Feature Review
The Neurobiology of Human
Attachments
Ruth Feldman1,2,
*
Attachment bonds are a defining feature of mammals. A conceptual framework
on human attachments is presented, integrating insights from animal research
with neuroimaging studies. Four mammalian bonds are described, including
parent–infant, pair–bonds, peers, and conspecifics, all built upon systems
shaped by maternal provisions during sensitive periods, and evolution from
rodents to humans is detailed. Bonding is underpinned by crosstalk of oxytocin
and dopamine in striatum, combining motivation and vigor with social focus,
and their time sensitivity/pulsatility enables reorganization of neural networks.
Humans’ representation-based attachments are characterized by biobehavioral
synchrony and integrate subcortical with cortical networks implicated in
reward/motivation, embodied simulation, and mentalization. The neurobiology
of love may open perspectives on the ‘situated’ brain and initiate dialog between
science and humanities, arts, and clinical wisdom.
The measure of the intensity of love
Is measure, also, of the verve of earth.
For me, the firefly's quick, electric stroke
Ticks tediously the time of one more year.
And you? Remember how the crickets came
Out of their mother grass, like little kin,
In the pale nights, when your first imagery
Found inklings of your bond to all that dust.
Wallace Stevens, Harmonium
Human Attachments throughout Life Share Underlying Neurobiology
Since the dawn of humanity, ‘the intensity of love’ has been depicted by modalities vastly
different from scientific ‘measurement’: cave paintings, clay figures, story-telling, dance, music,
and poetry. Over the last decades, studies in animal models, particularly rats and monogamous
prairie voles, began to uncover the cellular, neural, and endocrine mechanisms implicated in
maternal care and pair bonding. Those gave rise to a new field of inquiry – the neurobiology of
human attachments – which integrates insights from other mammals with new tools available for
human research – brain imaging, neuroendocrinology, genetics and epigenetics, and peptide
administration – to test the biological basis of human attachments. This emerging field is
generating a growing body of knowledge which requires a new conceptual framework, one
that integrates cross-species comparability with the distinct features of human love [1,2].
The goal of this paper is to provide such a conceptual frame for the neurobiology of human
attachments and address its tenets, parameters, and neural basis. While this conceptual
1
The Gonda Brain Sciences Center,
Bar-Ilan University, Ramat Gan, Israel
2
Yale University Child Study Center,
New Haven, CT, USA
*Correspondence:
feldman.ruth@gmail.com (R. Feldman).
80 Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2 http://dx.doi.org/10.1016/j.tics.2016.11.007
© 2016 Elsevier Ltd. All rights reserved.
Glossary
Activity-dependent facilitation:
occurs when presynaptic spike
activity is paired with activity of
facilitatory interneurons, leading to
enhanced neuronal activation [198].
Alloparenting: the care of infants by
adults other than the biological
mother. Alloparenting is common
across primate species and
enhances infant survival [84].
Biobehavioral synchrony: the
coordination of biological and
behavioral processes between
attachment partners during social
contact. It is a key feature of human
attachments.
Heteromers: G protein-coupled
receptors (GPCRs) consist of seven
membrane-spanning alpha-helical
segments that combine into a single
receptor. However, GPCRs can form
heteromers by combining two or
more GPCR subunits. The oxytocin
receptor belongs to the G proteincoupled
receptor family. NA shell
contains oxytocin receptors that may
form heteromers with D2 receptors
on medium spiny neuron. The ligandbinding
properties and neural
pathways of heteromers integrate
aspects of both parent receptors.
Long-term depression: reduction in
the efficacy of neuronal synapses
following a long repeated stimulus.
Medium spiny neurons (MSNs):
projection neurons that are
GABAergic (inhibitory) and comprise
over 90% of neurons in the human
striatum. MSN come in two formats.
The D1-type (D1 dopamine receptorexpressing
neurons) functions in the
‘direct pathway’, that is, convey their
information directly to the output
nuclei of basal ganglia. The D2-type
(D2 dopamine receptor-expressing
neurons) functions in the ‘indirect
pathway’, conveying information to
basal ganglia indirectly via pallidal
neurons. Some MSNs express for
both D1-type and D2-type receptors.
Myoactivity: the stimulation of
rhythmic tissue contraction.
Myoactivity is the most conserved
function of the oxytocin system,
which has been integrated in
mammals into the oxytocin-controlled
uterine contractions and milk ejection
[43,62].
Sensitive periods: specific time
windows in early life when the brain
must experience certain
environmental inputs for proper
maturation [2]. In the context of
framework is built upon empirical data in animals and humans, some of its details are speculative
and may guide future research. I argue that the study of mammalian bonding must be conducted
from a developmental perspective, both in relation to the life of an individual and in the context of
animal evolution, and that this is especially the case in humans whose large associative cortex is
wired, to a large extent, by early experiences within child-rearing contexts [3–5]. Later attachments,
with romantic partners, close friends, mentors, or in-group members from sports teams
to nations, repurpose the basic machinery established by the mother–offspring bond during
early ‘sensitive periods’ (see Glossary). I further suggest that the neurobiology of attachment
rides on systems that maintain brain plasticity through time-sensitive pulsatility – dopamine (DA)
and oxytocin (OT) – which, by forming tighter crosstalk during periods of bond formation [6],
integrates reward salience with social focus to reorganize neural networks around the new
attachment [7–9]. Studies in rodents have shown that the integration of OT and DA in striatum
supports the formation of maternal–infant and pair bonds [10]. Yet, while similar mechanisms are
thought to underpin bond formation in humans, attachment bonds acquired substantial complexity,
duration, and flexibility across mammalian evolution, reaching their apex in humans’ longterm
exclusive attachments that integrate subcortical reward with higher-order representational
components (Figure 1, Key Figure). Such flexibility affords not only the immense variability of
human attachments across cultural contexts but also enables later reparation, and while early
bonds shape the social brain and its underlying neurobiology, humans can repair, via top–down
processing, commitment, and discipline, the effects of early maladaptive relationships by later
benevolent ones. Key propositions of the model are summarized in Box 1.
Box 1. Key Propositions of the Neurobiology of Human Attachments Model
 Research on human attachments implicates a developmental perspective: Mammalian bonding is supported by
neurobiological systems shaped by the mother–offspring relationship during early sensitive periods [36].
 Continuity in neurobiological systems underpins human bonds: Human attachments repurpose the basic machinery
established by the parent–offspring bond in the formation of other attachments throughout life, such as romantic
attachment or close friendships [1].
 Human bonds are selective and enduring: Bonds are specific to attachment target and last for extended periods, often
a lifetime. Gradients of the selective and enduring components define the various human bonds (see Figure 1 in main
text).
 Bonding is behavior based triggered by the expression of species-specific, person-specific, and culture-specific
behavioral patterns: Bonding implicates bottom–up processes. Bonding-related brain and neuroendocrine systems
are activated by attachment-related behavior [5,37].
 Biobehavioral synchrony is a key feature of human attachments: Human attachments are characterized by the
coupling of coordinated nonverbal behavior with coordinated physiological response among partners during social
contact [101] (see Figure 2 in main text).
 Central role of the oxytocin system and oxytocin–dopamine connectivity: OT is implicated in human mothering,
fathering, coparenting, romantic attachment, and close friendship. Integration of OT and DA in striatum ignites
bonding, imbuing attachments with motivation and vigor [9].
 Bond formation involves increased activity and tighter crosstalk among relevant systems: Activation and closer links
among systems underpinning affiliation, reward, and stress management are observed during periods of attachment
formation [6].
 Human attachments promote homeostasis, health, and well-being throughout life: Social attachments enhance health
and happiness while social isolation increases stress, impaired health, and death [176].
 Patterns of attachment are transferred across generations: Behavioral patterns experienced in early life organize OT
availability and receptor localization in the infant's brain, shaping the capacity to parent the next generation [66,129].
 The human brain is a situated organ, shaped by the mother–infant attachment and proximity to mother's body to
function within the social ecology: The young mammal's immature brain at birth and need for close proximity to a
nursing mother shape the brain as a ‘situated’ organ, constantly responding online to the social world [71]. Humans’
protracted maturity sculpts the dialogical nature of the human brain and its constant need for social affiliations.
 Human bonds experienced throughout life are transformative and have the potential to repair early negative relationships
by later benevolent ones: The great plasticity of the human social brain and its behavior-based nature enable
later attachments to reorganize neural networks and repair, at least partly, negative early experiences. This highlights
the translational potential of research on the neurobiology of human attachments [177].
Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2 81
The Neurobiology of Mammalian Affiliation: Crosstalk of DA and OT
Our proposed model suggests that the ‘intensity of love’, the quality of attachment, is measured
in terms of the vigor [11] of DA action in striatum, particularly in the nucleus accumbens (NA). DA
acts in the NA to organize goal-directed reward-related behavior characterized by initiation and
vigor by inhibiting the inhibitory output of NA GABAergic (inhibitory) medium spiny neurons,
which then release ventral pallidum (VP) neurons in the basal ganglia to enable motor action [12–
15]. Disinhibition of the inhibitory control in the accumbens–pallidal indirect pathway, pathway
from striatum to basal ganglia which is not direct but acts via pallidal neurons, renders the VP
accessible to glutamate (excitatory neurons) inputs, leading to energetic behavior and marking
the striatum as a limbic–motor interface where reward translates into action marked by vigor and
goal directedness [16,17].
Yet, while DA neurons function as general-purpose stimulators to reward-related targets, it is
their close links with OT receptors in striatum, where OT receptors abound [18,19], that imbue
attachment bonds with incentive value and direct action toward affiliative goals, such as
maternal care [9,20,21]. Actions of DA D1-type and D2-type neurons on OT receptors in NA
shell establish maternal memory and form repetitive patterns of caregiving, as shown in rats
[22]. OT stimulates the accumbens–pallidal indirect pathway, strengthening synaptic activity
in VP and forming memories of the attachment context. NA shell contains OT receptors that
may form heteromers, neurons expressing for multiple receptors, with DA D2-type receptors
on medium spiny neurons, and OT binding to OT receptors increases affinity of DA to
associated D2-type receptors [23]. Since D2 receptors depress activity of medium spiny
neurons, OT can potentiate these inhibitory effects. The combination of DA D1-type and
D2-type receptors and OT receptors in NA shell functions to depress the striatal inhibitory
input to VP and enables supernormal excitation of basolateral amygdala projections to VP,
which, through activity-dependent facilitation, creates the effects of mesolimbic DA on
attachment-focused action [24,25]. The coactivation of D2-expressing neurons in the NA by
OT enables neurons specifically suited to identify sensory–motor reward patterns to employ
reward computations of D2 neurons to encode the temporal patterns of social reward, as
shown in rhesus macaques [26,27]. This allows the brain to internalize the social partner and
its preferences, encode relationship-specific patterns of social exchange, and draw reward
from the matching of self and partner's actions (i.e., social synchrony), which lead to
consolidation of the bond [13,26].
Overall, the tighter OT–DA crosstalk in the NA during bond formation enables plasticity of the
brain reward system and its flexible adaptation to incorporate the new bond into the self
[18,28,29]. Studies in prairie voles show that the NA receives OT receptors containing inputs
from multiple cortical regions, including sensorimotor and associative cortices and these
enable the formation of sensory and motor memories of attachment experiences [30].
Furthermore, OT receptor density in the NA in infancy was found to predict the time spent
huddling with partner in female prairie voles [31], and bereavement-like behavior and activation
of stress-related neurohormonal systems following partner loss in male prairie voles were
associated with suppression of OT signaling in the NA [32]. These findings highlight the role of
accumbens OT in forming continuity from parental to pair bonds and in buttressing the
protective function of long-term attachments. Finally, research in rats describes the role of OT
in long-term depression in amygdala, attenuating amygdalar response to aversive social
stimuli [33,34]. Such long-term depression reduces fear and facilitates the approach orientation
required for bonding [35]. Thus, while DA affords vigor and motivation, OT provides the
soothing and tranquility necessary for bond formation via its regulatory effects on hypothalamic–pituitary–adrenal
axis activity [36,37] and anxiolytic properties [38]. This creates a
unique neurobiological state of ‘immobility without fear’ [39], a state specifically suited for
the formation of new attachments.
bonding, these involve the speciestypical
parenting behaviors.
Striatum: a subcortical structure
serving key role in the reward
system. The striatum receives
dopaminergic inputs from multiple
brain areas and is the central input to
basal ganglia. The ventral striatum
contains the NA and the dorsal
striatum includes the putamen and
caudate. The ‘corpus striatum’
comprises the striatum and globus
pallidus.
Trophallaxis: the exchange of
sensory signals among members of a
social group [199]. The term was
extended to include social stimuli
[103] and to denote the reciprocal
multisensory stimulation of low
intensity that elicits approach
response. Parenting marks a
prototypical form of trophallaxis [105].
82 Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2
Key Figure
Attachment Bonds across Mammalian Evolution
Model systems
C. elegans
Oxytocin
Ancient funcƟons
Dopamine
Lamprey
EvoluƟonary origins
• Sensory–neurocircuitry coupling • Striato–pallidal pathway
• RegulaƟon of motor acƟon• RegulaƟon of basic life funcƟons
Parental
(maternal)
RomanƟc
(pair)
IntegraƟon of OT and DA in striatum ignites mammalian bonding
Friendship
(peer/clan)
Fellow humans
(conspecifics)
Olfactory-based,
Group-living,
expectaƟons-based,
corƟcal-monitored
affiliaƟons
RepresentaƟonbased,
long-term,
culture-informed
aƩachments
nest-bound,
hormone-dependent
bonds Rodents
Primates
Humans
• Non-exclusive
• Short-lived
• SubcorƟcal
• Evidence of
response to
distress of
familiar
conspecific
• Mostly none
• Prarie voles:
maƟng-based
recogniƟon
• No evidence
• Mostly none
• Monogamous
primates:
proximity-based
partner preference
• Exclusive,
alloparental
care
• Hormone primed,
not dependent
• Empathy/social
behavior to
group members
• Hormonal
the context of
coordinaƟon in
childrearing
• Time together
needed
• Exclusive, • Exclusive,
potenƟally
culture-defined,
independent,
long-term
associaƟon-based,
hormoneaƩachments
aƩachments
long-term,
independent,
memory-based
maƟng•
Personal, • AffiliaƟve behavior
long-term,
memory-based,
neurobiology of
and acƟvates the
affiliaƟon
and empathy that
acƟvate the
affiliaƟon
term aƩachment
neurobiology of
• Capacity for longto
other species
Figure 1. The figure describes the four bonds observed across mammalian species – parent–infant, pair bonds (romantic attachment), peers (close friendships), and
conspecifics (fellow humans) – and charts their expression in rodents, primates, and humans. Attachment bonds in mammals are underpinned by functioning of two
ancient systems, OT and DA, which maintained basic organization across vertebrate evolution and supported group living in harsh ecologies (OT) and motivational goaldirected
action (DA) throughout animal evolution. Caenorhabditis elegans and lamprey are presented here to illustrate model systems used by research to study the
ancient functions of OT and DA. The model proposes, on the basis of studies in rodents and primates, that the integration of OT and DA in striatum ignites mammalian
bonding. In humans, attachment bonds are marked by two main features: selective (specific to attachment target) and enduring (long lasting). The figure describes how
these two features undergo substantial reorganization across mammalian evolution. The decrease in color intensity from parental to pair to peer to conspecific indexes the
gradual weakening of intensity in these selective and enduring features from the parent–infant attachment (most intense color) to humans interactions with strangers (least
intense color). Abbreviations: DA, dopamine; OT, oxytocin.
Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2 83
Humans are wired for social affiliation via activity of this limbic circuit, comprising the OTproducing
hypothalamus, extended amygdala network, and striatum [including the ventral
tegmental area (VTA), which projects to striatum, and VP, which receives projections from
it]. This limbic network regulates critical survival and motivation functions and redirects them in
the service of social life [40]. Yet, while DA–OT links chart a mammalian-general mechanism of
bonding, as observed in rat mothers, prairie voles, and primates, connectivity of this limbic
system with cortical sites via multiple ascending and descending projections supports humans’
long-term exclusive attachments [5,41,42]. Notably, striatal activity has been detected in nearly
all imaging studies of human attachments; however, striatal/VTA activations are typically coupled
with both subcortical (amygdala and hypothalamus) and cortical structures, particularly the
anterior cingulate cortex (ACC), medial prefrontal cortex (mPFC), and orbitofrontal cortex (OFC)
of the reward system, in addition to structures supporting mentalizing, including the superior
temporal sulcus (STS) and temporoparietal junction (TPJ), and those underpinning embodied
simulation functions, such as anterior insula (AI), inferior parietal lobule (IPL), inferior frontal gyrus
(IFG), and supplementary motor area (SMA). Aspects of OT system functionality have similarly
been implicated in human maternal, paternal, romantic, and friendship attachments in research
employing OT administration, peripheral measures, or allelic variability and methylation of the OT
receptor gene (Box 2) [6,43–54]. Longitudinal studies following humans from infancy to adulthood
describe OT involvement in the transfer of attachment from parents to friends and romantic
partners [55,56]. Human studies indicate tighter connections between OT and DA in response to
bonding-related cues as mediated by social synchrony; for instance, coactivation of OT- and
DA-rich brain areas in response to infant stimuli [47,53], heightened VTA response to romantic
partner following OT administration [7], or increased coupling of peripheral biomarkers during
parental and romantic bonding [6]. This enables the subcortical system of motor ‘vigor’ to extract
Box 2. Time Sensitivity/Pulsatility of the Dopamine and Oxytocin Systems Enables Plasticity of Neural
Networks to Incorporate the New Attachment
Dopamine
Phasic DA striatal neurons process the timing of reward and encode reward anticipation, which builds the internal sense
of time in the brain [13]. Since DA neurons are sensitive to reward stemming from social interaction [26] and can link
reward to attachment experiences, they ground reward in cycles of caregiving actions. DA is implicated in circadian
timing and encoding the temporal component of experiences [60], which imbues attachments with sense of continuity
over time. Computations in striatal DA neurons, while not uniquely social, can integrate social components into their
temporal predictions, partly through OT's role in augmenting the salience of social stimuli [61]. This permits social signals
to act upon a pre-established synaptic tract and associate it with specific reward outcome [24]. It also enables an initial
brief, unselective, and broad increase in DA activity to become subjective and social, and function with accuracy, energy,
and specificity [13].
Oxytocin
Pulsatility is a defining feature of OT functionality across evolution [43,62]. OT is released from both OT-producing
hypothalamic neurons and dendrites, the branched projections of neurons, and this enables OT to operate at far
locations from OT-producing sites [178]. Dendritic release primes vesicle (small fluid-consisting structure within a cell)
stores for activity-dependent release and this enables a diffuse signal to maintain long half-life in the central nervous
system and extracellular fluid to execute far-reaching behavioral goals [179]. OT signals cause dendrite release without
increasing electrical activity, which, via peptidergic feedback, can become self-sustaining by creating autoregulated
release primed by salient experiences [180–183]. OT functions at both presynapsis and postsynapsis to attenuate
GABAergic inhibitory neurons, enlarging extracellular interactions among OT cells while reducing interactions with other
stimuli, which leads to synchronization across multiple brain areas [184–187]. Once activated, release is repeated in timesensitive
bursts. Special primed signals, such as attachment-specific cues, can trigger dendrite release, relocating OT in
vesicles from reserve to releasable stores [188,189] and future release is then shaped by the primed cue [190,191]. In
addition, OT participates in modifying the excitation-to-inhibition balance by causing GABAergic signaling to change from
excitatory to inhibitory around birth [192,193]. This opens a time window of increased neural sensitivity to specific
attachment cues (i.e., sensitive periods). Such time-sensitive mechanisms chart the way by which attachment experiences
impact the infant's OT release, the stimuli that will trigger it in future attachments, and its ultimate organization in
specific sites in the brain [2]. This is also how OT transmission, which is not between neurons but between populations of
neurons, can act across great distances and cause coherent, long-lasting, self-sustaining effects on behavior
[113,129,194].
84 Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2
from repeated attachment experiences the representation of love and transfer it to other bonds
throughout life, extending the neurobiology of maternal–infant bonding across human attachments
and beyond.
Time-Keeping Pulsatility
Another important feature of the neurobiology of attachment is the time sensitivity of both DA and
OT, which is critical for their role in neural plasticity. OT and (phasic) DA are characterized by
pulsatile release that supports time-keeping mechanisms implicated in patterned action and
seasonal rhythmicity. OT and DA are evolutionary-ancient systems involved in the regulation of
basic life functions across vertebrate evolution [57–59] (Figure 1). The pulsatility/time sensitivity of
OT and DA enabled their involvement in neural plasticity, which is required for selective
recognition and long-term memory, the two key features of human attachments.
Dopamine
While phasic DA striatal neurons encode for general reward and reward anticipation, these
neurons can incorporate social reward into their computations [13,26]. This lends support to the
hypothesis that attachment experiences, which are repeated and predictable in nature, may
become particularly salient targets for the reward computations of striatal DA neurons. The role
of DA in circadian rhythmicity [60] facilitates the consolidation of attachments, imbuing them with
a sense of regularity and stability. Studies in primates have shown that striatal DA neurons can
differentiate reward stemming from self and partner, anticipate predictable social interactions,
and draw reward from the matching of self and partner's actions [26]. It is thus assumed that the
temporal sensitivity of DA neurons enables humans to draw reward from the experience of
biobehavioral synchrony, which is built on familiarity with the partner's repeated social
patterns. Since OT increases the salience of social stimuli [61], the integration of OT and DA
in striatum enhances the experience of social synchrony, leading to cycles of coordinated
moments within attachment bonds that become rewarding and therefore repetitive, receiving
motivation and vigor from DA and social focus and tranquility from OT.
Oxytocin
Pulsatility is a defining feature of OT functionality across evolution, and myoactivity is OT's most
conserved feature [43,62]. Pulsatility is critical for the unique dendritic release that supports OT's
role in bonding (Box 2). This mode of functioning leads to autoregulated, feed-forward release
that is triggered by primed attachment experiences, which, once activated, release repeated
rhythmic bursts. Such time-sensitive mechanisms chart the way by which early attachment
experiences shape the ultimate organization of OT in specific sites in the infant's brain, the stimuli
that will trigger it in future attachments, and its cross-generational transfer via the expression of
parenting behavior in the next generation [2].
The molecular underpinnings of the time sensitive mechanisms for the two systems are
described in Box 2.
Mammalian Affiliative Bonds: Parents, Partners, and Peers
Attachment bonds are a defining feature of mammals. Pregnancy, birth, and lactation and their
underlying neurobiology define class mammalia [1,2,58,63,64]. Life for a young mammal begins
with two constraints; an immature brain at birth and the need for close proximity to a nursing
mother. Consequently, provisions embedded in the mother's body and the species-typical
maternal behaviors organize the immature brain, orienting it to social life via relationship with the
mother [65]. Networks supporting mammalian sociality develop in the context of the mother–
offspring bond and are shaped by variations in maternal care [4,66]. In the 3–5% of mammalian
species that are biparental, the father's presence and parenting behaviors also play a role in
infant brain development both directly and through their effect on reducing maternal stress [67].
Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2 85
The mother's body provides the first environment for the developing mammal. Maternal heart
rhythms, smell, touch, movement patterns, arousal dynamics, social cues, and stress
response mark the first environmental signals the brain encounters, programming it to live
in close proximity with others, signaling to the developing central nervous system the amount
of stress the environment contains [68,69], and tuning the brain to function as a ‘situated’
organ [70], constantly receiving information, updating predictions, and responding online to
the social world [71–73]. It has been recently argued [74] that the brain's modus operandi is
not solipsistic but situated and research on the ‘situated’ brain should become the focus of
social neuroscience. This position resonates with the central hypothesis proposed here, that
is, the social embeddedness of the immature mammalian brain at birth shapes it as a
fundamentally dialectic organ and that elucidating the mechanisms by which early attachments
program the brain may provide new understanding into the brain's basic mode of
action.
Attachment bonds are marked by two key features; they are selective (specific to attachment
target) and enduring (long-lasting) [37]. These two components underwent substantial reorganization
across mammalian evolution and specific combinations of their gradients define the
various human bonds (Figure 1). The human parent–offspring bond is selective and enduring.
Romantic bonds are also selective – at least in most cultures and recent human history – and
enduring, but more precarious; while humans rarely abandon their children, romantic attachments
can terminate under normative conditions and this may account for the tighter crosstalk of
the OT and reward systems during romantic bonding [6,75]. Close friendships are selective and
enduring, but these appear in a weaker form, with humans nurturing numerous friendships
simultaneously and long friendships dwindling with no overt breakup. Humans’ relationship to
conspecifics is neither selective nor enduring; yet humans are unique in their ability to activate the
behavioral and neurobiological systems of affiliation toward unfamiliar fellow humans. For
instance, humans express empathy or synchronize gaze with strangers and both activate
the OT system [76,77].
The ancient OT and DA systems foreshadow the selective and enduring features of mammalian
bonds. Across vertebrate evolution, the OT-family molecule has repurposed the basic life
functions controlled by the ancient vasotocin molecule in the service of social life, adapting it
to the social hierarchies, seasonality, and social organization of each species [59,78]. The
sensory–neurocircuitry coupling among group members in lower species, modulated by OT's
pulsatile release, transformed from group collaboration into the biobehavioral synchrony of
nursing mother and young in mammals [43]. The ancient DA system integrated repetitive motor
action with goal-directed reward via organization of the striatal–pallidal indirect network and the
evolution of GABAergic (inhibitory) control over motor neurons. Motor inhibition, a critical
component of any higher-order motor program [79], enabled the quiescence required for
the formation of attachment bonds.
Yet, as seen in Figure 1, humans’ selective and enduring bonds mark a long progress from their
ancient origins. The mother–offspring bond in rodents is nonselective and short lived; rodent
mothers care for any infant in their surrounding (bond to a generic infant) and bonds are bound to
the nest, primed by hormones of pregnancy, and depend on olfactory cues [1,10,80]. Within
these constraints, however, it is research in rodent mothers and monogamous prairie voles that
uncovered the cellular and molecular basis of the selective and enduring components of
attachment and charted commonalities between parental and pair bonds [10,81].
Primates’ enlarged neocortex enables the formation of selective attachments that rely on
complex social signals which are necessary for life in large groups [82,83]. The widespread
practice of alloparenting highlights the primates’ parental brain as an adaptive template that
86 Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2
can flexibly activate via bottom–up caregiving behavior [84,85]. Primates’ bonding is hormone
primed but not hormone dependent and olfactory cues are integrated into visually guided social
bonds [86]. Most primates, like rodents, are not monogamous and across both primates and
rodents, extended paternal care is observed only in monogamous species, indicating that male–
female mating and physical proximity are required to trigger the neurobiology of fathering [87,88].
This is in contrast to humans, for whom the paternal and pair bonds are independent [48]. As to
‘peers’, rodents [89] and primates [90] show behavioral and hormonal contingencies to distress
of a conspecific (member of the same species), such as elevation in cortisol or behavioral
mimicking, and cooperative breeding marmosets also display OT synchrony among childrearing
adults [91]. Peer-reared rhesus macaques, while exhibiting lifetime aberrations in social behavior,
express bonding to peers [92,93], indicating that friendshiplike behavior is common across
primate species.
Humans’ cortical complexity enables integration of the subcortical limbic network and ancient
OT and DA systems into love that is built on representations and memory, translates multisensory
experiences into higher-order associations, adapts to cultural norms to carry bonds across
generations and ground them in meaning systems, conceives both the overlapping and
autonomy of self and other [94], incorporates sociocognitive abilities of empathy and trust to
maintain long-term affiliations, and extends the here-and-now so that love can be felt in its
absence (e.g., deceased parents) and transcend to abstract ideas (God, homeland), humankind,
and other species (pets). Notably, all these forms of love activate the neurobiology of
affiliation [95–97] and are built on early attachment experiences [2,98,99]. Humans, as Wilson
recently noted [100], can create a feeling that life is meaningful by activating their affiliative biology
toward continuum of experience, from Earth's biosphere of flora and fauna to highest levels of
abstraction and the arts.
Biobehavioral Synchrony
Biobehavioral synchrony, the coordination of biological and behavioral processes between
attachment partners during social contact, is a critical component of human attachments
[1,2,25,101]. Biobehavioral synchrony evolved from the coordinated group activity of lower
species where joint motor action (involving DA) is locked with coupled physiology to achieve
survival-related collaborative goals (involving OT); for instance, ants carrying a grain of wheat to
shelter, fish swimming to ward off a shark, or birds flocking toward warmer climates
[1,2,37,102–104].
Life within social groups requires constant exchange of social signals among members and the
term ‘trophallaxis’ [95,105] has been coined by entomologists to denote the exchange of
sensory and social signals among members of a social group. Three aspects of trophallaxis have
been integrated into mammalian bonds: the low intensity and arousal-modulatory nature of
attachments, the social reciprocity and online construction embedded in them, and the trophallaxic
process as charting a line from parent–offspring bond to life within social groups [1]. Most
importantly, humans’ biobehavioral synchrony is straightforwardly built on trophallaxis in highly
social invertebrate species, such as ants.
Biobehavioral synchrony is observed across human attachments, in parental, romantic, friendship,
and fellow–human interactions, and employs great flexibility so that human synchrony is not
metronome precise but unfolds a stochastic process, follows dynamic systems’ principles, and
integrates patterned order and local variability [106,107]. The basic characteristics of biobehavioral
synchrony, however, are maintained across evolution; it involves the coordination of
biological processes and species-typical behaviors expressed during social contact, it initiates
young to life in social groups, it assembles online from the inputs of multiple parties, and it relies
on the ancient OT system [37,101].
Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2 87
During or immediately following social contact, human synchrony is evident in four systems:
behavior, autonomic, hormones, and brain, and, to varying degrees, this coupling is found
across the four human attachment constellations (Figure 2). Synchrony between partners’
nonverbal behaviors in the gaze, affect, vocal, and touch modalities has been observed in
mother–infant interactions since the 1950s and thought to entrain the neonate's physiological
periodicities of sucking, crying, and circadian rhythmicity [108,109]. Fathers similarly engage in
behavioral synchrony, but utilize a quick-paced, high-arousal temporal pattern [110]. Synchronous
parent–infant interactions are accompanied by physiological coordination [2,5,101,111];
parent and infant's heart rhythms are coupled during episodes of behavioral synchrony, but not
during nonsynchronous moments [112]; and following synchronous interactions, OT release is
coordinated between parent and child [113]. Synchronous moments induce brain-to-brain
coupling between mother and child in key nodes of the social brain.
Synchronous interactions experienced during early sensitive periods are expressed in later
attachments throughout life. Matched interactions are observed between romantic partners and
show similar second-by-second coordination of gaze and affect [6,114]. Heart-rate coordination
[115], OT coupling [116], and brain-to-brain synchrony have been described among couples.
Mother and father show a coordinated brain response in structures of the embodied simulation
and mentalizing networks (STS, IPL, and AI) when viewing a video of their own infant [117].
Interactions among close friends show behavioral reciprocity; however, interactions among
friends are not as tightly coupled as those observed in parental or romantic attachment [55,118].
Evidence suggests that OT increases following contact with friends, albeit the increase is not
coupled [55]. Finally, teams trained for coordinated action and group cohesion, such as military
units, exhibit wide response across the social brain in the alpha band to vignettes depicting
synchronous group activities, particularly coordinated unit in battle [119].
Unlike other mammals which require familiarity with conspecific for biobehavioral coordination,
humans display behavioral synchrony toward strangers; humans coordinate gaze and vocal
turn-taking during conversations with strangers while touch synchrony is preserved for intimate
bonds [1]. When strangers sit in close proximity and execute joint tasks, they also display heartrate
coupling, brain-to-brain synchrony of alpha rhythms, and coordinated brain response in
temporoparietal structures, such as STS and IPL [120–122]. Empathy to strangers in distress is
impacted by OT administration and observing groups in collaborative action elicits OT response
[119]. Furthermore, the brain responds to ‘similar to me’ synchronous action; mothers observing
synchronous interactions of unfamiliar mothers and their infants activate areas of the reward
system (NA, dorsal ACC), and the degree of activation parallels their own behavioral synchrony
[123]. Finally, evidence highlights humans’ preference for synchrony in large crowds in walking,
marching, or rowing [124]. Such group-maintaining mechanisms are rooted in earliest mammalian
experiences – the matching of physiology and behavior between mother and young
generalized by humans’ large associative cortex across time, place, and person.
Longitudinal studies show long-term associations between the degree of parent–infant synchrony
and the quality of later attachments with close friends and romantic partners and with
abilities that support participation in human social life, including empathy, moral orientation,
theory-of-mind, and culture-specific modes of self-regulation [125–127]. Early synchronous
interactions also shape children's social brain. For instance, parent–infant synchrony longitudinally
predicts intactness of the brain basis of empathy in adolescence [128]. Similarly, parents’
brain response to infant cues is combined with behavioral synchrony to predict preschoolers’
emotion regulation and socialization [129], and parental OT integrates with parent–infant
synchrony to shape children's social reciprocity toward best friends [55]. These studies demonstrate
that the parent's affiliative neurobiology and synchronous behavior shape human
children's attachments to nonparental figures and buttress human-specific social
88 Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2
Biobehavioral synchrony in human aƩachments
Behavioral
synchrony
• Synchronized
behavior in gaze,
affect, vocal, and
touch
• Mother-specific
father-specific
• CoordinaƟon of
brain response in
mentalizing
network in parents
• CoordinaƟon of
gamma oscillaƟons
in temporal cortex
in lovers
• Synchronized HR
during synchronized
interacƟons
• HR coordinaƟon
during or following
interacƟon
• CoordinaƟon of
OT and corƟsol
among parents
• CoordinaƟon of
OT among lovers
• Teams coordinate
heart rythms during
joint acƟon
• OT is released
during interacƟons
with friends
• Alpha response to
behavioral
synchrony among
teams in social
brain
• CoordinaƟon
among teams in
mirror network
• Evidence for
coordinated
acƟvaƟon in
mentalizing areas
during interacƟon
• No evidence for
coupling
• OT is implicated
in acts of empathy
• No evidence for
coupling
• Evidence for some
coordinaƟon during
joint acƟon in close
proximity
• Synchronized
nonverbal paƩerns
• Coordinated
self-disclosure +
empathy
• PaƩerns of social
reciprocity
• CoordinaƟon of
culture-spcific
display rules
(e.g., eye gaze)
• Coordinated OT
response following
contact
• Coordinated brain
oscillaƟons in alpha
and gamma rythms
• Coordinated corƟsol
response to stress
Parents
RomanƟc
partners
Friends
Strangers
Heart rate
coupling
Endocrine fit Brain-to-brain
synchrony
Figure 2. Biobehavioral Synchrony in Human Attachments. Human attachments are characterized by the coupling of the partners’ physiological and behavioral
processes during moments of social contact. Such coupling is observed across four systems: matching of nonverbal behavior, coupling of heart rhythms and autonomic
functioning, coordination of hormonal release, and brain-to-brain synchrony. In humans, biobehavioral synchrony is observed in the four affiliative bond constellations:
parental, romantic, friendship, and strangers. Abbreviations: HR, heart rate; OT, oxytocin.
Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2 89
competencies, highlighting the lifetime effects of the neurobiology of human attachment and its
cross-generational nature.
Notably, our focus on the OT system stems from its critical role in the formation and maintenance
of attachment bonds in humans and other mammals. Other hormones, including cortisol,
testosterone, prolactin, progesterone, vasopressin, beta-endorphin, and estradiol, have been
studied in relation to human attachments. Our hypothesis, supported by studies from our
laboratory [1], suggests that OT serves a key integrative function by providing a neuroendocrine
milieu for the effects of multiple hormones on the development of human attachments.
The various measures used in research on human attachments are described in Box 3.
Human Attachments and the Brain
Humans’ rootedness in mammalian affiliative biology renders the integration of OT and DA in
striatum an important foundation for human attachment, albeit the role of other neurohormonal
and neurotransmitter systems has been described [9,10,81]. Recently, fMRI studies began to
test the neural basis of humans’ multiple attachments by assessing brain responses to auditory,
Box 3. The ‘Measurement of Love’
Neuroscience research has utilized the following tools to measure human attachments:
Micro/macroanalysis of social behavior and behavioral synchrony: Observation of interactions between mothers and
infants and among couples has been conducted for nearly a century. Studies use either global rating scales addressing
the quality of the partners’ behaviors (e.g., ‘responsive’, ‘intrusive’) or focus on micro-level detection of bonding-related
behaviors (e.g., ‘motherese’ vocalizations, social gazing) and their coordination among partners [98]. Studies employed
similar micro- and macro-level analysis in other attachments, including romantic/marital relationships and friendships.
Autonomic response: Parenting and couple studies employed measures of heart period and respiratory sinus arrhythmia
as indices of parasympathetic functioning during social interactions, evaluating changes from baseline and during various
dyadic stressors (e.g., parent–infant ‘still-face’, couples ‘conflict dialog’). Skin conductance has been used to index
sympathetic activity and multiple autonomic measures have been integrated into a single index of autonomic arousal
[195,196].
Hormones: Peripheral measures of hormones from plasma, saliva, urine, and, less commonly, from cerebrospinal fluid,
have been tested as correlates of human attachment bonds. Hormones studied in attachment contexts mainly include
cortisol, testosterone, oxytocin, vasopressin, prolactin, progesterone, estradiol, salivary alpha amylase, and beta
endorphin.
Peptide administration: Nasal administration of OT and, to a lesser extent, vasopressin has been used to address the
effects of neuropeptides on affiliative response and the brain networks supporting human social abilities. Studies typically
employ a double-blind design where peptide administration is compared with placebo in a within-subject or betweensubject
design [197].
Brain oscillations: Electroencephalogram and emerging studies in MEG have been used to examine questions related to
bond formation and social affiliation, in addition to understanding the role of brain oscillations in human social functions
[119,128,174]. Research on brain oscillations and their cortical generators afforded by MEG can open new vistas on the
neurobiology of attachment.
Brain imaging: fMRI has been recently used to address various aspects of human attachments and these studies are
summarized in the Supplemental Information online. Studies often use auditory, visual, or multimodal stimuli of the
attachment partner (infant, romantic partner) as fMRI stimuli.
Genetics/Epigenetics: Individual differences related to allelic variability on genes related to the oxytocin–vasopressin
pathway (OXTR, AVPR1a), dopamine (DRD4, DRD2, DAT1, COMT), or serotonin (5-HTT) have been used to examine
genetic markers associated with individual differences in attachment behavior or the effects of various early attachment
experiences on later functioning. Recent studies have also tested methylation on the OXTR gene in relation to
attachment-related outcomes [43].
90 Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2
(A) Straitum detailed view
NAcc
PFC
IPLSTGpre-SMAdACC
CA
MFG
FP
NAcc
IFG
AI AMG
CA
PC
SMA
IFG
OFC AI TP
IPL
TPJ
STS
mPFC ACC
PCC
STR
VTA
vmPFC OFC AMG
Reward
Key:
Embodied simulaƟon
Mentalizing
PCC
TPJ
THAL
VTA
dmPFC
ACC
mPFC
NAcc
vmPFC
HT
OFC rACC AMG
PHG
Parental
RomanƟc
Friendship
Parental
Pair bonds
GP STS
GP CA VP AMG Pu HPC
Human aƩachment networksSagiƩal plane
(B)
(C)
(See figure legend on the bottom of the next page.)
Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2 91
visual, or multimodal stimuli of the attachment target; for example, infants to their parents,
romantic partners, or friends. Overall, various findings indicate that while the VTA/ventral striatum
ignites the brain's experience of attachment and imbues it with reward and vigor, human
attachments integrate subcortical with multiple cortical reward- and sociocognitive-related
networks (Figure 3).
A survey of published studies using fMRI to investigate humans’ various social attachments (see
the Supplemental Information online for more details) provides evidence for three main interconnected
neural systems that integrate to establish, maintain, and enhance our affiliative bonds
with others. Some brain areas participate in more than one system.
The first is the ‘reward-motivation’ system, including the striatum (NA, caudate, putamen),
amygdala, VTA, OFC, ventromedial prefrontal cortex (vmPFC), and ACC, employing DA- and
OT-rich pathways [12,130,131], and supporting multiple attachment-related motivational
behaviors, such as social orienting, social seeking, and maintaining contact across extended
periods [132,133]. Attachments have intrinsic motivational value that combines immediate
hedonic response with approach motivation, goal-directed behavior, and learning [134]. The
striatum and its massive projections from both frontal cortex and amygdala [130,135,136] are
implicated in detecting attachment-relevant cues, appraising their valence, and guiding action by
coding the affective properties of stimuli [137–139]. Notably, even within the striatum there is a
shift from ventral (NA) to dorsal striatum (caudate) in corticostriatal connectivity with the
stabilization of the bond [140,141], reflecting a shift from reward-related drive and novelty
seeking to familiarity processing and predictability [142,143]. Caudate–cortical connectivity is
associated less with passion, sexual desire, or parental response to vulnerable infants but with
long-term relationships, habit formation, and companionship among couples [141], and social
cooperation and trust among friends [144]. The caudate is involved in reinforcement learning,
goal-directed action, and weighing the relative values of outcomes [135,145] and authors
suggest that the shift from ventral to dorsal striatal functioning accompanies attachments as
they settle into joint goals, mutual habitat, and reciprocity, and is mediated by OT [140]. The
existence of convergent projections from the cortex to striatum, along with hippocampal and
amygdala-striatal projections, places the striatum as a central entry port for processing emotional/motivational
information supporting human attachments.
The amygdala and its associated network play a critical role in human attachment, particularly
mothering [5,10,146] and romantic attachment [88]. Maternal bonding requires vigilance for
infant safety and romantic attachment involves heightened emotionality and interoceptive
sensitivity to signs of safety and danger. Amygdala activations have been detected in ‘all’
imaging studies of mothers [5] and in most studies of fathers, romantic partners, and close
Figure 3. The Brain Basis of Human Attachments. (A) Connections among subcortical and cortical structures supporting attachment in the human brain are
indicated by solid green lines for parent–infant bonds, red lines for romantic bonds, and broken blue lines for suggested connections in friendship bonds (taken from 86
fMRI papers on humans’ various social attachments, see the Supplemental Information online for details of each study). Neural models for parental care in rats are
indicated by broken black lines and for pair bonding formation in prairie voles by dotted black lines [10,19,80]. (B) The basal ganglia intraconnections (striatum: NA, Pu,
CA; VP; and GP) and interconnections with cortical structures (PFC) and subcortical structures (AMG and HPC). (C) The human affiliation networks. Three main
interconnected neural systems underpinning human attachments (some areas participate in more than one system). The reward network (broken lines/pink colored),
supporting approach motivation, social orienting and seeking, goal-directed behavior, social learning, and the incentive value of attachment cues [134], includes the
striatum, OFC, ACC, vmPFC, VTA, and AMG. The embodied simulation network (broken lines/green colored) enables individuals to resonate with other's mental state
and emotion via embodiment mechanisms and grounds experience in the present moment [94] and includes the AI, ACC, IFG, IPL, and SMA. The mentalizing network
(dotted/bright blue colored), supporting social cognition, mental-state understanding, and social goal interpretation [164], comprises frontotemporal–parietal regions
including the STS, PCC, TPJ, TP, and mPFC. Abbreviations: ACC, anterior cingulated cortex; AI, anterior insula; AMG, amygdala; CA, caudate; CT, cortisol; dACC, dorsal
anterior cingulated cortex; GP, globus pallidus; HPC, hippocampus; HT, hypothalamus; IFG, inferior frontal gyrus; IPL, inferior parietal lobule; MFG, middle frontal gyrus;
NA, nucleus accumbens; OFC, orbitofrontal cortex; PC, precuneus; PCC, posterior cingulated cortex; PFC, prefrontal cortex; PHG, parahippocampal gyrus; Pu,
putamen; rACC, rostral anterior cingulated cortex; SMA, supplementary motor area; STG, superior temporal gyrus; STS, superior temporal sulcus; TP, temporal pole;
TPJ, temporoparietal junction; THAL, thalamus; vmPFC, ventromedial PFC; VP, ventral pallidum; VTA, ventral tegmental area.
92 Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2
friends. The amygdala guides attention to biologically relevant stimuli, adjusts social orienting,
codes the intensity of reward, and computes the salience of social information [147,148].
Interestingly, amygdala activation in human attachments is typically coupled with other areas
of the subcortical limbic circuit (hypothalamus, VTA, VP), insular–cingulate cortices, and temporal–frontal
areas [STS, superior temporal gyrus, prefrontal cortex (PFC)] [47,129,149].
Human attachments require complex higher-order processes that involve learning, memory,
planning, and predictions and depend on frontostriatal connections of the reward circuit,
particularly vmPFC, OFC, and ACC. These connections enable the encoding of reward-related
expectations, associations, and representations; evaluation of the affective valence of attachment
stimuli; and maintenance of flexible representations to guide action [150,151]. Such
corticostriatal connections provide the foundation for the human capacity to combine reward,
passion, proximity seeking, ‘vigor’, and unconscious motivation with higher-order abilities that
mark the top–down control, trust, empathy, and commitment of human attachments and enable
humans to tend and maintain them. The OFC, the latest evolving structure of the human brain
and the end point of the reward pathway [152], implicates in the representation of ‘pleasantness’
and in effortful, goal-directed actions to tend long-term relationships [153]. The OFC selects
among rewards, enables the resistance of immediate rewards toward long-term attachment
goals, and shapes affiliations in the color of culture, ritual, and personal preferences with stability
and far-sightedness [154]. The vmPFC enables representation of love and its entire ‘ripples’ of
associations, sense of ‘yearning’ that is critical for human love (maintaining love in its absence),
the appraisal of safety, and the sense of self as both overlapping and separate from attachment
partner, an overlap that defines the experience of intersubjectivity [155,156]. The vmPFC exerts
inhibitory control over limbic regions, reducing anxiety/avoidance in safe environments and longterm
attachments [157].
The second system underpinning human attachment is the ‘embodied simulation/empathy
network’, including the insula, ACC, IFG, IPL, and SMA. Embodied simulation is an evolutionaryancient
mechanism, which, via automatic interoception and internal representations, recreates
other's state in one's brain. Embodied simulation is critical for grounding a ‘shared world’ in the
brain and underpins the human capacity to build and maintain attachments [94,158]. This form
of interpersonal ‘matching’ relies on neural pathways that involve both the experience of internal
body formats and the perception of similar states in others via perceptual–motor coupling
[120,159]. This network enables the parent/partner to integrate interoceptive and affective
information, resonate with mental states and emotions, and ground experience in the present
moment thus giving it color, immediacy, and ‘situatedness’ [160,161]. von Economo neurons,
projection neurons located in layer V of the anterior cingulate and frontoinsular cortices, are
implicated in the conscious perception of bodily states and afford the integrated representations
of social moments as they are lived [162,163].
Finally, interoceptive mechanisms are insufficient to support representation-based human
attachments. Human bonds rely on ‘mentalizing’ processes – higher-order cognitive processes
involving complex top–down inferences of others’ mental states by attributing beliefs, thoughts,
and intentions to others to create a full sense of ‘togetherness’ [164,165]. Mentalizing processes
underpin attachment formation by building on the individual's ability to appreciate multiple
perspectives, understand partner's goals and motives, and keep in mind his/her values and
concerns [74,166]. Frontotemporal–parietal structures, particularly the STS, posterior cingulated
cortex, TPJ, temporal pole, and mPFC, are components of the ‘mentalizing system’, the
third network of the ‘global human attachment network’ (Figure 3). The STS and TPJ are central
regions of this network [167] and play a vital role in social cognition [164], evaluation of others’
state, social goal interpretation, and prediction making and their online updating [168–170]. The
STS combines embodied simulation (mirror) and mentalizing properties [171], integrates fast
Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2 93
bottom–up simulations (biological motion) with slower top–down understanding (theory-ofmind),
and provides critical support for the process of attachment formation [172]. Interestingly,
the STS has been shown as particularly relevant to the development of fathering, a bond built
more on top–down understanding of infant signals than on the ancient limbic structures that
support mothering [48].
Finally, research is beginning to use magnetoencephalography (MEG) to study the participation
of neural oscillations and their cortical generators in human attachments. Overall, it has been
suggested [70,74] that brain oscillations underpin brain-to-brain synchrony among attachment
partners or between humans during social interactions and participate in binding members into
a social group. In several recent studies, my colleagues and I detected the involvement of alpha
(8–14 Hz) and gamma (30–60 Hz) rhythms in human bonding, the two frequencies defining top–
down control mechanisms and bottom–up rapid processing, respectively, with gamma rhythms
often integrating into alpha to create the interplay of automaticity and control needed for bond
formation [173]. We found that empathy to others’ pain is supported by alpha rhythms in
mentalizing structures [174]; that adolescents exposed to maternal depression across the first
years of life terminate alpha response in posterior STS at a late time window (900–1100 s
poststimulus), suggesting aborted top–down processing of empathic resonance [128]; and that
brain-to-brain synchrony of alpha rhythms in SMA (embodied simulation) binds members of a
group and differentiates them from the outgroup [167]. Importantly, MEG studies of human
attachment are rare and may provide valuable information on the temporal course of the brain
response to attachment-related cues.
Concluding Remarks and Future Directions
Can the scientific measurement of love and research on the ‘affiliative brain’ (Box 3; see
Outstanding Questions) open new vistas not only for understanding human attachments but
also for neuroscience in general? I submit that the answer is affirmative for three reasons.
First, when humans are asked about the most important aspect of their life, they often describe
their affiliations. The capacity to give and receive love and maintain long-term bonds is increasingly
recognized as key to human thriving, impacting well-being, positive outlook in the face of
adversity, physical health, and better aging [175]. Yet, we still know relatively little about the
mechanisms by which social bonds impact our immune system, express throughout the life
span, predict better aging, or transmit from parent to offspring. Knowledge is also limited as to
how two humans coordinate their brain response online during social interactions and how early
experiences longitudinally tune the brain to social life. A better understanding of the neurobiology
of affiliation can shed light on how to live a personally meaningful life, as well as how we might
repair developmental and affiliative disruptions, as can occur in cases of maternal postpartum
depression, premature birth, or impoverished or dangerous environments where the social
envelop provides no safe haven for proper bonding.
Second, the flip side of the neurobiology of affiliation is the neurobiology of intergroup conflict,
racial bias, and tribal hatred, both activating the same ancient systems, which evolved to help
organisms rapidly distinguish friend from foe [77]. It is critical we understand how the brain shuts
down its empathic response when the inflicted is a member of the ‘outgroup’, particularly
outgroup perceived as potentially threatening. We recently found that shutting down the brain's
empathy centers is accomplished by tightening brain-to-brain synchrony among ingroup
members, increasing OT production, and imposing top–down attenuating processes on bottom–up
automatic response to the distress of outgroup [77,167].
Finally, the neurobiology of affiliation stands at the crossroad between science and humanities,
with the potential to provide deeper integration of the two after centuries of separation into
Outstanding Questions
Can the neurobiology of attachment
provide insights into the mechanisms
that support brain-to-brain coordination
among humans during social contact
and foster the transition from a
‘solipsistic’ to a ‘situated’ model of
the human brain?
Can knowledge on the neurobiology of
attachment help understand the ‘neurobiology
of reparation’: what processes
enable humans to thrive after
disrupted early attachments? Which
individuals are better disposed to
reparation following deficits in early
bonding? And what components must
still exist in the early environment to
make reparation possible?
Can the ‘measurement of love’ integrate
as a valid area of scientific
inquiry? Can we develop novel tools
and formulate new models?
How do cultural ecologies and meaning
systems shape the neurobiology of
attachment? Can conditions such as
nuclear versus extended family living,
traditional versus modern mate selection,
or monogamous versus open
partner relationships impact brain and
endocrine systems implicated in
bonding?
What are the lifetime effects of human
attachments on health, well-being, and
happiness? What are the processes by
which attachment bonds exert their
impact on health and longevity?
Can the neurobiology of attachment
provide a unique entry point for the
integration of science with the humanities,
arts, ethics, and clinical wisdom?
94 Trends in Cognitive Sciences, February 2017, Vol. 21, No. 2
distinct branches of knowledge. While Aristotle and Leonardo De Vinci were well-versed in both
the sciences and arts of their period, such integration is no longer available or encouraged. The
neurobiology of human affiliation requires that a biologically based evolutionary perspective,
which provides mechanistic understanding but pays little attention to the individual, is supplemented
by perspectives that focus precisely on the individual with his or her experiences,
expressions, and aspirations, and are committed to the individual's well-being, health, and
thriving. To study the neurobiology of human attachment, one must season the objectivity of
science with the wisdom of the clinician, foresight of the philosopher, and creativity of the artist
into a unified endeavor that can shed new light on the loftiest – and oldest – of human
experiences: ‘love’
Acknowledgments
Supported by the Simms-Mann Foundation and the Irving B. Harris Foundation. I wish to express my deepest gratitude to
Eyal Abraham for his hard work, insights, and wisdom, and to Maayan Harel for her exceptional talent and dedication in
creating the graphic work.
Supplemental Information
Supplemental information related to this article can be found, in the online version, at http://dx.doi.org/10.1016/j.tics.2016.
11.007.
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