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Oxytocin and social affiliation in humans
Department of Psychology and the Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan 52900, Israel
a b s t r a c ta r t i c l ei n f o
Received 7 October 2011
Revised 6 January 2012
Accepted 7 January 2012
Available online 20 January 2012
A conceptual model detailing the process of bio-behavioral synchrony between the online physiological and
behavioral responses of attachment partners during social contact is presented as a theoretical and empirical
framework for the study of affiliative bonds. Guided by an ethological behavior-based approach, we suggest
that micro-level social behaviors in the gaze, vocal, affective, and touch modalities are dynamically integrated
with online physiological processes and hormonal response to create dyad-specific affiliations. Studies across
multiple attachments throughout life are presented and demonstrate that the extended oxytocin (OT) sys-
tem provides the neurohormonal substrate for parental, romantic, and filial attachment in humans; that
the three prototypes of affiliation are expressed in similar constellations of social behavior; and that OT is
stable over time within individuals, is mutually-influencing among partners, and that mechanisms of
cross-generation and inter-couple transmission relate to coordinated social behavior. Research showing
links between peripheral and genetic markers of OT with concurrent parenting and memories of parental
care; between administration of OT to parent and infant's physiological readiness for social engagement;
and between neuropeptides and the online synchrony of maternal and paternal brain response in social-
cognitive and empathy networks support the hypothesis that human attachment develops within the matrix
of biological attunement and close behavioral synchrony. The findings have conceptual implications for the
study of inter-subjectivity as well as translational implications for the treatment of social disorders originat-
ing in early childhood, such as autism spectrum disorders, or those associated with disruptions to early
bonding, such as postpartum depression or child abuse and neglect.
This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.
© 2012 Elsevier Inc. All rights reserved.
Affiliative bonds: a conceptual model. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Behavior-based perspective on affiliation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Bio-behavioral synchrony . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Oxytocin, affiliation, and biobehavioral synchrony . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The role of oxytocin in affiliative bonds. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
OT and the parent–infant bond . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
OT and mothering . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
OT and fathering . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The cross generation transmission of OT in humans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
OT and mothering in atypical development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
OT and romantic attachment: pair bonding in humans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
OT and filial attachment; our best friends . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions and implications. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conceptual implications. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Translational implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Hormones and Behavior 61 (2012) 380–391
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“The roots of parenthood lie in the child's relations to his own parents
in his earliest years. The love which a mother has for her children is a
reflection of the love which she received when she was a little girl. The
love which a father has for his children is a reflection of the love
which he received when he was a little boy. It is in childhood that
we learn to love”
John Bowlby, The roots of parenthood, 1953 (p. 15).
Affiliative bonds: a conceptual model
Behavior-based perspective on affiliation
Affiliation, from the Medieval Latin word Affiliatus – to adopt as a
son – is defined as “to bring or receive into close connection”
(Merriam-Webster Medical Dictionary, 2002) and appears to contain
two elements; it refers to a close interpersonal bond, such as that be-
tween a parent and child, and it involves a process or action needed
for that bond to take place. During the mid 20th century, authors
such as Bowlby (1958), Harlow (1958), and Spitz (1946) began to
draw attention to the primary role of love as a central motivating
force of developmental progress and as a critical ingredient in the
survival, safety, and well-being of the young. Affiliative bonds, de-
fined as selective and enduring attachments, were conceptualized
as providing the foundation for the infant's capacity to function
competently within the eco-social niche, grow to form intimate
bonds with non-kin members of society, and eventually nurture
the next generation. This paradigm shift, which transformed “love”
from the realm of the literary to the domain of hard core science,
drew on several lines of concurrent inquiry in biology, philosophy,
and the social sciences. These new fields not only introduced novel
ideas but also advocated new methodologies as best practice for sci-
entific progress. Most important were the works of the early Ethol-
ogists (Lorenz, 1950; Timbergen, 1963) who underscored bonding
as the central process supporting mammalian adaptation, highlight-
ed behavior as the lens through which science should approach the
study of social maturation, and suggested that the meticulous docu-
mentation of behaviors that emerge or intensify during periods of
bond formation are necessary preconditions for any theory of
human nature. By focusing on concrete bonding-related behaviors,
these researchers advocated a bottom-up perspective of human de-
velopment that is behavior-based, thus opposing the two central
perspectives of the time: psychoanalysis, which outlined a theory-
based rather than behavior-based viewpoint of human develop-
ment, and Skinnerian behaviorism, which focused on the behavior
of individuals, not of relational units. This new ethological-based
approach altered the conceptualization of human affiliation in
three key ways. First, it suggested that bonding is expressed through
a set of species-specific stereotypic caregiving (and care-receiving)
behaviors that appear immediately after birth and provide the
foundation for the infant's neurobehavioral maturation, thereby ad-
vocating a critical-period viewpoint on attachment. Second, it indi-
cated that bond formation is supported by unique neurohormonal
systems and brain circuits, hence linking specific biology to specific
behavior in the formation of affiliative bonds. Third, it underscored a
lifetime perspective suggesting that (a) the three prototypes of affil-
iation in mammals – parental, pair, and filial – share underlying
physiological mechanisms and overt behavioral expressions, and
(b) bio-behavioral mechanisms formed in early infancy shape the
way individuals function within their various attachments through-
Several large-scales empirical programs and countless smaller
studies over the past half-century lend support to the propositions
forwarded by the attachment-ethological perspective and specified
the biological basis of affiliation. Long-term human studies following
individuals from infancy to adulthood demonstrated that sensitive
caregiving in infancy predicted better adult adaptation and more se-
cure romantic relationships (Sroufe, 2005). The empirical work of
Hofer, spanning 40 years of careful experimentations, teased apart
the provisions embedded in the maternal physical proximity in
mammals and demonstrated that the mother's physical presence in-
cludes a set of “bio-behavioral regulators” such as maternal touch,
odor, movements, or body rhythms, each functions to regulate a spe-
cific physiological system in the pup, including autonomic function-
ing, thermoregulation, or attention (Hofer, 1995). Finally, the work
of Meaney (2001; 2010; Zhang and Meaney, 2010) specified the re-
lations between Oxytocin (OT) – a nine amino-acid neuropeptide
synthesized in the hypothalamus – and patterns of maternal care.
This research program showed that the amount of maternal caregiv-
ing, particularly the licking-and-grooming (LG) behaviors of rat
dams, shaped the offspring's stress response and OT-mediated affili-
ation systems. Moreover, the generational transmission of OT and
parental behavior was mediated by behavioral, rather than genetic
mechanisms and was related to the amount of touch-and-contact
the mother received as an infant (Champagne et al., 2001;
Over the past decade, research at my lab followed these lines of in-
quiry in humans in an attempt to describe the role of OT in human so-
cial adaptation and the formation of affiliative bonds. We examined
the links between OT and parenting behavior; the relations between
brain structures implicated in parental care and their associations
with OT; the cross-generation transmission of OT; the relations be-
tween peripheral indices of OT with allelic variations on the Oxytocin
receptor (OXTR) and CD38 genes; and the consistency in OT-related
processes and relational behavior among the three prototypical
forms of mammalian affiliations – parental, pair, and filial – which
in humans refer to attachments with parents, romantic partners,
and best friends. In several longitudinal studies, we assessed the com-
bined effects of parenting and OT on children's social adaptation
across childhood and up to adolescence in typical as well as atypical
developmental conditions associated with disruptions to bonding
processes, such as maternal post partum depression, preterm birth,
and war-related PTSD. Following evolutionary models, we define so-
cial adaptation as the ability to function competently with non-kin
members of society at both the level of global adaptation to the eco-
social niche and the skills required to form and maintain intimate
bonds with non-kin (Clutton-Brock, 1991; Davis and Daly, 1997;
The work presented here in guided by our conceptual model on
bio-behavioral synchrony, which utilizes the concept of synchrony
and its emphasis on the temporal concordance of biological and social
processes as a useful framework for the study of affiliative bonds
(Feldman, 2007a, 2007b, 2007c, 2007d, in pressa, in pressb). Synchro-
ny is a concept coined by the first researchers on parenting in social
animals, beginning with research on the social insects nearly a cen-
tury ago (Wheeler, 1928). Prompted by the question of what enables
a group of ants to jointly carry a grain of wheat, or broadly speaking,
collaborate to achieve a social goal, researchers described the process
of bio-behavioral synchrony. Among members of a social group, such
as flocks of birds synchronizing their journey toward warm climates
or fish moving in perfect synchronous cycles to ward off a shark,
there is a temporal concordance between the behavioral patterns of
various members, between their online physiological processes,
such as neural firing or hormonal release, and between the physiolo-
gy of one member and the behavior of the other. Such synchronous
process creates a time-locked ongoing relationship between the
physiology and behavior of group members that is critical for the sur-
vival of the group as well as for the individual's adaptation to the
R. Feldman / Hormones and Behavior 61 (2012) 380–391
Author's personal copy
social milieu. Biobehavioral synchrony, therefore, is the process by
which organisms become members of a social group and function col-
laboratively within it. The evolution of mammals implied that indi-
vidual members of the eco-social niche are no longer initiated
directly into large social groups but are ushered into the social milieu
through intimate one-on-one reciprocal relationships with the care-
giver. Hence, mammalian young receive their training for social reci-
procity not within the large group but in the context of the nursing
dyad by means of finely-tuned bio-behavioral adaptations between
mother and child (Rosenblatt, 1965; Schneirla, 1946). Across mam-
malian species, dyad-specific maternal-infant bonds are built on
repeatedly-experienced patterns of sensori, motor, and behavioral
cues in each partner. Over time and repeated experience these dis-
crete synchronized bio-behavioral events coordinate to form the
unique bond that characterize the rhythms, content, focus, and pace
of the specific attachment relationship (Feldman, 2007a, 2012;
Fleming et al., 1999). Studies in mammals and emerging data in
humans suggest that the formation of these dyad-specific bio-
behavioral bonds is underpinned by the extended OT system (Gimpl
and Fahrenholz, 2001; Insel, 1997; Ross and Young, 2009). Yet, due
to the fact that both the distribution of OT receptors in the brain
and the links between maternal behaviors and OT expression show
substantial between-species variations (Insel, 2010; Ross et al.,
2009), it is critical that the specific associations between OT and pro-
cesses of social bonding should be studied in humans, notwithstand-
ing limitations of human neuroendocrine and molecular research.
Like other mammals, human mothers and infants engage in the
species-typical repertoire of postpartum behaviors, which includes
gaze at the infant's face or body, “motherese” high-pitched vocaliza-
tions, expression of positive affect, and affectionate touch, a behavior
akin to the licking-and-grooming of other mammals (Feldman and
Eidelman, 2007). Human mothers express these maternal behaviors
already in the first postpartum day, but, moreover, mothers provide
approximately 70% of their behaviors during the 7% of the time new-
borns spend in alert-scanning state, creating temporal contingencies
between infant state and maternal social behavior already at the
first post-birth hours (Feldman and Eidelman, 2007; Silberstein
et al., 2009). These social contingencies are supported by physiologi-
cal periodicities maturing in the fetus during the 3rd trimester of
pregnancy, including the biological clock and cardiac pacemaker
(Feldman, 2006; Groome et al., 1999; Mirmiran and Lunshof, 1996).
Thus, as soon the human infant is born, he or she can experience a
temporal match between their own state and the response of the
social environment as mediated by the mother. Such early temporal
concordance between maternal and infant readiness for social
engagement is a critical human addition to the physiological provi-
sions embedded in the maternal proximity in other mammals
(Hofer, 1995) or the expression of maternal behavior in rodents
(Meaney, 2010), and lays the foundation for the development of
human-specific social, emotional,
(Feldman, 2007a; Feldman and Eidelman, 2007; Feldman et al.,
2004). At approximately 3 months, infants enter the social world as
active partners and begin to engage in synchronous exchanges with
their caregivers that contain coordinated sequences of gaze patterns,
co-vocalizations, mutual expressions of positive affect, and loving
touch (Feldman, 2003, 3007a). Synchrony experienced during the
critical period between 3 and 9 months was found to promote chil-
dren's self-regulation (Feldman et al., 1999), symbol use (Feldman,
2007b), the capacity for empathy across childhood and up to adoles-
cence (Feldman, 2007c), as well as more optimal social adaptation
and lower depression in adolescence (Feldman, 2010). These longitu-
dinal findings support the sensitive period perspective suggested by
Ethological models in the effects of early synchrony on children's
neurobehavioral and social-emotional growth. From the end of the
first year of life and on, with the emergence of children's symbolic
competencies, interactions between close partners grow to contain
and cognitive competencies
two parallel lines: a non-verbal line of synchrony between the part-
ners' gaze, affective expression, vocal quality, body orientation,
movements, and proximity position, and a verbal line of synchrony
between levels of communicative intimacy, for instance between
the degree of self-disclosure between close friends or romantic part-
ners (Feldman, 2007d). Synchrony, therefore, describes a critical
component of close relationships that builds on familiarity with the
partner's style, manner, non-verbal patterns, personal rhythms, be-
havioral preferences, and pace of intimacy.
In this context, it is important to note that the construct of syn-
chrony describes only the temporal concordance between processes
that occur simultaneously or sequentially and postulates no heuristic
system of symbols or a-prior assumptions. As such, synchrony pro-
vides an optimal framework for a bottom-up model that centers on
discrete building blocks as they cohere into a theoretical model. Re-
cent perspectives in neuroscience have underscored synchrony as
the mechanism which underlies consciousness and supports the
brain's capacity to form a unitary event out of the simultaneous activ-
ity of discrete brain regions (Edelman, 2004; 2006; Damasio, 2003),
as stated by Llineas (2001, page 120): “timeness is consciousness”.
This transition from mechanisms of a “central organizer” to those of
temporal synchrony highlight the importance of a bottom-up per-
spective and parallels the shift advocated by the early Ethologists.
As such, the following review will focus specifically on studies that
demonstrate biobehavioral synchrony in the relations of OT and
matched dyadic behavior within attachment relationships: within
each partner, among attachment partners, and between OT in one
partner and social behavior in the other.
Oxytocin, affiliation, and biobehavioral synchrony
The exponential increase in empirical research on OT and social
functioning in recent years raises the question as to what are the
mechanisms mediating the effects of OT on human affiliation, apart
from the obvious involvement of OT in the birth of the “mammalian
dyad” by initiating uterine contraction and milk letdown, functions
that were considered for decades as the sole tasks of this neuropep-
tide (Gimpl and Fahrenholz, 2001; Insel, 2010; Young, 2009). OT is
a nonapeptide synthesized in the supraoptic (SON) and paraventricu-
lar nuclei (PVN) of the hypothalamus, although the spinal cord, bed
nucleus of the stria terminalis (BNST) and the anterior commissural
nucleus also serve as central sources of OT (Carter, 1998). Brain re-
gions receiving OT projections include the medial preoptic area
(MPOA), the BNST, the lateral septum, the nucleus accumbens
(NAcc), the amgydala, and the hippocampus as well as ventrally,
the ventral tegmental area, solitary tract nuclei, and the spinal cord
(Ross and Young, 2009). In addition, neurons in the PVN and SON re-
lease OT from their dendrite into the cerebral spinal fluid (Veening
et al., 2010) and OT is also released at peripheral cites, including the
heart, thymus, gastrointestinal tract, uterus, placenta, amnion, corpus
luteum, and testes (Gordon et al., 2011), underscoring the widely-
distributed and dynamic nature of OT production in body and brain.
The OT system is reciprocally engaged with the hypothalamic–
pituitary–adrenal axis (HPA) that mediates the stress response, and
neuroanatomical evidence suggests that the HPA and OT systems are
mutually regulated (Dabrowska et al., 2011). OT has shown to have
significant anxiolytic and anti-stress effects (Neumann, 2008;
Neumann and Landgraf, 2008), which are central for the initiation of
breastfeeding and the formation of maternal-infant bonding (Uvnas-
In addition to anti-stress effects that induce a feeling of safety and
support the approach behaviors required for bonding, OT plays a key
role in the motivation to bond through its connectivity with the dopa-
mingeric reward system. OT neurons are reciprocally connected with
mesolimbic dopaminergic neurons and this interconnection serves
an important role in both romantic and parental attachment by
R. Feldman / Hormones and Behavior 61 (2012) 380–391
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initiating sexual behavior and forming sexual preferences (Melis and
Argiolas, 2011) and by labeling the infant with an intuitive reinforce-
ment and increasing the incentive value of the infant for its mother
(Cardinal et al., 2002; Lee et al., 2000). Bos et al. (2011) suggest that
gonadal steroids and neuropeptides jointly influence social bonding
by increasing OT-dopamine interactions. In contexts perceived as
safe, Estrogen and OT increase parasympathetic efference and inhibit
amygdala output to the brainstem, leading to increased prefrontal
activity and OT-dopamine interactions that enhance the motivation
to bond. Recent data from our lab show that during the early stages
of romantic attachment, levels of plasma OT and testosterone are
inter-related and are associated with respiratory sinus arrhythmia
(RSA), an index of parasympathetic influences over heart rate
variability. Such hormonal-autonomic interactions were found to pre-
dict observed social reciprocity between new lovers, expressed in
mutual gazing, matched affect, positive arousal, and affectionate
Along the affiliation-supporting mechanisms of stress reduction
and incentive motivation, recent findings linking OT to the immune
system suggest that OT may enhance social affiliation through the
sense of well-being associated with close bonds and the role of OT
in promoting health (Hansenne, 2005; Macciò et al., 2010). For in-
stance, administration of OT was found to increase the expression of
both CD25 and CD95, proteins that mediate immune signaling
(Gordon et al., 2011; Macciò et al., 2010). Similarly, Jin et al. (2007)
showed that CD38, a transmembrane multi-functional molecule that
combines enzymatic and receptor properties and is implicated in
various physiological processes, including proliferation, differentia-
tion, and migration, triggers OT release from soma and axon terminals
of hypothalamic neurons through the mobilization of calcium.
maternal behavior in females, and social amnesia in males and similar
links have been found in humans (see below). Preliminary data from
our lab support the associations between OT and immune function-
ing. During periods of both parental and romantic bonding, we
found an increase in plasma IL-6 and this increase was associated
with the rise in OT during these periods.
Finally, OT is among the systems most open to environmental
influences, mediates the epigenetic effects of maternal behavior
(Szyf et al., 2008), and its generational transmission operates though
patterns of maternal care (Francis et al., 2002). Naturally-occurring
variations in maternal behavior, particularly maternal licking-and-
grooming (LG), induce changes in the offspring's gene expression
through a process of methylation, creating stable non-genomic
alterations in DNA expression that are shaped by the affiliative com-
ponents of the environment. These early maternal effects appear to
involve up regulation of hypothalamic OT receptors and infants
reared by high LG dams show elevated estrogene-primed OT recep-
tors in the MPOA, which continue to be sensitive to social influences
in the post-weaning period as seen in experiments involving both
social isolation and social enrichment (Champagne, 2011). Maternal
LG and the increased ER alpha expression in the MPOA increase
OT receptor binding and activate the mesolimbic dopamine system
and the release of dopamine in the NAcc (Cameron et al., 1992;
Champagne et al., 2004). On the other hand, low LG mothering
leads to elevation of cytosine methylation of ER associated with de-
creased ER alpha expression (Champagne et al., 2006). Maternal LG
similarly induces epigenetic effects on stress reactivity by increas-
ing glucocorticoid receptor expression within the hippocampus
(Weaver, et al., 2004; Zhang and Meaney, 2010), underscoring the
combined effects of OT and maternal behavior in shaping the off-
spring's long-term stress and reward pathways. Although very little
research examined methylation of the Oxytocin receptor gene
(OXTR) in humans, recent work points to the associations between
DNA methylation on the OXTR rs2254298 SNP and autism spectrum
disorder (ASD) (Gregory et al., 2009). Importantly, we found that
lower plasmaOT, disrupted
the GG risk alleles on the OXTR rs2254298 is associated with dimin-
ished parenting behavior (see below), highlighting the links between
OT, epigenetic effects, parenting behavior, and neuropsychiatric dis-
orders of early social dysfunctions.
Although much further research is required to chart the molecu-
lar, chemical, and neurological aspects of OT, it is clear that the OT
system is among the most widely-distributed throughout body and
brain and that OT is dynamically engaged with homeostatic, appeti-
tive, reparatory, stress reduction, salience and reward, and perceptual
systems in processes that involve ongoing transactions between the
organism and its environment (Bos et al., 2011; Landgraf and
Neumann, 2004; Veening, et al., 2010; Zhang and Meaney, 2010).
Such widespread connectivity forms a multi-dimensional system
that integrates the internal milieu in order to orient the organism to
the social world. Indeed, human studies demonstrate that intranasal
OT administration increases the salience of social cues and improves
the capacity to read subtle non-verbal signals through which individ-
uals understand the intentions and behaviors of social partners (Bartz
et al., 2011). We suggest that such overarching behavior- and
environment-sensitive system provides the neurobiological substrate
for the process of bio-behavioral synchrony which binds members of a
social unit into a unified time-locked event and affords ongoing phys-
iological and behavioral support for the formation of finely-tuned
The role of oxytocin in affiliative bonds
OT and the parent–infant bond
OT and mothering
The mother-infant bond, with its intimacy of contact and dyadic
unity, is not only part of our evolutionarily-based biology but is a cen-
tral component of the human cultural heritage. Throughout human
history and across cultural communities, images of maternal-infant
proximity – in sculptures, drawings, carvings, and ink paints – are
deeply rooted in our collective unconscious and serve as the primary
symbol for the human capacity to love. The behavioral building blocks
of maternal affection – gaze, touch, voice, and affect – serve as the
basic channels for the expression of love that underpin any form of
human intimacy (Feldman, 2011a).
Much research has implicated OT in the expression of maternal
behavior across a variety of species. OT-mediated maternal behaviors
include the licking-and-grooming and arched-back nursing of rat
dams (Francis et al., 2002), the sheep's olfactory-based recognition
of her ewe (Kendrick et al., 1997), and the grooming and contact of
Rhesus Macaques (Maestripieri, et al., 2009), as tested using periph-
eral measures, brain neurochemistry, OT knockout mice, and epige-
netics (Szyf et al., 2008; Zhang and Meaney, 2010). Much less
research examined the role of OT in human mothering, and such as-
sessment is complicated by the inability to directly test OT at the
brain neurochemical level and the need to rely on peripheral mea-
sures that are considered as proxies of brain activity (Rollins et al.,
2010). To date, research on the role of OT in human parenting has re-
lied on three methodologies: peripheral assessments of OT in plasma,
saliva, urine, and CSF; a molecular genetic approach assessing varia-
tions in the OXTR in relation to parenting; and intranasal administra-
tion of OT to parents.
In the first study to evaluate OT and the development of maternal
behavior in humans, we assessed maternal plasma OT and Cortisol
(CT), a biomarker of the HPA-axis stress response, repeatedly from
the first trimester of pregnancy and up to the first postpartum
month. Postpartum mothers were observed interacting with their
infants and were interviewed regarding their mothering-related
thoughts and behaviors. As compared to single women not involved
in a romantic relationship, plasma OT levels in pregnant and parturi-
ent women were significantly higher, pointing to increased activity of
R. Feldman / Hormones and Behavior 61 (2012) 380–391
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the OT system during periods of bond formation (Gordon et al., 2008).
OT levels were highly stable among individuals and women showing
higher OT in early pregnancy also exhibited higher levels in late preg-
nancy and the postpartum. Finally, maternal OT levels in the first
trimester predicted the amount of maternal postpartum behavior, in-
cluding gaze, positive affect, “motherese” vocalizations, and affection-
ate touch, suggesting that OT across gestation functions to prime
mothers for the expression of maternal behavior, consistent with
the effects described in other mammals (Nelson and Panksepp,
1998). OT and CT were unrelated at each assessment but each charted
an independent path to the prediction of maternal behavior, with
higher OT associated with increased and higher CT with reduced ma-
ternal post-partum behavior (Feldman et al., 2007). Furthermore,
maternal bonding to the fetus during the third trimester was pre-
dicted by the increase in plasma OT from the 1st to the 3rd trimester,
indicating dynamic associations between OT and the evolving
maternal-infant bond (Levine et al., 2007).
In addition to research directly assessing OT in mothers, two
studies addressed the relations between breastfeeding, a proxy for
OT production, with patterns of maternal care, brain activations, and
infant outcome. In the first, we observed mothers of premature in-
fants who expressed minimal, medium, and significant amounts of
breastmilk in mother-infant interaction prior to hospital discharge
and followed the infant's neuromaturation and cognitive develop-
ment. Mothers who expressed more than 75% of the infant's nutrition
exhibited more maternal postpartum behavior, particularly affection-
ate touch, and their infants showed better neuromaturation and cog-
nitive growth at six months (Feldman and Eidelman, 2003). In an
fMRI study, breastfeeding and formula feeding mothers were scanned
in the postpartum and were observed interacting with their infants
at 4 months. While listening to their own-infant cry, breastfeeding
mothers showed greater activations in areas described in human
and animal studies to play a key role in the expression of parenting,
including the amygdale, striatum, superior frontal gyrus, and insula
(Barrett and Fleming, 2011; Swain et al., 2007). Greater amygdala
activations were correlated with higher observed maternal sensi-
tivity, suggesting that the increase in brain activations triggered by
breastfeeding may prepare for the expression of coordinated parent-
ing at the stage when infants enter the social world (Kim et al., 2011).
Animal studies of maternal behavior have implicated OT-rich
brain areas in the expression of maternal behavior. In particular,
the NAcc, part of the mesolimbic dopaminergic reward circuit that
receives OT projections, provides motivational drive to maternal
behavior (Cardinal et al., 2002; Lee et al., 2000). Lesions and DA ma-
nipulations studies demonstrated that the NAcc is critical for
maternal motivation to nest and retrieve pups (Champagne et al.,
2004; Li and Fleming, 2003). The amygdala, a central node of the lim-
bic affective system similarly receiving OT projections, has also been
implicated in maternal attachment (Fleming and Korsmit, 1996; Lee
et al., 2000; Oxley and Fleming, 2000). Lesions to the amygdala reduce
maternal behavior (Toscano et al., 2009) and significant amygdala
c-fos changes are observed following mother-pup interaction
(Fleming and Korsmit, 1996). The NAcc and amygdala work in concert
with several cortical areas, including the medial preoptic area, an
OT-rich site that integrates infant sensory cues (Insel and Young,
(ACC),and thedorso-medialprefrontalcortex (dmPFC)(MacLeanand
Newman, 1988; Murphy et al., 1981; Stamm, 1955). It thus appears
that the neural basis of mothering integrates OT-rich sub-cortical
motivational limbic areas with higher-level networks implicated in
emotion modulation, social cognition, and empathy that allow the
mother to read her infant's signals and plan adequate parenting.
Few studies examined OT in relation to attachment-based brain
responses in humans. Strathearn et al. (2009) scanned secure and in-
secure mothers while viewing their own infant's happy and sad ex-
pressions. Secure mothers showed greater activations to their
infant's happy face in reward-related ventral striatum pathways
and in OT-rich hypothalamic areas and these activations correlated
with peripheral OT response to mother-infant contact. In contrast,
insecure mothers showed greater insular activation to their infant's
sad expression. In an OT administration study, Riem et al. (2011a)
found that OT reduced amygdala activation to infant cry, consistent
with its known anxiolytic effects, while increasing activations in
empathy-related networks. In a second study of the same group
(Riem et al., 2011b) assessing functional brain connectivity in re-
sponse to infant laughter, OT was found to reduce amygdala activa-
tion and enhance functional connectivity between the amygdala and
cortical and subcortical regions, pointing to enhanced salience of
infant positive signals under OT.
In a recent study integrating brain, hormones, and behavior, we
examined mothers' brain response to dynamic, ecologically-valid in-
fant stimuli. Two groups of mothers were recruited on the basis of
their social behavior during mother-infant interactions; synchro-
nous mothers – mothers who coordinate their social behavior with
the infant's signals, and intrusive mothers – those who provide ex-
cessive parenting when the infant signals a need for rest. Both the
synchronous and the intrusive maternal styles are stable maternal
styles from infancy to adolescence and bear important consequences
for children's development (Feldman, 2010; Sroufe, 2005). Whole-
brain analyses showed that synchronous mothers exhibited greater
activations in the left NAcc, indicating that parenting in these
mothers is underlay by reward-related motivational mechanisms,
whereas intrusive mothers activated the right amygdala, suggesting
anxious and stress-related mechanisms underlying maternal care.
Functional connectivity analysis showed that among the synchro-
nous mothers, left NAcc and right amygdala were functionally corre-
lated with emotion modulation, theory-of-mind, and empathy
networks whereas among intrusive mothers, left NAcc and right
amygdala were functionally correlated with pro-action areas. SPIN
analysis, a technique measuring the temporal coherence of activity
in a brain nucleus over time, indicated that in the synchronous
group, left NAcc and right amygdala activations displayed clearer or-
ganization over time, whereas in the intrusive group activations
were more disorganized. Finally, correlations between OT with
NAcc and amygdala activations emerged in the synchronous group
only. Overall, these findings suggest that optimal parenting is under-
lay by reward-related motivational mechanisms, temporal organiza-
tionof brainand behavior,
maternal brain, interactive behavior, and the functioning of the OT
system (Atzil et al., 2011).
Finally, a new study examined associations between central and
peripheral OT in humans by testing the links between plasma OT,
variations in the OXTR and CD38 genes, synchronous parenting, and
memories of parental care in a large group of 352 mothers, fathers,
and non-parents. Variations in OXTR have been associated with
multiple social and emotional processes (Apicella et al., 2010; Israel
et al., 2009; Kim et al., 2010; Rodrigues et al., 2009), and risk alleles
on the OXTR rs2254298 and rs1042778 SNPs have been associated
with increased risk for disorders characterized by social dysfunctions
such as autism spectrum disorder (ASD, Lerer et al., 2008) and major
depression (Thompson et al., 2011). In addition, we measured allelic
variations on the CD38 gene. In humans, the CD38 rs3796863 risk al-
lele has been associated with increased risk for ASD (Munesue et al.,
2010). We found that individuals with high risk alleles on the OXTR
rs2254298 or the OXTR rs1042778 SNPs or on the CD38 rs3796863
SNP had lower levels of plasma OT and the effects were similar in
mothers, fathers, and non-parents, demonstrating that peripheral
levels of OT partially reflect OT neuropathways. Reduced plasma OT
and risk alleles on the OXTR and CD38 genes were each related to
lower frequencies of parental affectionate touch during parent–infant
interactions, similar to the findings in rodents (Meaney, 2010). Epi-
sodes of parent–infant gaze synchrony, moments in which parent
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and infant share their social gaze, were the longest among parents
who had both high levels of plasma OT and the low-risk CD38 allele.
These findings provide initial evidence that human attachment is me-
diated in part by the extended oxytocinergic system, including
peripheral levels of plasma OT, the CD38 gene, which is essential for
OT release, and the OXTR, the single receptor encoding for this neu-
ropptide (Feldman et al., 2012).
OT and fathering
Paternal care is observed in only 3–5% of mammalian species, bi-
parental species that exhibit active paternal involvement in childcare
(Geary, 2000). Yet, whereas mammalian maternity is obligatory, mam-
malian paternity is facultative and functions to enhance infant endur-
ance in the context of maternal care. Facultative fathering shows
within-species variations that depend on social and ecological condi-
tions, affords offspring a social competitiveness advantage (Clutton-
Brock, 1991; MacDonald, 1988),and contributes tooffspringendurance
by means of both father-specific investments and mechanisms related
to the co-evolution of mothering and fathering (Geary, 2000; Zigler,
2000). Across species, bi-parental mothers and fathers exhibit a
gender-specific repertoire of parental behavior. Whereas the maternal
repertoire involves licking, grooming, and the species-typical forms of
touch-and-contact, paternal behavior is characterized by stimulatory
activities, encouragement of exploration, and carrying the pups in
space (Carter etal.,2005; Lonstein and DeVries, 2000). Human mothers
andfathers similarlyengageingender-specific behaviors,with mothers
preferring face-to-face positions and the maternal affectionate reper-
toire (Feldman et al., 2007), whereas fathers engaging in interactions
that induce high positive arousal, exploratory focus, and rough-and-
tumble contact (Lamb, 2010; Parke, 1996). Similarly, whereas mother-
infant synchrony is rhythmic and socially-focused, father-infant
synchrony is outward-oriented and contains quick and unpredictable
peaks of positive arousal. It thus appears that mothers and fathers pre-
pare infants to different elements embedded in attachment bonds:
Mothers establish asense of predictabilityand safety, whilefathers pre-
pare for novelty and excitement, and both components are needed for
the formation of lasting attachments (Feldman, 2003).
Most animal studies on the neuropeptide basis of fathering exam-
ined the relations between paternal behavior and Arginine Vasopres-
sin (AVP), a closely related neuropeptide to OT implicated in male
bonding and aggressive and territorial behavior (Bielsky et al., 2005;
Wang et al., 2000). Few studies in our lab examined OT in fathers
and showed links between OT and the parent-specific repertoire as
well as associations between AVP and paternal care.
In a study assessing OT in first-time fathers, we observed 160
mothers and fathers (80 couples) and their firstborn child, micro-
coded maternal and paternal social behavior, and measured the par-
ents' plasma OT and salivary CT in the first postpartum month and
again six months later. Counter to expectations, we found comparable
levels of baseline OT in fathers and mothers in the two time-points
and both mothers and fathers showed higher levels of plasma OT
compared to non-attached singles. Possibly, active paternal care pro-
vides one pathway to activate the OT system in bi-parental mammals,
which in mothers is triggered by birth and lactation. OT in mothers
and fathers showed biological synchrony, that is, maternal and pater-
nal levels were inter-related at both the postpartum period and six
months later, suggesting a process of endocrine fit in which partners
shape each other's neuropeptide response through affiliative behavior
and marital and coparental attachment. Finally, consistent with find-
ings in biparental mammals, OT in mothers correlated with the social-
affective repertoire, including maternal gaze, affect, vocalizations, and
affectionate touch, whereas OT in fathers was associated with the
object-oriented stimulatory play, consisting of positive arousal, object
exploration, and stimulatory touch (Gordon et al., 2010a).
A second study of 112 mothers and fathers (not couples) and their
4–6 month old infants examined whether the parent-specific form of
touch functions to induce an OT response in the parent. OT functions
as a bio-behavioral feedback loop and more touch and contact within
attachment relationships increase OT levels and vice versa (Feldman
et al., 2010b). Plasma and salivary OT were collected from mothers
and fathers at baseline and following a 15 minute “play-and-touch”
session, an experimental paradigm in which parents are asked to
play freely with their infants and include any form of touch they typ-
ically use. Consistent with the typologies of high- and low licking-
and-grooming rodents (Champagne, 2008; Zhang and Meaney,
2010), we found different profiles of OT response in the high-touch
and low-touch groups. Mothers who provided high levels of affection-
ate touch (>66% of the time) showed an increase in salivary OT from
pre- to post-interaction but such increase was not observed among
mothers providing minimal touch (b33%). Consistent with the
father-specific pattern of paternal care in mammals (Geary, 200), fa-
thers who provided high levels of stimulatory contact, such as moving
the child's limbs, throwing the infant in the air, or moving the child
across the room, increased their OT levels but not those engaging in
minimal stimulatory touch (Feldman et al., 2010a). These findings
have important translational implications and suggest that active pa-
rental touch can trigger an OT response in parents. Such findings can
be used to devise touch-based interventions in cases where the OT
system is dysfunctional, such as maternal post-partum depression.
Three studies examined OT and paternal behavior in combination
with other hormones. Plasma OT and AVP and parenting behavior
was measured in 144 mothers and fathers interacting with their
six-month old infants. Interactions were micro-coded for the two
behavioral constellations of mothers and fathers: social-oriented
affiliative play and object-oriented stimulatory play. OT and AVP
were not related and both showed comparable levels in mothers
and fathers. However, OT was associated with the social-affective
play in both mothers' and fathers' behavior, whereas AVP correlated
with the object-directed stimulatory type of engagement. Interesting-
ly, the infant's social and object play behaviors were also differentially
related to the parent's OT and AVP, consistent with the model's
predictions that attachment partners shape each other's physiology
through joint interactive behavior within a social context. In a second
study, OT and prolactin (PRL) were measured in the plasma of 43
fathers and their behavior during two play sessions — a social play
session and an object-exploration toy session were micro-coded.
OT and PRL were inter-related but were differentially associated
with paternal behavior in the two play sessions. OT correlated with
the father's behavior during the social play, whereas PRL was associ-
ated with his play during a session that called for introduction of
specific toys and coordinating exploration with the infant (Gordon
et al., 2010b). Consistent with much research on the links between
OT and heightened social focus in humans (Bartz et al., 2011), it ap-
pears that OT is especially linked with early parental behavior that
aims to engage infants socially and emphasizes non-verbal relational
components infants must learn in order to become members of their
social group. In addition to dyadic parent–child contexts, we mea-
sured parental OT and CT in relation to parents and infant's behavior
during a triadic mother-father-infant interaction. Triadic synchrony –
moments when parents and child are all in physical contact and coor-
dinate their social gaze – were predicted by both mothers' and
fathers' OT and were negatively related to the parents' CT (Gordon
et al., 2010c). Finally, apart from the father-specific modes of play,
we assessed plasma, salivary, and urinary OT in mothers and fathers
interacting with their 6-month olds, we found that plasma and
salivary OT were inter-related and both correlated with the degree
of interactive synchrony between parent and child's affective expres-
sions and with the number of positive communicative sequences
observed during play (Feldman et al., 2011). Overall, these studies
highlight the role of OT in supporting paternal behavior in both
dyadic and triadic interactive contexts and as a hormone linked
with the father-typical affiliative behavior.
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Biological synchrony at the brain level among attachment partners
was tested with an fMRI paradigm in which mothers and fathers were
scanned while observing the same video of the attachment target-
their own infant during solitary play. As suggested, fMRI studies of
parenting point to the involvement of two neural networks underly-
ing maternal care, a motivational-emotional limbic network, includ-
ing the amygdala and NAcc, and a cortical social-attention network
implicated in emotion modulation, social understanding, and empa-
thy, including the medial prefrontal cortex (mPFC), Superior Tempo-
ral Sulcus (STS), insula, and inferior frontal gyrus (IFG), which
integrate to support the mother's intuitive understanding of infant
signals (Barrett and Fleming, 2011; Swain et al., 2007). Thirty
mothers and fathers, comprising 15 married couples of young infants,
were canned while observing own-infant compared to standard-
infant videos and online correlations between the voxel-by-voxel
activations of mother's and father's brains were computed with a
specifically-tailored algorithm. Online synchrony in brain activations
between mothers' and fathers' brain emerged in social-cognitive
cortical networks implicated in empathy, theory-of-mind, and mirror
functions but not in limbic networks. Mothers showed greater limbic
activations than fathers, and activations in limbic-motivational areas
were correlated with maternal OT. Fathers showed greater activations
in emotion-regulatory circuits, particularly in the mPFC, which were
linked with paternal AVP. These findings are the first to show that
parents synchronize online brain activity in social-cognitive networks
that support intuitive understanding of the infant's communica-
tions and the planning of appropriate caregiving. These data provide
evidence for the bio-behavioral synchrony model and suggest that
such brain synchrony may support the emergence of human attach-
ment within the matrix of neurobiological attunement between social
partners (Atzil et al., 2011b).
Finally, an OT administration study to fathers provides further
support to a neuro-peptide bio-behavioral synchrony model. Thirty-
five fathers and their 6-month old infants participated in a double-
blind placebo-controlled crossover study. Fathers inhaled either OT
or placebo and salivary OT from both father and infant were
measured four times — at baseline and in 20-minute intervals follow-
ing administration. Respiratory sinus arrhythmia (RSA) was recorded
from father and child during play and paternal and infant social
behavior was micro-coded. Following OT administration, father's
salivary OT increased dramatically and RSA was higher, pointing to
a greater physiological readiness for social engagement (Porges,
2003). In addition, fathers showed more frequent touch and longer
durations of engagement behavior in the OT condition. Moreover,
consistent with the model's predictions, administration to father
had a similar effect on the physiology and behavior of the infant. In-
fant salivary OT showed a similar dramatic rise in the OT condition,
despite the fact that infants did not directly inhale OT. Similarly, in-
fant RSA was higher and durations of infant social gaze and toy explo-
ration were longer when fathers inhaled OT.
mechanisms of transmission are not entirely clear, these findings
are the first to demonstrate that OT administration to a parent can
lead to alterations in the physiology and behavior of the infant in
ways that induce greater readiness for social contact. These findings
have important translational implications for a potential neuropep-
tide treatment of infants at risk for social dysfunctions, such as sib-
lings of children with ASD, without the actual risk of administering
drug to a young infant (Weisman et al., 2011).
The cross generation transmission of OT in humans
Research in animal models indicates that the generational trans-
mission of OT operates through parenting behavior (Francis et al.,
2002; Champagne, 2008, 2011) and similar mechanisms may be
expected in humans. Assessing cross-generation transmission of OT
as mediated by parenting behavior, we measured salivary OT in
mothers and fathers and in their 6-month old infants at baseline
and following the “play-and-touch” paradigm and micro-coded the
partners' interaction synchrony. Already at this young age, parent
and infant's OT levels were inter-related at both the baseline and re-
activity assessments and the degree of OT increase following con-
tact was correlated as well. Parent–infant synchrony was found to
moderate the inter-generational effect. In the context of high par-
ent–infant synchrony, the degree of concordance between the parent
and infant's OT was high whereas no associations emerged between
parent and infant's OT when synchrony was low. These data sug-
gest that behavioral coordination provides one channel through
which parental OT shapes the infant's emerging neuropeptide organi-
zation and its ensuing life-time effects on social affiliation (Feldman
et al., 2010a).
A different line of research on the generational transmission of
OT examined adults' retrospective accounts of parental care in their
childhood in relation to OT. Heim et al. (2009) found lower levels of
OT in the CSF of women with a history of child abuse. Gordon et al.
(2008) showed that adult memories of the warmth and care they
received as children were related to higher plasma OT. Bartz et al.
(2011) demonstrated that the effects of OT administration on memo-
ries of maternal closeness in childhood were mediated by the indivi-
dual's history of reported attachment security and the beneficial
effects of OT inhaling were observed only among securely attached
individuals. Finally, Feldman et al. (2011) found that mothers' and
fathers' plasma and salivary OT were related to more positive memo-
ries of parental care as well as to more secure attachment to romantic
partners. Finally, in the aforementioned study of plasma OT and ge-
netic variability (Feldman et al., 2012), memories of parental care
were examined in relation to the parent's actual behavior toward
his or her infant. Among both parents and non parents, more positive
memories of parental care were associated with higher plasma OT
and the low risk alleles on the CD38 rs3796863 SNP. Furthermore,
mothers and fathers who reported more positive care in their own
childhood provided more affectionate touch to their infants, con-
sistent with the generational transmission of optimal parenting
through patterns of maternal touch described for other mammals.
OT and mothering in atypical development
Emerging research suggests that disorders associated with disrup-
tions to maternal–infant bonding are marked by disordered function-
ing of the OT system. Mothers with high symptoms of antenatal and
post-partum depression had lower plasma OT (Skrundz et al.,
2011). Lower levels of OT and AVP were found among adopted chil-
dren with a history of disrupted early attachment (Fries et al.,
interactions with their infants also showed greater OT response and
greater ERP activation of the P3 component, implying greater focused
attention to their infant's pictures (Bick and Dozier, 2010). In a longi-
tudinal study of 155 clinically depressed and non-depressed mothers
and their children followed from birth to six years, we found that
nearly 60% of the children growing up in the context of chronic
maternal depression suffered a psychiatric disorder, mostly anxiety
or conduct disorders, and showed lower emotional self-regulatory
skills, reduced empathy to the distress of others, and disruptions to
social engagement behavior, expressed in social withdrawal, minimal
eye contact, diminished arousal, enthusiasm, and creativity, and
lower symbolic play. Depressed mothers had significantly lower sali-
vary OT, but consistent with expectations, lower levels of peripheral
OT were also observed in the children as well as in the fathers and
were related to the diminished reciprocity between parent and
child. Moreover, we found that functioning of the OT system provided
a buffer against the effects of chronic maternal depression on infant
social growth and psychopathology. Chronically depressed mothers,
as well as their children, were four time more likely to be homozy-
gous for the G risk allele on the OXTR rs2254298, consistent with pre-
vious research pointing to associations between this allele and
expressed morejoy during
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greater risk for major depression (Thompson et al., 2011). Yet, chil-
dren of depressed with the A low risk allele on the OXTR rs2254298,
had higher levels of salivary OT, significantly lower levels of psycho-
pathology and their expressed empathy was comparable to that of
controls. These findings suggest that in the context of risk associated
with maternal-infant bonding, more optimal functioning of the OT
system may promote resilience and provide a buffer that mitigates
some of the effects of maternal depression on children's social com-
petence, empathy, and proneness to psychopathology (Feldman,
2011b). Taken together, these findings highlight the lifetime risk im-
posed by early disruptions to the parent-infant bond that preclude
the experience of bio-behavioral attunement between maternal and
infant's physiology and behavior, whether by risk related to infant
biological conditions, such as ASD or prematurity, maternal dis-
order, such as postpartum depression, or contextual risk, such as
abuse and neglect.
OT and romantic attachment: pair bonding in humans
Romantic relationships have a profound effect on adult life and
have been associated with well-being and health, whereas the inabil-
ity to form and maintain intimate bonds is linked with much psycho-
logical distress (Burman and Margolin, 1992; Bloom et al., 1978). Yet,
very little research addressed the neuroedocrine basis of pair bonding
Animal studies point to the role of OT in pair bonding in mammals
(Carter, 1998). OT plays a critical role in the regulation of pair-bond
formation in monogamous prairie voles (Insel and Hulihan, 1995):
intracerebroventricular infusion of OT facilitates partner's attachment
in female prairie voles (Williams et al., 1994), blockade of OT recep-
tors impairs bond formation (Cho et al., 1999), and peripheral levels
of OT correlate with partners' affiliative behavior (Snowdon et al.,
2010). Human studies similarly highlight the involvement of OT in
pair bonding. OT administration increased couples' positive commu-
nication (Ditzen et al., 2009) and plasma OT was related to positive
communication, affiliation, and emotional support between partners
(Gonzaga et al., 2006; Grewen et al., 2005). Yet, results are mixed
and few studies found correlations between OT and negative emo-
tions, anxiety, and distress in romantic couples (Holt-Lunstad et al.,
2008; Tabak et al., 2010; Taylor et al., 2010).
In addition to direct measurement of OT, imaging studies of ro-
mantic partners showed greater activations in OT- and dopamine-
rich brain areas, such as greater neural activity in the left posterior
cingulate cortex and caudate regions, in the initial stages of romantic
attachment, whereas activations of the cortical regions including an-
terior cingulate, insular cortex, and ventral pallidum was increased
in long-term pair-bonds (Aron et al., 2005; Bartels and Zeki, 2004;
Kim et al., 2009). Both the initial period of romantic love and long-
term relationships are associated with neural activity in dopamine-
rich reward and basal ganglia systems, such as the ventral tegmental
area (VTA) and dorsal striatum (Aron et al., 2005; Acevedo et al.,
2011; Bartels and Zeki, 2004). These finding underscore the OT-
dopamine associations proposed as one mechanism that mediates
the effects of OT on bond formation. Consistent with the OT-
dopamine model, an increase in parasympathetic activity, as mea-
sured by RSA response to negative and positive emotions, was also
found during the first period of falling in love (Schneiderman et al.,
2011). Interestingly, brain regions implicated in maternal attach-
ment were also shown to be activated in prolonged romantic rela-
tionships as assessed by both fMRI (Acevedo et al., 2011) and ERP
(Weisman et al., in press), consistent with the position that parental
and romantic attachment share underlying mechanisms (Feldman,
in pressa, in pressb).
In a recent study, we assessed the role of OT in romantic attach-
ment in a group of 163 young adults, including 120 new lovers
(60 couples) three months after the initiation of a romantic
relationship and 43 non-attached singles. Twenty-five of the 36 cou-
ples who stayed together were seem again six months later to evalu-
ate dynamic changes in OT during the period of pair bonding in
humans. Similar to our research in parents, couples were observed
in dyadic interactions and were each interviewed regarding
relationship-related preoccupations, thoughts, worries, and typical
attachment behaviors. Results showed that plasma OT levels were
significantly higher in new lovers as compared to singles, suggesting
increased activity of the OT system when falling in love. Interestingly,
comparing OT in new parents, new lovers, and singles, levels among
the new lovers were the highest, significantly higher than those ob-
served in parents, highlighting the first period of romantic attach-
ment and its accompanied euphoria as the one associated with
greatest increase in OT production. During the six months between
the first and second assessments, these high OT levels did not drop
and were stable within individuals. Plasma OT correlated with the
couple's interactive synchrony, including behaviors such as social
focus, positive affect, affectionate touch, and synchronized dyadic
states, as well as with new lovers' preoccupations and worries regard-
ing the partner and the relationship. These findings show remarkable
similarity to those observed in parents and lend support to our model
that proposes consistency between the three prototypes of attach-
ment in humans. The findings further corroborate our proposition
that both parental and romantic attachment is supported by similar
OT-based neuroendocrine mechanisms and is expressed in a similar
behavioral repertoire including gaze, touch, affect, and vocalizations
and their online coordination (Schneiderman et al., 2012).
OT and filial attachment; our best friends
The TV series Friends captured the imagination of an entire gener-
ation, possibly as filial attachment represents a deep human need that
is often left unmet in today's technological society. Any random
stretch from the long-running series demonstrates with remarkable
precision that close friendship is expressed by intimate familiarity
with the pace, rhythms, jokes, movements, behavioral mannerisms,
and verbal idiosyncrasies of each member of the clan. However,
although close friendships are important components of well being
and social adaptation, in contrast to the extant research on the
parent-infant bond and, to a lesser extent, on romantic attachment,
nearly no research has focused on the long-term attachments indi-
viduals form with their best friends, their physiological correlates,
and mental health sequalae. Research has documented children's
entry into social groups at the preschool years and described the
development of children's friendships across middle childhood
(Asher and Gottman, 1981; Hartup, 1989; Schneider et al., 1989),
yet, we are aware of no study that examined best-friend relationships
from an “affiliation” perspective, observing interactions between
close friends and assessing the reciprocity, engagement, and interper-
sonal sensitivity between children and their intimate friends and
their neurohormonal correlates.
In two longitudinal studies we examined children's interac-
tions with their best friends and their links with the synchrony
children experienced within the mother-child and father child re-
lationship in infancy, thereby addressing the consistency between
parental and filial attachment. In one of these studies, OT was also
The first study was a longitudinal follow-up of the cohort of
mothers and fathers and their firstborn child described above
(Gordon et al., 2010a). We re-visited these families when the children
were 3 years, the age when children first show selective attachment
to a “best friend” (Asher and Gottman, 1981). Mothers' and father's
plasma OT and interactive synchrony were measured when infants
where one and six months. At 3 years, children were videotaped
interacting with mother, father, and best friend and baseline and
reactivity assessments of salivary OT were collected before and after
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play. Consistent with the model's predictions, we found that children
experiencing more synchronous parenting in infancy and more sensi-
tive and responsive concurrent interactions with their parents trans-
ferred these positive internalized relationships to their first “filial
affiliation” and their interactions with best friends were marked by
greater reciprocity, rudimentary concern for the friend's needs (e.g.,
“you can have the toy”), greater emotional involvement, and higher
affective attunement, as has been long suggested by Bowlby (1969).
OT showed individual stability in each parent. These data describe a
three-year stability in peripheral OT in humans and suggest that OT
production may be set in early childhood through experiences within
the mother-infant relationship and continues to function in a relative-
ly consistent manner throughout life. Consistent with our previously
described findings for the cross generation transmission of OT in in-
fants and children of depressed mothers, child OT correlated with par-
ents' OT and was predicted by the level of synchrony the child
gest a mutually influencing bio-behavioral process where child OT is
shaped by the parents' early behavior,the parents'postpartum behav-
ior is predicted by their OT levels, and the parents' early behavior and
neuroendocrine response predict more reciprocal dialog and greater
empathy between children and their close friends at the time when
children make their first attachments to non-kin members of society.
In the second study, we followed children's multiple affiliative
bonds and social adaptation longitudinally from infancy to adoles-
cence. Children were observed at 5 months, 3 years, and 13 years
during interactions with mother and father. At 3 years, children
were also observed in lengthy ecological observations at childcare
to assess social competence and aggression in the peer group. At
13 years, children were observed interacting with same-sex best
friend in a positive (planning a school activity) and conflict (dialoging
a conflict in their relationship) interactions. We found that the degree
of reciprocity children formed with mother and father were individu-
ally stable across the 13-year period and were mutually-influencing
between couples so that maternal and paternal reciprocity were
inter-related at each stage. Children reared in contexts of high paren-
tal reciprocity throughout infancy showed greater social adaptation at
childcare, that is, they were more friendly, cooperative, interacted
with ease with adults and peers, were able to show both leadership
and participation, were self-regulated, maintained social involve-
ment, and were able to find more prosocial solutions to conflicts
with peers (e.g., “you take the red color first and then I take”). Adoles-
cents whose parents were more reciprocal throughout childhood
showed better dialogical skills during interactions with best friends.
Dialogical abilities imply the capacity to acknowledge the other's
needs, opinions, and emotions; view oneself in someone else's posi-
tion; discuss disagreements with empathy while maintaining positive
affect and involvement; and engage in a give-and-take, fluent, and
non-constricted exchange while maintaining an autonomous stance
(Feldman and Bamberger, 2011). Dialogical skills are thought to pro-
vide the basis of the individual's empathic, prosocial, and moral orien-
tation (Batson, 1991; Day and Tappan, 1996). Although OT was not
measured in this study, previous studies showed that OT adminis-
tration increases both trust and empathy (Bartz et al., 2011). This sug-
gests that the capacity for empathy develops within close attachment
bonds in early infancy, develops to include the first non-kin mem-
bers of the social group children encounter, continue with intimate
friends in early adolescence, an age when children often consolidate
life-long friendships (Hartup, 1989), and culminate in the capacity
to form and maintain romantic bonds and eventually provide nurtur-
ance to the next generation. Overall, these findings demonstrate the
consistency between the three types of affiliative bonds humans
form throughout life – with parents, partners, and best friends –
and demonstrate that both behavioral expressions and neurohor-
monal substrates play an important and mutually-influencing role
in the formation and maintenance of affiliative bonds.
Conclusions and implications
Our capacity to form, maintain, and conduct our lives in the con-
text of close affiliative bonds marks, at least according to some per-
spectives, the apex of the human condition. This review offers a
behavior-based neuroedocrine perspective on affiliation in humans
within an evolutionary framework. The biobehavioral synchrony
model highlights the behavioral building blocks of social bonding,
including gaze, touch, vocal, body, and affective expressions; con-
siders the ways in which these micro-social behaviors coalesce into
unique affiliative bonds with specific pace, rhythm, patterns, and in-
terpersonal focus starting from the first day of life; and describes
how early social bonds transform yet maintain their consistent ex-
pression and underlying neurobiology across multiple relationships
throughout life. The theoretical model and empirical findings pre-
sented here resonate with two types of conclusions, conceptual con-
clusions and translational conclusions, and each is discussed in turn.
Gerald Edelman, among the well-known theoreticians in neuro-
science, argues in his latest book Second nature (2006) that the cen-
tral unresolved issue in current neuroscience is that of subjectivity.
After countless of studies, models, dollars, and effort resulting in
great advances in the study of the brain and its workings, knowledge
of the human brain remains external to the experiencing individual.
There is still no way science can bridge the “subjectivity gap” and
measure how perceptions, thoughts, emotions, and physiological
states are felt by the living self-aware person. This, Edelman main-
tains, is not merely a problem to be resolved by more sophisticated
machines but may represent an inherently unsolvable gap. While
acknowledging the gravity of the subjectivity dilemma, we tenta-
tively suggest that one way to approach the issue of subjectivity is
through the lens of inter-subjectivity. According to the phenomeno-
logical philosophy of Husserl, detailed in his famous Philosophy as a
rigorous science (Husserl, 1911), the human capacity to “know”
about “things” in the outside world is never categorical but always
involves a relationship, a relationship between the perceiving self
and the external object. Consistent with this perspective, our bio-
behavioral synchrony model suggests that the human capacity to per-
ceive such relationships between the self and the external world, per-
ceptions which provides the basis for any knowledge, is formed
within the matrix of the “nursing dyad”. The human infant's capac-
ity to engage in the world and learn its signals is supported online
by neurohormonal and brain systems that maintain the infant's in-
volvement with close attachment partners. The role of these attach-
ment partners is to become intimately familiar with the infant's
social signals and escort the child into the world in a step-by-step
manner that resonates with the infant's subjectivity at both the bio-
logical and behavioral levels. Within such finely-tuned attachments,
the human infant can send signals that are reciprocated and turn
into interpersonal events that transform subjectivity into inter-
subjectivity. These mutually-regulated bio-behavioral cycles keep
the child's focus on the social world and provide the basis for explo-
ration, sharing, and meaning-making. It can thus be suggested that
these moments of inter-subjectivity lie at the mid-range between
Edelman's closed brain that is available only to the experiencing indi-
vidual and the external material brain that is accessible to scientific
research. Such conceptualization echoes the “intermediate area” of
play, love, and creativity described by Winnicott (1971), in which
the internal and the objective are mutually influenced and co-
constructed. Synchronous processes, through their online integra-
tion of physiology and behavior between attachment partners within
a social context, can transform the intra-psychic into an inter-
personal event that is open to objective measurement while still pre-
serving its personal qualities. Synchrony, therefore, may offer a
R. Feldman / Hormones and Behavior 61 (2012) 380–391
Author's personal copy
unique venue for the external observation of a private brain experi-
ence, as seen by the findings which show parallel response in one
partner to the physiological changes in the other, whether involving
brain activations or alterations in peripheral hormones and autonom-
ic activity following OT administration. As such, the current model
offers a framework for future theory and research on the ongoing
co-construction of brain activations, hormonal response, and behav-
ioral expressions between attachment partners that may tap the
issue of subjectivity by objectively describing shared “private” pro-
cesses at the hormonal, brain, and behavioral levels.
The potential for neuropeptide therapy to treat disorders of social
functioning has been recently suggested, triggered by the marked and
consistent effects of intranasal administration of OT on improving
social and emotional functioning in healthy individuals and in
remedying some key features of the disorder in high-risk populations
(Meyer-Lindenberg et al., 2011). OT therapy has been suggested, and
in some cases studied, in conditions such as ASD, depression, schizo-
phrenia, and social anxiety. The current findings provide a detailed
description of the reciprocal relations between OT and attachment-
related social behaviors beginning in the neonatal period with the
parents, and continuing through children's close friendships, young
adults' romantic attachment, and adults' parental and co-parental
processes. These rich micro-level behavioral observations may high-
light several translational directions. First, results indicating associa-
tions between OT increase and high levels of parental touch may
help devise interventions for mothers suffering from post-partum
depression, a condition affecting nearly 18% of women in industrial
societies (Serretti et al., 2006), or following premature birth, a condi-
tion occurring in approximately 12% of births (March of Dimes, 2006).
Depressed mothers tend to show minimal levels of affectionate touch
(Feldman et al., 2009) and maternal touch following premature birth
is similarly reduced (Feldman and Eidelman, 2007). This diminished
maternal contact may mediate the low levels of OT in their children.
Interventions that induce maternal touch, educate mothers on the
importance of tactile contact for infant development, and teach
mothers concrete techniques for more optimal touch may help trigger
the OT system in depressed mothers. Such techniques may also be
important following premature birth, when the OT system has often
not been initiated properly due to C section, difficulties in breastfeed-
ing, incubation, and the physical separation between mother and
child. Due to the mutual effects of maternal and paternal OT on
each other and on the child, fathers' touch may also be important in
cases of maternal postpartum depression and premature birth.
Emerging data from our lab point to the positive effects of OT on emo-
tional functioning and well-being in combat-related PTSD, and such
techniques may ease the often lifetime negative effects of the dis-
order on the veteran and his family. The dramatic increase in OT
during the initial stages of romantic attachment and its relation to
couple reciprocity may suggest that OT therapy can be used in con-
junction with concrete behavioral-relational intervention for couples
in distress. The intriguing findings showing that OT administration to
parent and have parallel effects on the infant's hormonal and auto-
nomic systems that support social engagement may open new oppor-
tunities to treat young children who are at high risk for social
dysfunctions, such as children growing in abusive contexts of siblings
of ASD children, without the ethical difficulties of administering drug
to a very young infant. Finally, the associations described between al-
lelic variations on the OXTR and CD38 genes suggest that integrating a
molecular genetic approach into the study of OT intervention may
specify treatment to those most at need on the basis of their genetic
make-up. Yet, it is important to remember that although advances
in translational OT research may open new and exciting vistas, it is
critical that such advances should be integrated with effort directed
to parental training, re-evaluation of social priorities, and policy mak-
ing. Nearly 60 years ago Bowlby (1953) advocated for the well-being
of children with the plea that “it is in childhood that we learn to love”.
Our responsibility as caregivers, scientists, policy makers, mental
health professionals, and concerned citizens is that every young
child should be given the opportunity to learn how to love and
every young parent should receive the guidance to make it happen.
Research at Prof. Feldman's lab is supported by the Israel Science
Foundation (#1318/08), the US-Israel bi-national Science Foundation
(2005-273), the NARSAD Foundation, the German-Israel Science
Foundation (GIF), the Irving B. Harris Foundation, the Kor Family
Foundation, and the Katz Family Foundation.
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