F., & Feldman, R. (2010).
Oxytocin and the development of parenting in humans.
Biological Psychiatry, 68, 377–382.
Heinrichs, M., & Gaab, J. (2007). Neuroendocrine mechanisms
of stress and social interaction: implications for mental dis-
orders. Current Opinion in Psychiatry, 20, 158–162.
Herman, J.P., Flak, J., & Jankord, R. (2008). Chronic stress
plasticity in the hypothalamic paraventricular nucleus. Pro-
gress in Brain Research, 170, 353–364.
Holstege, G. (2005). Micturition and the soul. Journal of
Comparative Neurology, 493, 15–20.
Holt-Lunstad, J., Birmingham, W.A., & Light, K.C. (2008).
Influence of a ‘warm touch’ support enhancement interven-
tion among married couples on ambulatory blood pressure,
oxytocin, alpha amylase, and cortisol. Psychosomatic Medi-
cine, 70, 976–985.
Jonas, K., Johansson, L.M., Nissen, E., Ejdeback, M., Ransjo-
Arvidson, A.B., & Uvnas-Moberg, K. (2009). Effects of
intrapartum oxytocin administration and epidural analgesia
760Ruth Feldman et al.
? 2010 Blackwell Publishing Ltd.
on the concentration of plasma oxytocin and prolactin, in Download full-text
response to suckling during the second day postpartum.
Breastfeeding Medicine, 4, 71–82.
Kendrick, K.M., Keverne, E.B., & Baldwin, B.A. (1987).
Intracerebroventricular oxytocin stimulates maternal behav-
iour in the sheep. Neuroendocrinology, 46 (1), 56–61.
Keverne, E.B., & Kendrick, K.M. (1992). Oxytocin facilitation
of maternal behavior in sheep. Annals of the New York
Academy of Sciences, 652, 83–101.
Lancel, M., Kromer, S., & Neumann, I.D. (2003). Intracerebral
oxytocin modulates sleep-wake behaviour in male rats. Reg-
ulatory Peptides, 114, 145–152.
N., & Mayes, L.C. (2004). Primary parental preoccupation:
circuits,genes,andthe crucialrole oftheenvironment.Journal
of Neural Transmission, 111 (7), 753–771.
Leckman, J.F., Mayes, L.C., Feldman, R., Evans, D., King,
R.A., & Cohen, D. (1999). Early parental preoccupations
and behaviors and their possible relationship to the symp-
toms of obsessive-compulsive disorder. Acta Psychiatrica
Scandinavica (Supplementum), 100 (396), 1–26.
Lee, H.J., Macbeth, A.H., Pagani, J.H., & Young, W.S. 3rd
(2009). Oxytocin: the great facilitator of life. Progress in
Neurobiology, 88, 127–151.
Maestripieri, D., Hoffman, C.L., Anderson, G.M., Carter,
C.S., & Higley, J.D. (2009). Mother–infant interactions in
free-ranging rhesus macaques: relationships between physi-
ological and behavioral variables. Physiology and Behavior, 96
Marazziti, D., Dell’Osso, B., Baroni, S., Mungai, F., Catena,
M., Rucci, P., Albanese, F., Giannaccini, G., Betti, L.,
Fabbrini, L., Italiani, P., Del Debbio, A., Lucacchini, A., &
Dell’Osso, L. (2006). A relationship between oxytocin and
anxiety of romantic attachment. Clinical Practice and Epi-
demiology in Mental Health, 2, 28.
Matthiesen, A.S., Ransjo-Arvidson, A.B., Nissen, E., & Uvnas-
Moberg, K. (2001). Postpartum maternal oxytocin release by
newborns: effects of infant hand massage and sucking. Birth,
Meaney, M.J. (2010). Epigenetics and the biological definition
of gene · environment interactions. Child Development, 81,
Nelson, E.E., & Panksepp, J. (1998). Brain substrates of
infant–mother attachment: contributions of opioids, oxyto-
cin, and norepinephrine. Neuroscience and Biobehavioral
Reviews, 22, 437–452.
Neumann, I.D. (2008). Brain oxytocin: a key regulator of
emotional and social behaviours in both females and males.
Journal of Neuroendocrinology, 20, 858–865.
Parker, G., Tupling, H., & Brown, LB. (1979). A parental
bonding instrument. British Journal of Medical Psychology,
Pedersen, C.A. (2004). Biological aspects of social bonding and
the roots of human violence. Annals of the New York Acad-
emy of Sciences, 1036, 106–127.
Pedersen, C.A., & Prange, A.J. Jr. (1979). Induction of
maternal behavior in virgin rats after intracerebroventricular
administration of oxytocin. Proceedings of the National
Academy of Sciences, USA, 76 (12), 6661–6665.
Ross, H.E., Cole, C.D., Smith, Y., Neumann, I.D., Landgraf,
R., Murphy, A.Z., & Young, L.J. (2009). Characterization of
the oxytocin system regulating affiliative behavior in female
prairie voles. Neuroscience, 162, 892–903.
Ross, H.E., & Young, L. (2009). Oxytocin and the neural
behavior. Frontiers in Endocrinology, 30, 534–547.
Seltzer, L.J., Ziegler, T.E., & Pollak, S.D. (2010). Social
vocalizations can release oxytocin in humans. Proceedings of
the Royal Society B, Biological Sciences, 277 (1694), 2661–
Slattery, D.A., & Neumann, I.D. (2010). Chronic icv oxytocin
attenuates the pathological high anxiety state of selectively
bred Wistar rats. Neuropharmacology, 58, 56–61.
Strathearn, L., Fonagy, P., Amico, J., & Montague, P.R.
(2009). Adult attachment predicts maternal brain and oxy-
tocin response to infant cues. Neuropsychopharmacology, 34,
Taylor, S.E., Klein, L.C., Lewis, B.P., Gruenewald, T.L.,
Gurung, R.A., & Updegraff, J.A. (2000). Biobehavioral
responses to stress in females: tend-and-befriend, not fight-
or-flight. Psychological Review, 107, 411–429.
Taylor, S.E., Saphire-Bernstein, S., & Seeman, T.E. (2010). Are
plasma oxytocin in women and plasma vasopressin in men
biomarkers of distressed pair-bond relationships? Psycho-
logical Science, 2, 3–7.
Tops, M., van Peer, J.M., Korf, J., Wijers, A.A., & Tucker,
D.M. (2007). Anxiety, cortisol, and attachment predict
plasma oxytocin. Psychophysiology, 44, 444–449.
Tronick, E.Z. (1989). Emotions and emotional communication
in infants. American Psychologist, 44, 112–119.
Uvnas-Moberg, K. (1998). Oxytocin may mediate the benefits
of positive social interaction and emotions. Psychoneuroen-
docrinology, 23, 819–835.
Waldherr, M., Nyuyki, K., Maloumby, R., Bosch, O.J., &
Neumann, I.D. (2010). Attenuation of the neuronal stress
responsiveness and corticotrophin releasing hormone syn-
thesis after sexual activity in male rats. Hormones and
Behavior, 57, 222–229.
White-Traut, R., Watanabe, K., Pournajafi-Nazarloo, H.,
Schwertz, D., Bell, A., & Carter, C.S. (2009). Detection of
salivary oxytocin levels in lactating women. Developmental
Psychobiology, 51, 367–373.
Winslow, J.T., Hearn, E.F., Ferguson, J., Young, L.J., Matzuk,
M.M., & Insel, T.R. (2000). Infant vocalization, adult
aggression, and fear behavior of an oxytocin null mutant
mouse. Hormones and Behavior, 37 (2), 145–155.
Wynne-Edwards, K.E., & Timonin, M.E. (2007). Paternal care
in rodents: weakening support for hormonal regulation of the
transition to behavioral fatherhood in rodent animal models
of biparental care. Hormones and Behavior, 52, 114–121.
Yoshida, M., Takayanagi, Y., Inoue, K., Kimura, T., Young,
L.J., Onaka, T., & Nishimori, K. (2009). Evidence that
oxytocin exerts anxiolytic effects via oxytocin receptor
expressed in serotonergic neurons in mice. Journal of Neu-
roscience, 29, 2259–2271.
Ziegler, T.E. (2000). Hormones associated with non-maternal
infant care: a review of mammalian and avian studies. Folia
Primatologica (Basel), 71, 6–21.
Received: 17 April 2010
Accepted: 10 September 2010
Oxytocin and parent–infant synchrony 761
? 2010 Blackwell Publishing Ltd.