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Toward a Neuroscience of Attachment



Neurobiological studies of attachment are either abundant or scarce, depending on one's research tradition and scientific understanding of the term "attachment." On the one hand, the past two decades have seen a great deal of nonhuman animal work detailing the various neural manifestations of social bonding, familiarity, affiliation, caregiving, and other behaviors that can (and often do) fall under the general rubric of "attachment." On the other hand, neuroscientific investigations of normative attachment in humans have been limited and slow to develop, and similar investigations of the neural circuits supporting, or even associated with, individual differences in attachment (e.g., secure, anxious, avoidant, in the social psychology tradition; autonomous, preoccupied, and dismissing, in the clinical and developmental tradition; see Crowell & Fraley, Chapter 26, this volume) are exceedingly rare. These facts (and a cursory glance at the table of contents for this volume) underscore the complexity of attachment as a domain of inquiry, and suggest that, at present, any neuroscience of attachment is likely to strike some as limited in both empirical foundation and theoretical scope. Nevertheless, it is important to make a beginning somewhere, and a neuroscience of attachment has much to gain from the integration of multiple research perspectives. Following Bowlby (1969/1982) and Ainsworth (1989), attachment bonds are considered in the present chapter to be those characterized by a high frequency of close proximity to the putative "attachment figure," especially during times of emotional stress. Moreover, attachment relationships are considered in this chapter to serve regulatory functions, often in relation to basic physiological needs, but also with respect to many forms of emotional responding.
2nd Edition
Pages 241 - 265
The Guilford Press, NY
James A. Coan
University of Virginia
University of Virginia, Department of Psychology, 102 Gilmer Hall PO Box 400400, Charlottesville, VA 22904
telephone: 434-243-2322 email:
Neurobiological studies of attachment are
either abundant or scarce, depending on one’s
research tradition and scientific understanding
of the term “attachment. On the one hand,
the past two decades have seen a great deal of
nonhuman animal work detailing the various
neural manifestations of social bonding, famili-
arity, affiliation, caregiving, and other behaviors
that can (and often do) fall under the general
rubric of “attachment.” On the other hand,
neuroscientific investigations of normative at-
tachment in humans have been limited and
slow to develop, and similar investigations of
the neural circuits supporting, or even associ-
ated with, individual differences in attachment
(e.g., secure, anxious, avoidant, in the social
psychology tradition; autonomous, preoccu-
pied, and dismissing, in the clinical and devel-
opmental tradition; see Crowell & Fraley, Chap-
ter 26, this volume) are exceedingly rare. These
facts (and a cursory glance at the table of con-
tents for this volume) underscore the complex-
ity of attachment as a domain of inquiry, and
suggest that, at present, any neuroscience of
attachment is likely to strike some as limited in
both empirical foundation and theoretical
Nevertheless, it is important to make a begin-
ning somewhere, and a neuroscience of at-
tachment has much to gain from the integra-
tion of multiple research perspectives. Follow-
ing Bowlby (1969/1982) and Ainsworth (1989),
attachment bonds are considered in the present
chapter to be those characterized by a high fre-
quency of close proximity to the putative “at-
tachment figure,” especially during times of
emotional stress. Moreover, attachment rela-
tionships are considered in this chapter to serve
regulatory functions, often in relation to basic
Coan!Toward a Neuroscience of Attachment
Toward a Neuroscience of Attachment
James A Coan
University of Virginia
physiological needs, but also with respect to
many forms of emotional responding. These
regulatory functions are social insofar as they
result from interaction with conspecifics (other
members of the same species). Some of the
regulatory functions of attachment relation-
ships are obvious and fundamental. For exam-
ple, human infants literally cannot survive
without the assistance of an adult caregiver. In
later childhood, however, and in adult attach-
ment relationships, emotion becomes the pri-
mary target of social regulation (Mikulincer &
Shaver, Chapter 23, this volume). A major
source of interest here is that the likely mecha-
nism underlying the well-known link between
social contact and health is the social regulation
of emotion, particularly the social regulation of
threat responding. The social regulation of
threat responding is itself a major feature of
attachment (Carter & DeVries, 1999; Edens,
Larkin, & Abel, 1992; Hofer, 1995).
A large literature now suggests that a range of
interactive social behaviors target physiological
systems, temperamental dispositions, and overt
behaviors associated with the stress response
(Berscheid, 2003; Diamond, 2001; Sapolsky,
1998; Uchino, Cacioppo, & Kiecolt-Glaser,
1996). For example, supportive social behaviors
are known to attenuate stress-related activity in
the autonomic nervous system (ANS) and the
hypothalamic-pituitary-adrenal (HPA) axis
(Boccia, Reite, & Laudenslager, 1989; Flinn &
England, 1997; Lewis & Ramsay, 1999; Weiss,
1990; Wiedenmayer, Magarinos, McEwen, &
Barr, 2003). Maternal grooming behaviors af-
fect glucocorticoid receptor gene expression
underlying hippocampal and HPA-axis stress
reactivity in rat pups (Weaver et al., 2004). In
the context of a novel, mildly stressful new en-
vironment, rats in the company of a familiar
companion engage in more exploration and
play-soliciting behavior compared to rats in the
company of an unfamiliar companion (Terra-
nova, Cirulli, & Laviola, 1999).
Theorists have long argued that social bonding
serves security-provision and distress-
alleviation regulatory functions with respect to
negative affect and arousal (Bowlby, 1973;
Mikulincer, Shaver, & Pereg, 2003). Prominent
evolutionary theorists dating to Darwin have
even argued that because mammalian emo-
tional responding evolved in a social context,
emotional behavior is virtually inextricable
from social behavior (Brewer & Caporeal, 1990;
Buss & Kenrick, 1998; Darwin, 1872/1998).
These diverse perspectives and literatures sug-
gest that any robust conception of attachment
will include multiple, distributed subsystems
including (but probably not limited to) those
devoted to emotion, motivation, emotion regu-
lation, and social affiliation.
The promise of the emerging field of what we
can here consider to be “attachment neurosci-
ence” is at once to provide critical information
about how the brain supports attachment be-
haviors and to forge links between research
traditions as diverse as the basic neurosciences,
behavioral ecology, and various subdomains of
psychology such as developmental, social, and
clinical, as well as affective science. In this
chapter, the neural systems supporting emo-
tion, motivation, emotion regulation, and social
behavior are first reviewed. Following this, the
social regulation of emotion and individual dif-
ference in attachment behavior will be consid-
ered from the perspective of behavioral neuro-
science. Based on these reviews, the social base-
line model of social affect regulation will be
proposed. The social baseline model uses a
neuroscientific framework to integrate models
of attachment with a neuroscientific principle,
economy of action, in the management of
metabolic resources devoted to emotional and
social behavior. Finally, recommendations are
made for the development of a robust future
neuroscience of attachment.
Coan!Toward a Neuroscience of Attachment
Attachment as a Neural Construct
Although attachment bonds are widely believed
to result from a universal, innate “attachment
behavioral system,” attempts to locate a single,
dedicated attachment circuit are likely to be, to
paraphrase Wittgenstein, a bit like trying to find
the real artichoke by peeling away all its leaves.
Almost any interpretation of the attachment
behavioral system reveals it to be a higher order
construct comprised of constituent behaviors
about which a great deal is known, even at the
neural level (Fox & Hane, Chapter 10, this vol-
ume; Polan & Hofer, Chapter 7, this volume).
For example, many studies have addressed the
neurobiology of social behaviors such as rec-
ognition and familiarity, proximity seeking,
separation distress, soothing behaviors, and ma-
ternal caregiving. Thus, one of the goals of this
chapter is to introduce the neuroscientific study
of attachment from the perspective of what is
currently known about its social and emotional
A corollary goal is to move toward bridging
two broad, rigorous, productive, and unfortu-
nately disparate literatures. One is a thriving
animal literature dedicated to what is variously
termed “social bonding,” “pair bonding, and
“attachment bonding.” The other contains a
vast body of research on human attachment
behavior, including studies of individual differ-
ences in internal working models of attachment
(reviewed in Mikulincer & Shaver, 2007, and in
J. Feeney, Chapter 21, this volume). Tradition-
ally, these two worlds have had little to say to
each other—a reflection of their starkly differ-
ent research strategies as much as their differ-
ent subject populations. Animal models, partly
by virtue of what is ethically permissible with
the population, often emphasize the study of
social processes in terms of specific causal neu-
ral structures, circuits, neurotransmitters, neu-
ropeptides, pheromones, or hormones. At-
tachment relationships are defined observa-
tionally, by the presence of separation distress
or physiological soothing as a function of close
proximity, or both. By contrast, social, clinical,
and developmental psychologists often focus
their efforts on “behavioral systems,” seeking
to understand how humans behave in and, im-
portantly, what they have to say about, rela-
tional contexts.
This is not to say that research on attachment
in humans has not utilized physiological meas-
urement. On the contrary, psychologists have
used measures of autonomic physiology, elec-
troencephalography (EEG), glucocorticoid lev-
els, and, more recently, functional magnetic
resonance imaging (fMRI). These measures
have provided valuable insights into human
social behavior, but they are rarely capable of
identifying causal brain- behavior relationships
(Norris, Coan, & Johnstone, 2007), and their
frequent dependence on self-report measures
(including coded interviews) may result in neu-
robiological correlates that are quite distinct
from those of behaviorally defined animal
models (cf. Williamson, 2006).
Yet another difficulty presents itself in bridging
these literatures. Even if the definitions of at-
tachment were perfectly matched and each neu-
ral measure applied to humans and non- human
animals were identical, the neural processes as-
sociated with attachment behaviors in non-
human animals may not generalize perfectly to
those in humans. Work on the social communi-
cation value of pheromones provides an excel-
lent example of this point. Pheromones are
chemical substances that convey information
between members of the same species (Insel &
Fernald, 2004). It is certain that nearly all ani-
mals, including humans, show at least some
evidence of two distinct olfactory systems. The
primary olfactory system is dedicated to the
detection of odors that convey information
about food or the presence or predators, and
this system is most commonly associated with
the sense of smell. By contrast, the accessory
Coan!Toward a Neuroscience of Attachment
olfactory system is, in many species, dedicated
to the detection of specific pheromonal infor-
mation. This accessory olfactory system con-
sists of the vomeronasal organ (VNO) and the
accessory olfactory bulb (AOB). Pheromones
make contact with the VNO, exciting
pheromone-specific sensory neurons projecting
to the AOB.
In a wide variety of species, this system is ca-
pable of providing rapid and powerful infor-
mation about sex, reproductive capacity, mate
location, territorial boundaries, and even social
status (Insel & Fernald, 2004). Nevertheless,
the strongest of these findings derive exclu-
sively from studies of animal populations, and
after a great deal of initial excitement about the
possibility of a human pheromone system, en-
thusiasm has waned significantly amid evidence
that, although there does appear to be a human
VNO, (a) there is no obvious pheromone-
specific sensory neuron associated with it; (b)
vomeronasal receptor genes present in the hu-
man genome appear to be pseudogenes (genes
that have lost their protein-coding ability); and
(c) the AOB does not appear to exist at all in
the brains of adult humans (Meredith, 2001).
In other words, the VNO—the primary and
best-understood mechanism of socially critical
pheromonal communication in animals—ap-
pears to be vestigial in humans.
Interestingly, evidence does suggest that chemi-
cal communication between humans can occur
(e.g., Jacob & McClintock, 2000). However, un-
like so many social species, the extent to which
such effects are pheromonal, and whether they
have anything whatever to do with the VNO, is
uncertain at best. It is more likely that odors
can moderate social information in humans,
and that they do so through a distinct mecha-
nism that is as yet poorly defined and under-
stood (Meredith, 2001).
Despite all of these cautions, it is clear that re-
search on animals has yielded invaluable infor-
mation about the neurobiology of attachment,
without which any understanding of human
attachment would, at the neural level, be se-
verely impoverished. Moreover, advanced neu-
roimaging techniques such as high density
EEG, positron emission tomography (PET),
transcranial magnetic stimulation (TMS), and
functional magnetic resonance imaging (fMRI)
promise access to human neural processes at a
level of detail undreamed of until the very end
of the 20th century. Hence the potential for
building bridges between the animal and hu-
man attachment literatures is higher than it has
ever been. FMRI studies in particular are, by
virtue of their rapid proliferation and relative
lack of invasiveness, beginning to supply pieces
of the human social bonding puzzle that will
compliment anatomical and molecular work in
animals. Such advances promise the formation
of a more comprehensive neuroscience of at-
The Neural Constituents of
Neural systems supporting attachment are
likely to include, at a minimum, those underly-
ing incentive motivation, certain forms of emo-
tional responding, emotion regulation, and dis-
crete social behaviors such as the establishment
of familiarity and preference, proximity seek-
ing, separation distress, and social affect regula-
tion. This chapter is not intended to provide an
exhaustive treatment of all possible constituent
systems underlying attachment. In truth, be-
cause so many neural structures are involved
one way or another in attachment behavior, it is
possible to think of the entire human brain as a
neural attachment system. Auditory, olfactory,
and visual sensory systems are heavily impli-
cated for obvious reasons. Memory processes
involving, for example, long-term memory
consolidation and retrieval in the hippocampus,
underlie familiarity, recognition, and the main-
tenance of shared histories. A wide variety of
Coan!Toward a Neuroscience of Attachment
regulatory needs affected by attachment rela-
tionships are likely to be related to activity in
the hypothalamus. Conflict monitoring de-
mands will be made on the anterior cingulate
cortex (ACC). Each of these systems and more
contribute to attachment in a variety of ways.
In this chapter, however, a smaller number of
putatively basic elements will be reviewed.
Behavioral versus neural systems. I should first dis-
tinguish between what ethologists have long
referred to as “behavioral systems” and what
neuroscientists refer to as “neural systems.” In
ethology, a behavioral system is a set of behav-
iors associated with a common causal antece-
dent and resulting, once activated, in a common
consequent, which in turn deactivates the sys-
tem. Drawing on an ethological approach,
Bowlby (1969/1982) described several behav-
ioral systems associated with attachment. When
discussing behavioral systems such as these,
there is a great temptation to view the behav-
ioral system as having a one-to-one relationship
with some underlying neural system. But such
tidy correspondences are rare. The term “neu-
ral system” describes coordinated neural inputs
and signaling targets among a population of
neurons that form a circuit. Neural systems can
be tightly organized in close physical proximity
or distributed throughout the brain. Highly
similar or even identical behaviors may, across
individuals, result from different combinations
of activity in dissimilar neural systems. Moreo-
ver, similar neural activations can result in quite
distinct behaviors. Thus, the search for specific
neural circuits associated with time-honored,
observationally defined behavioral systems is
fraught with theoretical and empirical difficulty.
Bottom-up versus top-down processing. Although the
terms “bottom-up” and “top-down” processing
are frequently used in the cognitive neurosci-
ences (and throughout the remainder of this
chapter), their meanings may not be immedi-
ately obvious. Bottom- up processes are
thought to begin, more or less, with sensory
information, or with more evolutionarily
“primitive” brain structures, working “up” to
more integrative and evolutionarily modern
areas such as the cortex. The process of receiv-
ing sensory inputs from the environment and
converting those inputs into neural pulses that
are relayed to cortical structures as consciously
perceived information about one’s surround-
ings would be an example of this. Top-down
processes are essentially the opposite. In this
case, integrative and evolutionarily “new” struc-
tures pass neural information “down” to more
sensory-oriented and evolutionarily old struc-
tures, often to suit some regulatory purpose.
One example of a top-down process might be
the brain’s tendency to impute information
from memory and experience into stimuli in
the periphery of the visual field, thereby im-
posing “best guesses” on visual information
that is ambiguous.
Emotional and Motivational
Incentive motivation, reward, and the dopamine system.
Incentive motivation involves the acquisition of
rewarding stimuli. The intensity of incentive
motivation varies as a function of the state of
the individual and the magnitude of the reward.
For example, if a typical Westerner is mildly
hungry and is offered a kind of food that is
normally undesirable to him or her—uni (raw
sea urchin), for example—there will be little
incentive motivation to eat the food. If the in-
dividual is extremely hungry, however, the in-
centive motivation to eat the uni will be high.
Similarly, if the same individual is again only
mildly hungry, but is given a food item that is
highly desirable—say a piece of chocolate
cake—the incentive motivation to eat the cake
will be high.
Incentive motivation plays a key role in a num-
ber of attachment-related processes (e.g., prox-
imity seeking) and is tightly linked to the do-
pamine projection system of the ventral teg-
Coan!Toward a Neuroscience of Attachment
mental area (VTA). Dopamine is produced in
the VTA and substantia nigra and projected to
as many as 30 distinct networks (Le Moal &
Simon, 1991). It has long been held that dopa-
minergic activity represents a neural substrate
for the facilitation of goal- directed behavior
(Berridge, 2007; Depue & Collins, 1999).
Strongly implicated in this function is the nu-
cleus accumbens, which is a major terminal area
of dopaminergic projections from the VTA
(Tzschentke & Schmidt, 2000). Dopaminergic
activity within the VTA and nucleus accumbens
has been repeatedly associated with reinforcing
stimuli and the experience of pleasure. For ex-
ample, rats capable of directly stimulating these
circuits with a lever press will repeatedly do so,
even in lieu of access to food, water, and sex.
This preference for lever pressing over food
and water will continue even to the point of
death (Bozarth & Wise, 1996).
Dopaminergic cells in the VTA are also highly
responsive to conditioning (Depue & Collins,
1999), especially to cues that predict the receipt
of reward (Schultz, Dayan, & Montague, 1997).
Importantly, the VTA is also responsive to
stimuli that are unconditioned. Unconditioned
stimuli are those that naturally, automatically,
and unconditionally trigger a response in an
organism. Positive unconditioned stimuli act as
reinforcers, and include certain flavors, water,
sleep, touch, and the presence of a variety of
social cues. Negative unconditioned stimuli act
as punishers or negative reinforcers, and in-
clude pain, social deprivation, and putrefying
odors (Rolls, 2007a). With repeated exposure to
unconditionally reinforcing stimuli, dopaminer-
gic neurons in the VTA become sensitive to
cues associated with those stimuli. In this way,
the VTA begins to activate the nucleus accum-
bens earlier and earlier in a “chain of cues” that
increase the probability of coming into contact
with the original unconditioned reinforcer (e.g.,
an attractive potential mate). Put another way,
conditioned associations between cues related
to desirable unconditioned stimuli and dopa-
minergic activity in the VTA increase the pre-
dictability of those unconditioned stimuli, and,
hence, the opportunities for obtaining them
(Depue & Collins, 1999).
The amygdala and hippocampus in affect and memory.
The amygdala is now one of the most widely
recognized brain structures associated with
emotion (Phelps & LeDoux, 2005). Far from a
unitary structure, the amygdala contains many
sub-nuclei, accounting for its involvement in a
vast array of emotional responses. A large body
of research now supports the notion that the
amygdala is sensitive to both conditioned and
unconditioned signs of threat. Moreover, at
least two pathways to amygdala activation asso-
ciated with visual stimuli exist, both of which
can mediate fear learning. One is a very rapid
and direct route through the thalamus (the
thalamo-amygdala pathway) that processes ob-
vious or highly specific sensory information
(e.g., the shape of a snake, Le Doux, 2000;
Öhman, 2005). Another pathway processes
slower and more complex information in the
visual cortex before activating the amygdala.
When paired with unconditioned aversive stim-
uli (e.g., a loud noise, pain), otherwise meaning-
less stimuli quickly come to be associated with
the presence of a threat, and this conditioning
appears to be dependent to a large degree on
amygdala functioning in humans as well as
animals. Importantly, although it at first appears
as if threat responding in the amygdala is an
entirely bottom-up phenomenon, there is evi-
dence that amygdala activity is modulated by
top-down processes related to attention (Pes-
soa, Kastnerb, & Ungerleider, 2002).
Interestingly, the amygdala is exquisitely sensi-
tive to social signals expressed on the face (Be-
nuzzi et al., 2007; Rolls, 2007b). Human pa-
tients with impaired amygdala functioning have
difficulty processing emotional facial expres-
sions, especially those communicating social
emotions (Adolphs, Baron-Cohen, & Tranel,
Coan!Toward a Neuroscience of Attachment
2002; Adolphs & Tranel, 2003; Adolphs, Tra-
nel, & Damasio, 1998). Fearful faces in particu-
lar reliably activate amygdala in normal human
subjects (Thomas et al., 2001; Whalen, in
press), even when the presentation of faces is
so rapid that subjects have no conscious mem-
ory of them (Whalen et al., 1998), or when the
faces are reduced to “essential elements,” such
as when no cue but the raised upper eyelid is
shown (Whalen et al., 2004).
Bearing all of this in mind, it is noteworthy that
the amygdala also plays a major role in the con-
solidation of both positive and negative long-
term memories. Amygdala activity during
memory encoding is associated with the recall
of emotionally salient information even weeks
after testing (Hamann, Ely, Grafton, & Kilts,
1999). Beta-adrenergic blockade of amygdala
function appears to impair these effects (Cahill,
Prins, Weber, & McGaugh, 1994). These find-
ings suggest that the amygdala “tags” sensory
experiences as significant or salient and that
this tagging is prominently represented in long-
term memory consolidation. Importantly, the
hippocampus appears to support the forma-
tion, storage, and consolidation of associations
between internal states and spatial or contextual
environmental stimuli (Brasted, Bussey, Murray,
& Wise, 2003; Kennedy & Shapiro, 2004).
Ultimately, both the amygdala and the hippo-
campus are likely to underlie the identification
and consolidation of significant interactions
between attachment figures and emotionally
salient situations. The amygdala will tag emo-
tionally salient stimuli and participate, along
with the hippocampus, in the consolidation of
contextual cues associated with those stimuli in
long-term memory. Among those contextual
cues will be the behavior of attachment figures.
Threat responding, social soothing, and the hypothala-
mus. The hypothalamus regulates a variety of
metabolic and autonomic processes, as well as
linking the central nervous system to the endo-
crine system, most famously in the case of cor-
tisol release via the hypothalamic-pituitary-
adrenal (HPA) axis (Kemeny, 2003). The hypo-
thalamus receives inputs from a wide variety of
structures implicated in social behavior, emo-
tion, stress, and attachment, including the
amygdala, prefrontal cortex, and hippocampus
(McEwan, 2007). The periventricular nucleus of
the hypothalamus is capable of synthesizing
corticotrophin-releasing hormone (CRH;
Gainer & Wray, 1994). In threat responding,
CRH released by the hypothalamus stimulates
the release of adrenocorticotropic hormone
(ACTH) in the pituitary gland. ACTH causes
increased production of cortisol and catecho-
lamines (e.g., epinephrine and norepinephrine)
in the adrenal cortex. This cortisol is circulated
throughout the body, including the brain. Criti-
cally, circulating cortisol in the brain is capable
of activating glucocorticoid receptors in the
hippocampus that feed back to inhibit the
HPA- axis (Kemeny, 2003).
Importantly, the hypothalamus is one of the
key structures implicated in the regulatory ef-
fects of social soothing on neural threat re-
sponding, including interactions with attach-
ment figures (Carter, 2003; Coan, Schaefer, &
Davidson, 2006b). The precise mechanisms by
which social soothing down-regulates HPA-axis
activity are currently unknown (Coan et al.,
2006b), but the hypothalamus is known to co-
ordinate the activity of many behavioral and
physiological systems, including those involved
in maternal behavior and pair bonding. Moreo-
ver, maternal and pair bonding behaviors are
strongly associated with oxytocin and vaso-
pressin, neuropeptides (reviewed below) that
the hypothalamus is capable of synthesizing in
abundance (Carter, 2003; Gainer & Wray,
The prefrontal cortex (PFC), emotion, and emotion
regulation. Many regions of the PFC are impli-
cated in emotion, motivation, and emotion
regulation (Coan & Allen, 2004; Coan, Allen, &
Coan!Toward a Neuroscience of Attachment
McKnight, 2006a). Indeed, portions of the
PFC are strongly connected to the dopaminer-
gic projection system (e.g., nucleus accumbens
and VTA), and the PFC shares numerous con-
nections with the amygdala, hippocampus, and
hypothalamus. For example, the orbitofrontal
region of the PFC assists the amygdala and
hippocampus in linking the emotional value of
secondary sensory information (e.g., place cues)
to primary reinforcers such as food, water, and
social contact (Rolls, 2007a).
One of the major functions of the PFC is the
regulation of emotion. Prefrontal regions may
bias brain circuits responsible for appraising the
emotional content of sensory stimuli and in-
stantiating behavior directed toward approach-
or avoidance- related goals (e.g., via amygdala
or nucleus accumbens; Davidson & Irwin,
1999). Different portions of the PFC underlie
different emotion-regulation strategies (see
Ochsner & Gross, 2005, for a review). These
can include “automatic” forms of emotion-
regulation and effortful forms related to the
cognitive control of attention or stimulus ap-
praisal (Ellenbogen, Schwartzman, Stewart, &
Walker, 2006). Automatic forms of emotion
regulation include conditioning and extinction
learning, including instrumental avoidance.
These rapid and automatic regulatory functions
(especially extinction learning) have been asso-
ciated with the ventromedial and medial orbital
PFC (Milad et al., 2005; Quirk & Beer, 2006;
Sierra-Mercado, Corcoran, Lebrón-Milad, &
Quirk, 2006). More “effortful” forms of regu-
lation require attention, working memory, and
other cognitive operations (Ochsner, Bunge,
Gross, & Gabrieli, 2002). For example, cogni-
tive reappraisals have been used to alter the
meaning of a stimulus, and attentional practices
(e.g., meditation) have been used to alter atten-
tional foci associated with affective stimuli.
These processes have been associated with
more lateral, especially dorsolateral, portions of
the PFC—regions also known to support
working memory, language, and action planning
operations (Ochsner et al., 2002).
Thus, the PFC may be associated with attach-
ment processes in at least two ways. First, over
time, medial orbital circuits may encode condi-
tioned or “automatic” responses to attachment
figures related to excitatory or inhibitory re-
sponses to threat cues. Second, dorsolateral
circuits may modulate cognitive operations as-
sociated with attachment figures in reflective,
working memory. In truth, these distinctions
are not likely to be as discrete as the above
formulation suggests, but the distinction be-
tween medial orbital and dorsolateral circuits of
the PFC offers a useful neural heuristic for
thinking about the regulatory influences of at-
tachment figures in automatic versus explicit
terms, respectively.
Emotional constituents in combination. Because all of
the constituent systems described above are
linked, it is possible for them to coordinate in
important ways. For example, dopaminergic
neurons in the VTA share connections with
many regions other than the nucleus accum-
bens, including the amygdala (in various nuclei
as well as the extended amygdala), the hippo-
campus, the hypothalamus, and the PFC
(Depue & Collins, 1999). In this way, these
structures form their own distributed networks
of often reciprocal influence. To understand
how such a network may function, consider the
distribution of activity following an encounter
with an unconditionally rewarding stimulus.
Dopamine is released from the VTA, which
stimulates dopaminergic activity in the nucleus
accumbens associated with pleasure. The
amygdala “tags” sensory properties of the
stimulus as affectively salient or significant,
placing special emphasis on those properties
during the process of long-term memory con-
solidation via the hippocampus, which also en-
codes contextual information as part of the
consolidation process. The PFC uses this in-
formation to effect action plans and regulate
Coan!Toward a Neuroscience of Attachment
subsequent behavior—both automatic and ef-
fortful—relevant to the stimulus. As experience
with the rewarding stimulus increases in fre-
quency (partly as a function of successful regu-
lation and action planning activity in the PFC),
the affective “tagging” of cues associated with
it proceeds down a “chain of cues,” increasing
the probability that the rewarding stimulus will
be accessed (or avoided in the case of uncondi-
tionally negative reinforcers).
For a more concrete example, consider an en-
counter with an attractive potential mate. In
many species, including humans, such an en-
counter is unconditionally reinforcing. The en-
counter initially elicits pleasurable feelings and
an increase in incentive motivation associated
with the partner. Amygdala tags sensory fea-
tures of the encounter as salient during the
process of memory consolidation in coopera-
tion with the hippocampus, and the VTA be-
comes conditioned to cues associated with (and
predictive of) the potential mate, thereby acti-
vating incentive motivation circuits early in the
“chain of cues” that will increase the likelihood
of encountering the potential mate again. With
repeated exposures, and perhaps a bit of luck,
the potential mate may even respond in kind.
With this, the foundation of pair-bond attach-
ment has been set, and the complex process of
attachment bonding has begun (see Zeifman &
Hazan, Chapter 20, this volume). During the
attachment bonding process, the PFC utilizes
information about the potential mate to adjust
its emotion-regulatory activities, opting, in
many cases, to cede some level of regulatory
effort to the potential mate, as discussed below.
Social Elements
Familiarity and preference. One of the bedrock
features of any species deemed social (as well
as any conception of attachment) is the ability
to distinguish individuals who are familiar from
those who are not—an ability that in turn is
yoked to a preference for the familiar. Indeed,
the establishment and maintenance of prefer-
ences for familiar others (caregivers, peers,
one’s mate, etc.) form the first necessary condi-
tion of attachment bonds. Through evolution-
ary time, familiarity was likely a matter of sur-
vival, and so it remains in the case of infants
and their caregivers. One of the striking things
about humans (and many other mammals) is
how well designed we are for affiliation (Depue
& Morrone-Strupinsky, 2005). Many stereo-
typed behaviors, including facial expressions,
vocalization, bodily gestures, etc., are calibrated
to signal social closeness and/or discomfort.
These signals are readily recognized by most
humans, and may in many cases be innate
(Laird & Strout, 2007; Rolls, 2007a).
More than half a century ago, Bowlby (1969/
1982) suggested that infant-mother bonds,
characterized by both the ability to distinguish
the caregiver from others and a strong prefer-
ence for the caregiver, formed very rapidly, and
this appears to be true in many species. Most
researchers who study infants agree that the
development of attachment bonds is critical,
because infants often must survive long periods
of early development totally dependent upon
their caregivers, even when those caregivers are
neglectful or abusive (Simpson & Belsky, Chap-
ter 6, this volume). The formation of such
bonds appears mainly among birds and mam-
mals, and is thought to have been present in
their common ancestor, the therapsids (Insel &
Winslow, 1998).
Among social species, the most common mani-
festation of the attachment bond—indeed its
commonest exemplar—is, as Bowlby sug-
gested, the bond between a human infant and
its mother (Insel & Fernald, 2004). Human in-
fants have the capacity to distinguish their
mother from others within hours after birth
(DeCasper & Fifer, 1980). Most researchers
agree, however, that in many species attach-
ment bonding represents a more generalized
capacity—one that is only very frequently ap-
Coan!Toward a Neuroscience of Attachment
plied to the actual mother. Indeed, many birds
become bonded within hours to the first mov-
ing object they encounter. Interestingly, Lorenz
(1935) discovered that geese reared by him not
only bonded to him (and followed him) as if he
was the parent, but also that they “courted”
him upon reaching sexual maturity, preferring
him to other geese. These observations raise
important questions for a neuroscience of at-
tachment, concerning the degree to which early
sensory objects associated with a caregiver are
rapidly and permanently “etched” into the de-
veloping brain, how such a thing can occur, and
whether a critical period of bonding formation
exists in early development.
Filial bonding, the locus coeruleus, and the amygdala.
Filial affiliations are those concerning an off-
spring relating to a parent. In humans, strong
attachment to the caregiver usually develops at
six months of age, but filial bonds resembling
this process appear from birth. Filial bonds
may, however, differ from adult affiliation be-
haviors in important ways due to the dependent
nature of the offspring-parent relationship.
Many offspring of social species are totally de-
pendent upon a caregiver for survival, and at-
tachments are imperative regardless of the
quality of the care (Hofer & Sullivan, 2001).
Indeed, nonhuman primates have been ob-
served to exhibit strong attachments to their
mothers even when the mothers are abusive,
and this pattern extends to human children
(Moriceau & Sullivan, 2005). Rat pups have
been observed to form preferences even to
stimuli paired with electric shock, a seemingly
paradoxical effect thought to have developed as
a means of preventing pups from aversion
learning while being handled roughly by the
mother (Hofer, 2006), an unfortunate predica-
ment but generally not as unfavorable as being
abandoned. Ultimately, filial bonds need to be
understood in the context of this high level of
dependence, at least early in development.
It is largely for this reason that at least some of
the neural circuitry associated with attachment
in infants is likely to be different from that in
adults. This may explain why filial bonds occur
so rapidly and unconditionally by comparison
with attachment formation in adulthood. In
fact, filial bonding may precede birth, where
learning about the mother’s voice and odor may
occur. In many species, odor is thought to play
a significant role in the identification of the
primary caregiver soon after birth and thereaf-
ter, even among human infants (Insel & Fer-
nald, 2002). For example, maternal odor has
been observed to elicit orienting responses in
infants, as well as having soothing effects on
human infant crying (Marlier & Schaal, 2005;
Schaal, Marlier, & Soussignan, 1998).
Filial bonding also occurs in a context of sig-
nificant neural development. The human brain
grows exponentially during the first year of life
and continues to develop rapidly into the sec-
ond year (Franceschini et al., 2007). Glucose
metabolism rises gradually until about the 4th
year, and on average the level of brain glucose
metabolism is more than double that of adults
until about age 10 (Chugani, 1998). The pro-
duction of neurotrophins— proteins that aid in
neuron survival—are dependent upon neuronal
activity and, by extension, environmental stim-
uli (Berardi & Maffei, 1999; Cancedda et al.,
2004). Within the first two years of develop-
ment in humans, the brain’s production of ax-
ons, dendrites, and synapses far exceeds its
needs. Synaptic connections are then “pruned”
throughout childhood due to lack of use; that
is, synaptic connections that go unused are dis-
carded (Reichardt, 2006). In this way, the envi-
ronment exerts its influence on the otherwise
genetically determined neural development of
the brain. At a systems level, neural organiza-
tion tends to follow functioning— repetitive
and patterned activation—during development
(Hebb, 1949; Posner & Rothbart, 2007).
Coan!Toward a Neuroscience of Attachment
Throughout the earliest stages of this process,
at least two brain structures, the locus co-
eruleus and the amygdala, interact to facilitate
the familiarity and reinforcement associated
with the caregiver in filial bonding. Although in
adults, norepinephrine (NE) moderates mem-
ory consolidation and learning (Cahill et al.,
1994), NE from the locus coeruleus appears to
be both necessary and sufficient for learning in
human and animal neonates (Sullivan, 2003).
And the neonate locus coeruleus releases large
amounts of NE early in development (Naka-
mura & Sakaguchi, 1990). When combined
with sensory information such as the look,
sound, and smell of a caregiver, that sensory
information is likely to be learned rapidly. Im-
portantly, this learning is occurring alongside a
neonatal amygdala that is not yet fully func-
tional, making it difficult or impossible for
aversive conditioning to occur (Sullivan, 2003).
In other words, the amygdala, being immature
during early neonatal development, may not be
capable of associating aversive stimuli with
alarm or avoidance behavior, leaving virtually
all stimuli to be simply encoded as “familiar,”
which is, for many intents and purposes at this
stage, unconditionally reinforcing.
During this developmental period, neural
pathways linking amygdala to hippocampus are
similarly underdeveloped, as are many regions
within the PFC (Herschkowitz, 2000). This
suggests that learning in neonates may not in-
volve the PFC, or may do so only in limited
ways. In either case, these systems begin to de-
velop rapidly in infancy, leading many to refer
to this developmental time as a “critical” or
“sensitive” period for neural development. Sen-
sitive periods have been studied extensively in
terms of the brains sensory systems. For ex-
ample, Hubel and Wiesel (1970) observed that
a temporary blockage of visual input to one eye
in cats during early development caused irre-
versible impairment in the visual cortex. Simi-
larly, children born deaf have been observed to
cease vocalizations in late infancy, likely due to
a lack of auditory stimuli (Schauwers et al.,
2004). Interestingly, research on the social
complexity of rearing environments in rats
suggests that environments rich in social and
cognitive complexity are associated with signifi-
cantly more synapses per neuron throughout
the visual cortex compared to simple socially
paired housing and individual housing (Briones,
Klintsova, & Greenough, 2004). These effects
remained even after later environments were
changed or reversed, suggesting that plastic
changes associated with early experiences are
In combination, these findings suggest that fil-
ial bonding occurs rapidly and unconditionally.
Moreover, the filial bond develops in a context
of rapid neural development, during what ap-
pears to be a sensitive period of learning. As
will be discussed in greater detail below, this
process, especially to the extent that it involves
developing links between the PFC and affective
structures like the amygdala and nucleus ac-
cumbens, may result in the development of
different reflexive “assumptions” about the na-
ture of the social world, including that world as
it will be encountered in the future. This may
set the stage for different broad strategies for
engaging (or avoiding) social stimuli, perhaps
especially during emotional situations. Indeed,
conditions under which the filial bond forms
and develops may constitute a kind of rudi-
mentary “pre-working model” of interdepend-
ence and affect regulation—of attach-
ment—that is either altered or reinforced dur-
ing the course of development throughout
Adult affiliation, nucleus accumbens, and the social
neuropeptides. Of course, attachment bonds
characterized by interdependence and affect
regulation extend far beyond the prototypic
mother/infant relationship. Adult attachments
occur in the context of romantic relation-
ships—especially monogamous ones—but
Coan!Toward a Neuroscience of Attachment
adult attachment is probably not restricted to
this. Indeed, relationships that meet attachment
criteria have by now been documented between
pairs of individuals as diverse as adult romantic
partners (Fraley & Shaver, 2000); captive chim-
panzee cage mates (Bard, 1983; Miller, Bard,
Juno, & Nadler, 1986); chimpanzees and their
human caretakers (Miller, Bard, Juno, & Nadler,
1990); and even between domesticated dogs
and their owners (Topal, Miklosi, Csanyi, &
Doka, 1998). Aspects of attachment seem to
occur even between organization members and
their leaders (Davidovitz, Mikulincer, Shaver,
Ijzak, & Popper, 2007).
Of interest here are neural circuits that support
the establishment and maintenance of attach-
ment bonds in later childhood and adulthood.
How does the brain facilitate movement from
close proximity, to familiarity, to attachment?
To start, positive, possibly unconditioned, so-
cial affiliation behaviors (e.g., eye gaze, soothing
vocalizations, non-threatening facial and bodily
behaviors) increase proximity between conspe-
cifics, setting the stage for motivated attach-
ment bonding. It is clear that some social cues
are unconditionally capable of activating neural
structures supporting incentive or reward moti-
vation, especially the nucleus accumbens and
the VTA (Allen et al., 2003). For example, pas-
sively viewed images of female faces have been
observed to activate the VTA and nucleus ac-
cumbens unconditionally in heterosexual men
(Aharon et al., 2001). In rats, maternal females
show an increase in dopamine release in the
nucleus accumbens when exposed to pups
(Hansen, Bergvall, & Nyiredi, 1993). Depletion
of dopamine in the VTA and nucleus accum-
bens via lesions or dopamine antagonists virtu-
ally eliminates rat maternal behavior (Hansen,
Harthon, Wallin, Löfberg, & Svensson, 1991).
Interestingly, maternal behaviors not directly
associated with caregiving, such as nest build-
ing, passive nursing, and aggression, are virtu-
ally unaffected by these manipulations. Other
studies have linked dopamine release in the
nucleus accumbens and VTA to the spontane-
ous establishment of partner preferences (Ara-
gona et al., 2006).
Mating behavior in the absence of partner
preference is also associated with dopamine in
the nucleus accumbens (Balfour, Yu, & Coolen,
2004; Pfaus, Kippin, & Centeno, 2001), how-
ever, suggesting that dopaminergic activity in
the nucleus accumbens is insufficient for the
establishment of partner preferences. This
raises the question of how the establishment of
partner preferences is “linked up” to the do-
paminergic incentive motivation system. Here,
the neuropeptides oxytocin and vasopressin
appear to play major roles (Depue & Morrone-
Strupinsky, 2005; Young & Wang, 2004). Both
have been associated with the formation of
partner preferences regardless of mating be-
havior, and both, but especially oxytocin, are
elicited by positive social behaviors (Uvnaes-
Moberg, 1998).
Perhaps the most celebrated example of the
function of these neuropeptides derives from
work on pair bonding within monogamous
prairie voles (Borman-Spurrell, Allen, Hauser,
Carter, & Cole-Detke, 1995; Carter, 2003; Insel
& Fernald, 2004; Young & Wang, 2004). When
these animals forge a pair bond, they mate,
share nests and territory, cooperate in care of
young, and forcefully reject intruders of either
sex (Borman-Spurrell et al., 1995). Unlike
nonmonogamous animals—including other
variants of vole—the nucleus accumbens of
these animals is rich in oxytocin receptors.
Moreover, structures like the ventral tegmen-
tum and ventral palladium are rich in receptors
for vasopressin (Lim, Hammock, & Young,
2004; Lim & Young, 2006).
Findings such as these provide clues as to how
social cues activate incentive motives associated
with dopaminergic activity and in turn the for-
mation of partner preferences and proximity-
Coan!Toward a Neuroscience of Attachment
seeking behavior. Socially sensitive oxytocin
and vasopressin circuits in the VTA, nucleus
accumbens, and ventral palladium probably
stimulate dopaminergic activity linked to incen-
tive motivation. Because activation of this do-
paminergic system is frequently associated with
positive affect and reward, it may be that the
degree of oxytocin and vasopressin activity de-
termines the degree to which a social experi-
ence is rewarding, by virtue of the dopaminer-
gic cascade that follows it.
Proximity seeking, the dopamine system, and
endogenous opiates. One of the natural conse-
quences of familiarity, preference, and bonding
is proximity seeking, a characteristic of social
behavior strongly associated with attachment.
Proximity seeking is likely an extension of mo-
tivational circuits associated with reward and
partner preference. Of course, individuals can
seek close proximity as a function of positive
affect and reward or in response to cues of
punishment where the goal is the provision of
safety (Depue & Morrone-Strupinsky, 2005). In
the case of positive affect, proximity is sought
because the attachment figure has become as-
sociated with rewarding feelings of pleasure,
and close proximity increases the frequency or
intensity of these feelings. In the case of nega-
tive affect, the attachment figure may serve as a
safety cue, eliciting approach behaviors ori-
ented toward the acquisition of security. In this
way, proximity seeking can involve both
reward-related approach behaviors and ap-
proach behaviors associated with active avoid-
Behaviorally, these motivations may appear to
be identical, but they are likely to involve both
shared and distinct neural circuits. Moreover,
although attachment theory emphasizes the
emotion-regulatory function of proximity-
seeking due to the need for security, it may be
counterproductive to downplay the role of
proximity-seeking due to reward processes. It
may be the case, for example, that at the neural
level reward-related proximity conditioning is
tightly bound to the provision of security by
the attachment figure in other contexts. From
the perspective of the VTA and nucleus ac-
cumbens, there may be little difference, because
they become in either case sensitized to the
presence of the attachment figure as a positive
In addition to the reinforcing nature of dopa-
minergic activation, consummatory pleasure
may play a role in rewarding social interaction.
After all, positive social experiences are charac-
terized in everything from semi-structured sci-
entific interviews to ancient literature as involv-
ing feelings of warmth, closeness, love, affec-
tion, and pleasure. Depue and Morrone- Strup-
insky (2005) have argued that feelings of con-
summatory pleasure promote the development
of contextual associative memory networks
that help both to establish and to maintain so-
cial bonds and that are ultimately responsible
for many of the regulatory effects associated
with the soothing and security provided by at-
tachment relationships. The critical substrate
for these feelings, and perhaps for the socioaf-
fective regulatory effects that accompany them,
may be the release of opiates that often follow
activation of oxytocin receptors, also in struc-
tures like the nucleus accumbens and VTA.
There is abundant evidence for the role of en-
dogenous opiates in a wide variety of social
behaviors. In humans and other animals, these
opiates are released during childbirth, nursing,
maternal caregiving, sexual activity, and many
modes of tactile stimulation, including groom-
ing and play behavior (Carter & Keverne, 2002;
Keverne, Martensz, & Tuite, 1989. This release
may mediate the reward associations that are
forged between infants and mothers, as well as
between romantic partners, and even platonic
friends. For example, morphine, an opiate re-
ceptor agonist, increases the reinforcing effects
of a host of maternal behaviors, mother-infant
bonding, time spent by juveniles (rats) with
Coan!Toward a Neuroscience of Attachment
their mothers after a brief separation, groom-
ing, and juvenile play behavior (Agmo, Barreau,
& Lemaire, 1997; Niesink, Vanderschuren, &
van Ree, 1996; Nocjar & Panksepp, 2007; Pank-
sepp, Nelson, & Siviy, 1994). By contrast, opi-
ate receptor antagonists such as naltrexone re-
duce reward conditioning effects associated
with each of these forms of social contact
(Graves, Wallen, & Maestripieri, 2002; Hollo-
way, Cornil, & Balthazart, 2004). In humans,
the administration of the opiate antagonist
naltrexone was associated with increased volun-
tary isolation from friends, as well as decreased
levels of enjoyment in the company of others
(Jamner & Leigh, 1999).
Importantly, tactile stimulation appears to play
a particularly powerful role in the activation of
affiliative reward conditioning (Burgdorf &
Panksepp, 2001; Melo et al., 2006). In some
animals, the affiliative conditioning associated
with maternal behavior is attenuated in the ab-
sence of tactile stimulation (Melo et al., 2006).
Attachment and the
Social Regulation of Emotion
Many evolutionary accounts of the reproduc-
tive advantages of infant-caregiver bonds have
been proposed, but similar accounts of adult
attachment bonds are relatively recent (Simp-
son & Belsky, Chapter 6, this volume; Zeifman
& Hazan, Chapter 20, this volume). Fraley and
Shaver proposed that adult attachments repre-
sent homologies of the infant-caregiver bond
co-opted by natural selection to facilitate pair
bonding (Fraley & Shaver, 2000). By this ac-
count, adult and infant-caregiver attachment
systems entail similar goals (the survival of off-
spring) and operate according to similar condi-
tions of activation (e.g., presence of a threat)
and termination (e.g., regulation of threat re-
sponding by the attachment figure). Evolution-
ary perspectives like these address ultimate
function, in the sense of explaining why at-
tachment bonds and capabilities persist among
so many species.
Function can be considered in a more proxi-
mal, ontogenetic sense as well, and it is at this
level that the regulation of affect may take cen-
ter stage. Proximal functions of the attachment
system are, following basic survival during in-
fancy (Hofer, 2006), primarily concerned with
the social regulation of emotional responding.
Bowlby (1969/1982), following along with
Ainsworth and her colleagues (e.g., Ainsworth,
Blehar, Waters, & Wall, 1978), argued that a
critical function of attachment figures was the
provision of a secure base from which infants
could explore their worlds relatively free of
anxiety, and a safe haven to which the infant
could return when distressed. It was proposed,
for example, that the base from which an infant
could explore its world was secure to the extent
that the caregiver was responsive to the infant’s
distress. Many have since proposed that the
quality of the caregiver-infant attachment
bond—especially of the caregiver’s status as a
secure base—holds consequences for child and
adult emotional functioning, including styles of
interpersonal relating and emotion-regulation
capabilities. A very large behavioral database
now supports this notion with respect to both
childhood and adulthood (for reviews, see
Thompson, Chapter 16, and Mikulincer &
Shaver, Chapter 23, both in this volume).
Throughout childhood, and certainly by adult-
hood, the regulatory effects of attachment rela-
tionships are likely to be felt in two broad ways.
The first is immediate, as when the attachment
figure is present and regulating emotional re-
sponding “on line.” An example of this may be
when a caregiver holds her child’s hand during
a blood draw at the doctor’s office, thus actively
soothing the child’s anxiety as it occurs. The
second is generalized, where the attachment
figure is present only in the form of a mental
representation. These representations may in
theory manifest either as “internal working
Coan!Toward a Neuroscience of Attachment
models” based on procedural and semantic
memory, or as declarative, explicitly recalled
mental images. Indeed, on-line regulation expe-
riences likely condition mental representations
in both implicit and declarative memory. In the
sections that follow, immediate, “on line” regu-
lation is considered in contrast to “mental rep-
resentations” of the attachment figure, often
referred to as “internal working models,” that
may serve to preempt the level of distress an
individual experiences in the face of a potential
The “On-Line” Social Regulation
of Emotion
Many researchers have observed the stress-
buffering effects of social contact on behaviors
and physiological systems related to emotional
responding. This social buffering occurs at all
levels (e.g., group, caregiver, familiar conspe-
cific), but familiarity and attachment are associ-
ated with the strength of social regulation ef-
fects. Even in rats, the presence of familiar
conspecifics (“buddy” rats) increases explora-
tion and attenuates HPA-axis activity under
conditions of threat (Kiyokawa, Kikusui,
Takeuchi, & Mori, 2004; Ruis et al., 1999; Ter-
ranova et al., 1999). Familiar conspecifics at-
tenuate emotional stress responding in non-
human primates during new social group for-
mation and social conflict (Gust, Gordon, Bro-
die, & McClure, 1996; Weaver & de Waal,
2003). As reviewed above, these effects are
widely believed to derive from social cues that
activate the release of oxytocin and vasopressin
in the VTA, ventral palladium, and nucleus ac-
cumbens (Carter & DeVries, 1999; Heinrichs et
al., 2001; Izzo et al., 1999; Uvnaes-Moberg,
1998; Windle, Shanks, Lightman, & Ingram,
1997). This in turn is thought to activate do-
paminergic and endogenous opiate activity as-
sociated with consummatory pleasure and
physiological soothing.
In humans, very little work to date has actually
sought to identify how neural circuits associ-
ated with social affiliation and emotion func-
tion in a context that combines social interac-
tion with externally generated emotional stress.
Recently, Coan and colleagues (Coan et al.,
2006b) collected functional brain images from
16 married women as they were subjected to
the threat of mild electric shock while either
holding their husband’s hand, holding the hand
of an anonymous male experimenter, or hold-
ing no hand at all. Their results suggest that
physical contact from both attachment figures
and strangers attenuates threat responsive neu-
ral activity in affect-related action and bodily
arousal circuits (e.g., in the ventral anterior cin-
gulate cortex), but also that down regulation of
structures such as the nucleus accumbens, dor-
solateral prefrontal cortex, and superior collicu-
lus was achieved only via hand holding with the
attachment figure. Moreover, Coan et al.
(2006b) observed that some of the regulatory
effects of soothing physical contact varied as a
function of relationship quality, with higher
quality predicting yet greater attenuation of
threat-related neural activation in the right ante-
rior insula, superior frontal gyrus, and hypo-
thalamus during spousal, but not stranger, hand
holding. These findings suggest that social
proximity in general, and the presence of an
attachment figure in particular, exerts bottom-
up regulatory influences on the perception of
threat in the brain. Moreover, the fact that
stranger hand holding conferred regulatory
benefits at all suggests that the human brain is
unconditionally soothed to some extent by so-
cial proximity, which may lay the groundwork
for the additional regulatory benefits associated
with attachment figures.
Internal Working Models and
Individual Differences
Thus far, we have primarily considered basic
systems supporting “normative” manifestations
Coan!Toward a Neuroscience of Attachment
of attachment behavior, as well as a concrete
example of the emotion-regulation functions
of the attachment system occurring “on line”
in real time. However, the emotion-regulatory
effects of caregiving experiences such as those
between infants and caregivers, or even be-
tween romantic partners, are likely to extend far
beyond online moments of soothing and secu-
rity provision. Bowlby (1979) considered many
facets of early attachment experiences to hold
implications for interpersonal and emotional
functioning “from the cradle to the grave” (p.
129), and in the past several decades many re-
searchers have adopted this idea as one way to
understand adult interpersonal functioning and
emotion-regulation capabilities.
Unfortunately, a large portion of what is
known about links between early social experi-
ence, neural development, and subsequent
emotional behavior derive from studies of
abuse and neglect. For example, neglect and
abuse (both physical and verbal aggression) are
associated with risk for heightened stress reac-
tivity, anxiety, depression, and social deviance
that extend well into adulthood (Teicher, Sam-
son, Polcari, & McGreenery, 2006). In one re-
cent study, children who had experienced social
deprivation and neglect in Romanian orphan-
ages were observed to have lower overall levels
of vasopressin, as well as blunted oxytocin re-
sponses to physical contact with their caregiv-
ers, relative to normally family-reared children
(Wismer-Fries, Ziegler, Kurian, Jacoris, & Pol-
lak, 2005). This is consistent with findings re-
garding social isolation as a well-known risk
factor for a number of neurodevelopmental
and psychosocial problems, ranging from anxi-
ety and depression to increased risk of suicide,
family problems, and even stress-related dwarf-
ism (Barber, Eccles, & Stone, 2001; Kawachi,
2001; Newcomb & Bentler, 1988; Skuse, Al-
banese, Stanhope, Gilmour, & Voss, 1996). In
nonhuman primates, frequent or prolonged
separation of offspring from caregivers (pri-
marily mothers) can result in socially deviant
behavior and physiology later in life (Mineka &
Suomi, 1978). Among brown capuchins mon-
keys, patterns of mother/offspring behavior
partially determine the post-conflict reconcilia-
tion styles of offspring during later interactions
with nonfamilial conspecifics (Weaver & de
Waal, 2003).
Neural mechanisms linking early parental care
to trait-like individual differences in threat re-
sponding over the life span have been expertly
described by Meaney and colleagues (Weaver et
al., 2004). This work suggests that in rats,
grooming behavior by the mother “sets” or
“programs” the degree to which her offspring
react to threat cues throughout their lives. This
modulation of threat reactivity has been ob-
served both in behavior and in HPA- axis activ-
ity. Moreover, associations between maternal
grooming and offspring threat reactivity have
been linked to the expression of specific genes
that moderate HPA-axis functioning. As re-
viewed above, the HPA-axis has its own built-in
regulatory mechanism in the hippocampus,
whereby circulating cortisol activates hippo-
campal glucocorticoid receptors, which in turn
down-regulate the production of
corticotrophin-releasing hormone in the hypo-
thalamus. Grooming induces the expression of
genes that encode for glucocorticoid receptors
in the hippocampus, thus making the hippo-
campus more sensitive to circulating cortisol
and, hence, more susceptible to down-
regulation during stress. Cross- fostering stud-
ies by Meaney and colleagues strongly suggest
that lifelong stress reactivity, and even the sub-
sequent maternal behavior of female rat pups,
is largely attributable the degree of post-natal
maternal grooming and not to genetic inheri-
tance (Weaver et al., 2004).
Attachment and internal working models. According
to attachment theory (Bowlby, 1969/1982,
1973; Mikulincer & Shaver, 2007; Mikulincer
&Shaver, Chapter 23, this volume), threat de-
Coan!Toward a Neuroscience of Attachment
tection capabilities evolved in part to activate
the attachment behavioral system, thus increas-
ing the likelihood that humans, beginning in
infancy, would seek out and maintain proximity
to attachment figures. Moderating the degree to
which proximity to attachment figures is sought
out in the context of a threat is attachment se-
curity, which is itself the product of many
attachment-related experiences involving both
threats and attachment figures. These experi-
ences shape “internal working models” of at-
tachment that guide emotion-regulation
throughout life (see Bretherton & Munholland,
Chapter 5, this volume). According to Bowlby
(1969/1982), internal working models are men-
tal representations of the availability and prac-
tical utility of attachment figures when threats
arise, and of the self in relationship with these
Recently, Hofer (2006) described a process by
which very early developmental experiences in
interactions with a caregiver may plausibly pro-
ceed from the on-line regulation of fundamen-
tal neural systems supporting sensory-motor,
thermal, and nutrient functions to the shaping
of internal working models of attachment se-
curity. In this model, access to primary rein-
forcers (e.g., food, water, warmth, touch) is de-
pendent in early development on (a) caregiver
support and (b) affective brain circuitry used to
solicit caregiver support via expressed affect.
Over the course of development, what begins
as the regulation of physiological needs via af-
fect becomes the regulation of affect per se
(Hofer, 2006). Throughout this process, the
regulatory behavior of the attachment figure
(e.g., the provision of security, the alleviation of
distress) is likely to set expectations about the
availability of attachment figures during times
of stress—the “internal working models” re-
flecting attachment security.
Thus, internal working models likely reflect
conditioned associations between proximity to
attachment figures and both internal needs and
external signs of threat, mediated through the
amygdala, nucleus accumbens and hippocam-
pus, as well as portions of the prefrontal cor-
tex. These conditioned associations may remain
stable for long periods of time, especially to the
extent that they continue to be reinforced by
internal feelings of security, prevailing social
contingencies, or both.
This process likely allows individuals to adapt
themselves to a variety of environmental condi-
tions (e.g., security restoring or enhancing expe-
riences with attachment figures, frequent or
lengthy absence of the caregiver, abuse by the
caregiver, excessive caregiving). Such adapta-
tions are referred to, in various research tradi-
tions, as attachment patterns, attachment styles,
or attachment states of mind (e.g., secure, anx-
ious, avoidant, preoccupied). These adaptations
are thought to be relatively stable when the in-
dividual remains in a stable environment, and
can be measured by observations, self-report
questionnaires, and structured interviews (e.g.,
Crowell & Fraley, Chapter 26, Kerns, Chapter
17, and Solomon & George, Chapter 18, all this
Behavioral research on the effects of different
adult attachment styles suggests the presence of
two relatively independent axes regarding at-
tachment insecurity—anxiety and avoid-
ance—along which individuals can vary (J.
Feeney, Chapter 21, this volume; Mikulincer &
Shaver, 2007). Moreover, different combina-
tions of scores along these dimensions can re-
sult in particular styles of relating interperson-
ally. For example, individuals low in attachment
anxiety and low in attachment avoidance would
be considered generally secure in their attach-
ments to others. Individuals high in both
avoidance and anxiety are thought to avoid at-
tachment relationships out of fear, while those
high in avoidance but low in anxiety are
thought to be “dismissing” of attachments,
compulsively self-reliant, and unlikely to seek
proximity to attachment figures under stress
Coan!Toward a Neuroscience of Attachment
(Bartholomew & Horowitz, 1991; Brennan,
Clark, & Shaver, 1998). Finally, individuals low
on avoidance but high on anxiety are thought
to be preoccupied with attachment relation-
Few studies to date have investigated individual
differences in attachment styles using measures
of neural activity, and some of the work that
has been done serves only as an approximation.
Indeed, attachment styles may, at a neural level,
manifest as little more than individual differ-
ences in response capabilities among neural
circuits supporting emotion, emotion-
regulation, and social behavior. Interestingly,
Dawson and colleagues (Dawson et al., 2001)
observed that insecurely attached infants of
depressed mothers were more likely to show
PFC asymmetries lateralized to the right. By
this metric, asymmetries in EEG activity in the
alpha (8-13Hz) range (Coan & Allen, 2003;
Coan & Allen, 2004) correspond with emotion
regulation capabilities (Coan et al., 2006a), with
relatively greater left PFC activity indexing an
increased probability of approach behavior
(e.g., anger, joy), and relatively greater right
PFC activity indexing an increased probability
of withdrawal behavior (e.g., sadness, fear).
Thus, according to Dawson, insecurely attached
infants of depressed mothers have a trait-like
propensity to engage in withdrawal behavior
(Dawson et al., 2001).
A very small number of studies have begun to
associate adult attachment styles with brain
function using functional neuroimaging tech-
nology. Recently, Coan and colleagues (2005)
reported a variety of interaction effects be-
tween self-reported attachment scores and
hand holding condition (spouse, stranger,
alone) on threat-related neural activity through-
out the brain. For example, under threat of
mild electric shock, secure attachment scores
were negatively associated with activity in the
ventral anterior cingulate cortex (vACC) during
spouse hand holding, and positively correlated
with activity in the same region when holding
the hand of a stranger. The vACC is implicated
in the modulation of affect-related arousal.
Avoidance scores corresponded with increased
activation during spouse hand holding, and de-
creased activation during stranger handholding,
in the right ventromedial PFC, a region com-
monly associated with the regulation of nega-
tive affect.
In another recent fMRI study, 20 women were
asked to think about—and then to stop think-
ing about—various relationship scenarios (Gil-
lath, Bunge, Shaver, Wendelken, & Mikulincer,
2005). Attachment anxiety was positively asso-
ciated with activity in the dorsal anterior cingu-
late cortex, and anxiety scores were positively
correlated with brain activity in the temporal
pole, but negatively with brain activity in the
orbitofrontal cortex, during thoughts about
negative relationship scenarios. This suggests
that attachment-anxious individuals are not en-
gaging neural systems that would help to regu-
late their emotional responses during negative
relationship thoughts.
More recently, Bucheim and colleagues
(Buchheim et al., 2006) collected functional im-
ages of the brain while adults told “attachment
stories” in response to images from the Adult
Attachment Projective (Lorberbaum et al.,
1999) intended to activate the attachment be-
havioral system. Attachment stories from the
AAP were used to classify individuals as either
“organized” or “disorganized.” Individuals
classified as disorganized were more likely to
show amygdala and hippocampal activation
when shown pictures portraying traumatic as
opposed to neutral attachment situations.
Although findings from each of the studies
described above should be considered prelimi-
nary, they do contribute to our understanding
of how attachment styles and internal working
models may moderate neural processes associ-
ated with the regulation of emotion. They are
Coan!Toward a Neuroscience of Attachment
the initial steps in what is likely to be an in-
creasing effort to use brain imaging techniques
to study the neural correlates and underpin-
nings of processes studied previously only
through verbal and behavioral reactions to
laboratory procedures.
The Social Baseline Model
Social influences on the regulation of affect are
sufficiently powerful and unconditioned to
suggest that the brain’s first and most powerful
approach to affect regulation is via social prox-
imity and interaction. This is most obvious in
infancy, where very basic physiological needs
are regulated first via affect expression, leading
to a dynamic of regulating affect per se, where
caregivers become the primary agent through
which infants regulate affective responding
(Hofer, 2006). For the infant, this is occurring
in a context of rapid and expansive neural de-
velopment—possibly a “critical period” during
which a number of expectations about the na-
ture of the infant’s future environment are be-
ing formed. A great deal of this development is
occurring in the prefrontal cortex, a region of
the brain powerfully implicated in self-
regulation of affect. Because the prefrontal cor-
tex is underdeveloped in infancy, the caregiver
effectively serves as a kind of surrogate pre-
frontal cortex, a function that attachment fig-
ures likely continue to serve for each other to
varying degrees throughout life.
What I will call the social baseline model sug-
gests that social affect regulation was long ago
adopted as an efficient and cost- effective
means of regulating affect. It draws on the
principle of economy of action, which states
that organisms must, over time, consume more
energy than they expend if they are to survive
to reproduce (Proffitt, 2006). Because all bodily
neural activities—expend energy, energy ex-
penditure must be managed. Proffitt (2006) has
proposed that one of the ways in which the
brain manages energy expenditure is via altera-
tions in sensory perception that aid in decision-
making about the deployment of an organism’s
resources. For example, Proffitt (2006) has ob-
served that donning a heavy backpack causes
hills to appear steeper and objects to appear
farther away, thus discouraging individuals from
using their resources to climb those hills or ap-
proach those objects. In this way, the brain can
be thought of as a “Bayesian machine,” making
“bets” at any given time about what resources
to deploy, and at what level of effort (Addis,
Wong, & Schacter, 2007; Bar, 2007).
The social baseline model proposes that social
species are hard-wired to assume relatively
close proximity to conspecifics, because they
have adopted social proximity and interaction
as a strategy for reducing energy expenditure
relative to energy consumption. This implies
that the absence of conspecifics, in defying this
baseline assumption, functionally adds to the
perceived cost of interacting with the environ-
ment—especially in threatening contexts (an
implication discussed explicitly by Bowlby,
1969/1982). In other words, the social baseline
model proposes that social isolation is, for a
social organism, akin to donning a heavy back-
pack, altering the real and perceived demands
associated with its environment. There are at
least two ways in which the presence of con-
specifics may reduce, for social organisms, the
actual and perceived cost of engagement with
the environment. I will call these strategies risk
distribution and load sharing.
Risk distribution. The first way in which social
species, including humans, benefit from close
social proximity is via the simple distribution of
risk in the environment. Many species benefit
from living in groups, and simple risk distribu-
tion strategies are likely to be plesiomorphic, or
relatively ancient in evolutionary terms. Al-
though group living comes at a cost at the level
of resource consumption, the benefits may
Coan!Toward a Neuroscience of Attachment
outweigh those costs sufficiently to create con-
ditions under which group cohesion ultimately
promotes the survival of each individual in the
group. Risk distribution speaks to the amount
of risk a given individual carries as a function
of the degree to which he or she is alone, and it
can manifest in many ways (Krebs & Davies,
1993). For example, the larger the group, the
more individuals there are to scan for possible
signs of danger. Similarly, a given individual is
at substantially reduced risk of personal danger
(e.g., predation) when group size increases. A
similar example among warm-blooded species
may be the thermal advantage of huddling to-
gether. Some social species utilize group size to
maximize their performance as predators, and
this, too, can be a form of risk distribution, for
if predation (especially of large target animals)
is maximized in groups of predators, the risk
that any one predator will perish from starva-
tion is minimized.
From the perspective of the social baseline
model, it is important that the brains of social
species appear to be capable of assessing the
distribution of risk and making Bayesian deci-
sions about the cost-effectiveness of affective
behavior at any given time. Practically speaking,
the presence or absence of conspecifics pro-
vides, at the lowest level of social proximity, a
heuristic for deploying potentially costly re-
sources. For example, in the presence of oth-
ers, individuals may work less hard at being
vigilant for—or even fleeing—predators. These
activities, which may be yoked to perceived
bodily resources (Proffitt, 2006), are deployed
only as needed. The resources that are saved by
close social proximity are either simply con-
served or used for other valuable purposes.
Load sharing. Risk distribution processes are not
likely to have strong effects on processing at
the cortical level, especially in the prefrontal
regions supporting attention, working memory,
and the self-regulation of affect. Interestingly,
such prefrontally mediated activities are
thought to be particularly costly to deploy
(Galliot & Baumeister, 2007). Evidence for this
derives from studies of cognitive depletion as a
consequence of effortful attention and self-
control. In this work, individuals who are asked
to engage in tasks requiring self-regulation are
subsequently less capable of similar tasks.
Moreover, engaging in these tasks has been ob-
served to result in temporary depletions in
blood glucose concentration (Galliot & Bau-
meister, 2007).
The social baseline model predicts that the pre-
frontal cortex, and many of the regulatory
processes it supports, may be particularly af-
fected by the presence of an attachment figure,
especially in the context of a threat. Here, the
advantage of close proximity extends far be-
yond simple models of risk distribution: Over
and above the dilution of risk via large num-
bers, a trusted and interdependent associate can
be counted on to engage in a number of
health- and safety-enhancing behaviors on
one’s behalf. Such behaviors may include the
identification and acquisition of resources, vigi-
lance for environmental threats, caring for one’s
needs, and nurturing of one’s offspring. These
allegiances—these attachments—serve to dis-
tribute the cost of many of life’s metabolically
expensive activities, not least being the regula-
tion of one’s own negative affect. Simply put,
affect regulation is possible, but more difficult,
in isolation. I refer to this second level of social
regulation as load sharing, and I believe it is an
essential component of attachment relation-
ships throughout the life span. Load sharing is
likely to be apomorphic, or relatively advanced
in evolutionary terms, having arisen as a strat-
egy relatively recently. Human brains are highly
sensitive to the load sharing significance of
close attachment bonds, and adjust their efforts
accordingly. For example, individuals in close,
trusted relationships will invest less effort in
down-regulating their negative affect, leaving
them less responsive to threat cues and other
Coan!Toward a Neuroscience of Attachment
signs of possible harm (Coan et al., 2006b;
Edens et al., 1992; Mikulincer & Florian, 1998;
Robles & Kiecolt-Glaser, 2003). Thus, the so-
cial brain is designed in part to distribute affect
regulation activities to attachment figures. As
with the metabolic benefits of risk distribution,
this should produce major metabolic resource
Unlike risk distribution strategies, which are
primarily sensitive to numbers alone, load shar-
ing, especially in adult attachment relationships,
likely develops as the brains of individuals in a
relationship become conditioned to one an-
other, especially in the context of coping with
threats. Over time, individuals in attachment
relationships literally become part of each
other’s emotion regulation strategy. This is not
metaphorical, but literal, even at the neural
level. For example, an individual who has been
alone for a long period of time may have
learned to exercise his prefrontal cortex in the
service of regulating his threat responses. The
social baseline model predicts that upon estab-
lishing an attachment relationship, the individ-
ual’s perception of the degree to which his en-
vironment is threatening or dangerous will
change, decreasing the frequency with which he
exercises his prefrontal cortex in the service of
emotion regulation. Note that this is because
his brain assumes a decrease in the need for
emotion regulation. With sufficient experience
in the relationship, the level of interdependence
associated with emotion-regulation needs can
become strong. Indeed, a grim reminder of this
occurs when one or the other member of an
attached pair is suddenly absent due to death or
divorce, leaving the partner severely dysregu-
lated (Bowlby, 1980; Sbarra, 2006); see Fraley &
Shaver, Chapter 3, this volume).
An example of this dynamic of increasing need
for self- regulation as a function of distance
from an attachment figure can be found in the
previously mentioned study by Coan et al.
(2006b), in which married women in an MRI
scanner were confronted with the threat of a
mild electric shock under each of three condi-
tions: while alone, while holding a stranger’s
hand, and while holding their spouse’s hand.
Women in the highest quality relationships
showed the lowest degree of threat-related
brain activation, limiting their response to rela-
tively automatic regulation of threat perception
via structures such as the ventromedial PFC.
When the marital relationship was of relatively
poor quality, however, the
number of problems confronting the woman’s
brain under threat increased to include atten-
tion to bodily sensory afferents, presumably
related to the threat of shock (right anterior
insula), task salience (superior frontal gyrus),
and release of regulatory stress hormones (hy-
Presumably, the regulatory benefits associated
with attachment figures in both the higher and
lower quality relationships reflected the load
sharing function of attachment relationships.
As the nature of the hand-holding partner
switched from attachment figure to stranger,
however, yet more problems presented them-
selves, with additional threat-related brain acti-
vations triggered to solve them. For example,
threat-related vigilance increased (e.g., via the
superior colliculus), effortful emotion-
regulation strategies were employed (e.g., via
right dorsolateral PFC), and areas were re-
cruited that indicated increased threat-related
avoidance motivation (e.g., caudate/nucleus
Still, the brain was less active while holding the
hand of a stranger than while alone, presuma-
bly reflecting the effects of risk distribution via
fairly minimal social proximity. While alone, the
brain appears to get busy solving yet more per-
ceived problems, adding to those already enu-
merated somatic preparations for threat re-
sponding, increasing bodily arousal (e.g.,
through the ventral ACC) and coordinating vis-
Coan!Toward a Neuroscience of Attachment
ceral and musculoskeletal responses (e.g., poste-
rior cingulate, supramarginal gyrus, postcentral
It is important to emphasize that social affect
regulation appears to be a relatively bottom-up
process, as opposed to one’s solo affect regula-
tion, which is more top down. When engaging
in self-regulation, a person is likely to need to
engage in costly, effortful cognitive and atten-
tional strategies in the service of inhibiting ei-
ther somatic responses or structures supporting
the identification of threat cues. This effortful
regulation of affect relies to a great degree the
prefrontal cortex. In this way, self- regulation
frequently occurs in the context of an affective
response that has already occurred. By contrast,
social affect regulation may often affect the
perception of threat in the first place, thereby
decreasing the need for threat responding and
leaving the prefrontal cortex with relatively little
or nothing to regulate. Thus, social affect regu-
lation could be said to be more efficient, or less
costly, than self-regulation strategies, such as
the suppression of emotional responses, the
cognitive reappraisal of threatening situations,
and even popular strategies such as meditation.
The extent to which this is true awaits further
Attachment styles as Bayesian priors. Of course, the
preceding discussion offers only a simplified,
idealized model of social affect regulation, and
one highly dependent on situational contingen-
cies. It is likely that superimposed on all of the
processes described above are trait-like assump-
tions about the function and metabolic cost of
social factors in regulating the perception of
threat cues and, hence, of affect. Accordingly,
one way to conceptualize attachment styles and
internal working models is as prior probabilities
in a Bayesian decision-making process, where
the goal is to predict the regulatory cost-
effectiveness of attachment figures. In this way,
attachment styles come to represent strategies,
based on prior experience, for making decisions
about how to utilize one’s own neural resources
in the presence or absence of strangers and
attachment figures. A secure attachment style
presumably disposes a person to make bets
closely in accordance with the idealized picture
described above. By contrast, avoidant and anx-
ious strategies may encourage individuals to
make greater use of their own resources, even
in the presence of social support, or to place
themselves outside the reach of social support
in the hopes of avoiding additional costs (e.g.,
having to regulate others as well as self), thus
again requiring one to rely on one’s own
emotion-regulation strategies.
At present, the social baseline model, as well as
this Bayesian conceptualization of attachment
style, is predominantly a matter of conjecture.
As I stated at the outset, however, we have to
begin somewhere in the move from evolution-
ary, behavioral, observational, self-report, and
interview-based analyses of attachment proc-
esses to analyses based on the methods pro-
vided by rapidly developing neuroscience. I ex-
pect that future neuroscientific studies of at-
tachment will provide additional clues as to the
nature of social affect regulation in the brain.
Recommendations and
In this chapter I have sought to synthesize a
broad array of studies in the service of intro-
ducing the reader to the current state of the
neurosciences as they pertain to research on
attachment, and to propose a plausible model
of how what is known about the social brain
and affect regulation may eventually be com-
bined with attachment theory. This effort nec-
essarily included discussions of the neural con-
stituents of attachment, from neural systems
supporting emotion and motivation to those
supporting emotion- regulation, filial bonding,
familiarity, proximity seeking, and individual
differences in attachment style. What follows is
a partial list of recommendations for research-
Coan!Toward a Neuroscience of Attachment
ers excited about pursuing the neuroscience of
attachment. (Other models and suggestions can
be found in other chapters in the present vol-
ume, especially those by Simpson & Belsky;
Fox & Hane; and Polan & Hofer.)
Use designs that combine social contact with
emotional provocations. Studies of the neural
systems underlying attachment should combine
the presence or absence of attachment cues
(e.g., proximity to attachment figures) with
laboratory situations that elicit emotional re-
sponses, including threats to either the partici-
pant’s attachment system or to the participant
directly. Many theorists have proposed that the
attachment behavioral system is activated dur-
ing threats to the individual or to the individ-
ual’s attachment bond, but few studies of at-
tachment processes at the neural level have ac-
tually designed studies with this in mind.
Moreover, no work to date has sought to iden-
tify how social contact influences neural re-
sponses to positive affect elicitations.
Be sensitive to sex differences. Little is known about
how the sex of an individual under study af-
fects activity in the attachment behavioral sys-
tem, or the neural constituents of attachment.
Self- reported sex differences have been noted
in behavioral studies, however. For example,
women are more likely to endorse items indi-
cating a preoccupied attachment strategy (char-
acterized by worry that the partner will leave
them), whereas men are more likely to endorse
a dismissive-avoidant strategy (characterized by
discomfort with interpersonal closeness) (Bar-
tholomew & Horowitz, 1991). And many stud-
ies have found that women are most bothered
by their male partners’ avoidance, whereas men
are most bothered by their female partners’
anxiety (Mikulincer & Shaver, 2007). Others
have reported sex differences in relationship
stability as a function of attachment styles, sug-
gesting that attachment styles may interact in
important ways with gender roles (Kirkpatrick
& Davis, 1994). Our own work on the norma-
tive regulation of affect via social channels was
done only with women, and it may not general-
ize to men.
Pursue animal models of attachment style. To date,
virtually no studies exist of attachment styles in
non-human animals, despite growing evidence
that other personality dimensions are evident in
non-human animals (Gosling & John, 1999).
For example, King and Figueredo (1997) pro-
vided strong evidence that the “big five” per-
sonality structure and distribution is very simi-
lar in humans and chimpanzees, and the anxiety
and avoidance dimensions of attachment style
are somewhat related to the big-five traits of
neuroticism and agreeableness, respectively
(Noftle & Shaver, 2006). Other personality
traits shared to one degree or another with
humans have been observed in species as di-
verse as gorillas, hyenas, domesticated dogs,
cats, donkeys, pigs, rats, octopi, and even gup-
pies (Gosling & John, 1999). Attempts to study
attachment styles in non-human animals would
constitute a badly needed step toward bridging
the gaps between the human and animal litera-
tures addressing attachment behavior.
Allow for systemic effects in research designs.
Most attachment style research identifies effects
of a given participant’s attachment style on that
person’s own attachment behavior. One ques-
tion of great interest is the degree to which the
attachment style of one member of a dyad af-
fects the behavior of the other member. (See J.
Feeney, Chapter 21, this volume for examples.)
For instance, Coan et al. (2005) presented evi-
dence that the husband’s preoccupation score
corresponded with increased neural threat reac-
tivity throughout the wife’s brain if she was
holding the hand of a stranger (while her pos-
sibly jealous husband looked on). These sorts
of effects are likely to be numerous and are of
great interest to any neuroscience of attach-
ment. (Such findings also suggest that the ef-
fects of context are likely to be profound.)
Coan!Toward a Neuroscience of Attachment
Seek to understand contextual and situational
influences. Nearly a half-century of research
makes clear that personality is most stable
within classes of situations as opposed to
across situations (Mischel, Shoda, & Mendoza-
Denton, 2002). The question can reasonably be
asked: Is a given individual secure in her rela-
tionship with her spouse to the same degree as
she is in her relationship with her best friend
mother, or sister? Moreover, does her attach-
ment style manifest in the same way to a threat
to her relationship as it does to her personal
sense of bodily harm? Would she have en-
dorsed the same level of security during her
last relationship as she does in her current one?
Some studies suggest that within-person varia-
tion in attachment style across different rela-
tionships is substantial (La Guardia, Ryan,
Couchman, & Deci, 2000). This is likely to be
especially true at the neural level, where meas-
ures can be very sensitive to small changes in
Implement longitudinal designs. One extremely
important problem for the neuroscience of
attachment is delineating the process by which
two individuals progress from not being at-
tached to being attached (see Zeifman &
Hazan, Chapter 20, this volume for a discus-
sion of this issue). What is the rate at which
this typically occurs? How is this affected by
attachment style? With special relevance to the
present chapter, which neural structures associ-
ated with emotional responding, motivation,
and emotion regulation are particularly sensitive
to this process? For example, at what point, or
with what kinds of interpersonal experiences,
does a stranger who regulates the brain’s auto-
nomic and musculoskeletal response to threat
become a partner who regulates additional neu-
ral processes related to effortful affect regula-
tion and threat vigilance? Longitudinal studies
may also address questions of within-subject
variation in attachment style over both time and
Pursue clinical implications. As reviewed briefly
above, and by scores of other scholars in recent
decades (Cacioppo et al., 2002; Coyne et al.,
2001; Flinn & England, 1997; Harrison, Wil-
liams, Berbaum, Stem, & Leeper, 2000; House,
Landis, & Umberson, 1988; Kawachi, 2001;
Kim & McKenry, 2002; Robles & Kiecolt-
Glaser, 2003; Uchino et al., 1996; Uvnaes-
Moberg, 1998), social relationships hold major
implications for health and well-being. As the
neural mechanisms supporting these effects
become better known, it may be possible to
implement clinical interventions that not only
emphasize the forging and maintenance of
close relationships, but that also focus on the
use of social affect regulation for clinical pur-
For example, it may be possible to use certain
relationship interventions (see Johnson, Chap-
ter 33, this volume) to transform couples that
do not show a strong social regulation effect on
neural threat responding into those that do.
Johnson (2002) has already used attachment-
related marital interventions to help with the
treatment of post-traumatic stress disorder.
It warrants emphasis here that most stress-
reduction techniques involve highly individual-
ized activities (e.g., cognitive behavioral therapy,
mindfulness meditation) that may be less effi-
cient or more costly than using social networks
or attachment relationships in the implementa-
tion of affect-regulation strategies. Few or no
interventions are designed with this specifically
in mind, and even those that are rarely if ever
offer training in how to allow oneself to be
soothed by another person.
Finally, the careful delineation of neural sys-
tems underlying attachment stands to expand
our basic understanding of a wide variety of
disorders that implicate social processes. The
potential exists for this work to inform research
on disorders ranging from autism to fragile X
syndrome, Williams syndrome, depression, so-
Coan!Toward a Neuroscience of Attachment
cial anxiety, schizophrenia, and virtually all of
the personality disorders (most or all of which
are more or less defined in terms of social be-
Differentiate behavioral from neural systems. A major
challenge to future neuroscientists interested in
the study of attachment will be the temptation
to think of the attachment behavioral system as
a unitary neural construct, which it almost cer-
tainly is not. A host of neural processes, each
with its own unique problems to solve, con-
tribute to what we have come to call the at-
tachment behavioral system, and the attach-
ment behavioral system may indeed be little
more than a convenient rubric for describing
the collective social activities of social bonding
and social affect regulation. On the other hand,
the attachment behavioral system may repre-
sent an emergent property of its constituent
neural components that is, under some condi-
tions and in some situations, relatively irreduci-
Collaborate. The neuroscience of attachment
represents uncommonly fertile ground for a
wide variety of researchers, from neuroscien-
tists to psychologists, biologists, physicians,
epidemiologists, and others. Individuals from
diverse scientific traditions stand to contribute
many essential pieces to this fundamentally im-
portant puzzle. Because this area is so necessar-
ily multidisciplinary, researchers interested in
these and related questions will do well to ex-
plore contacts in related disciplines as their par-
ticular research questions call for it (Cacioppo
et al., 2007). It is for precisely this reason that
collaborations are increasingly the norm among
the social, cognitive, and affective neurosci-
ences. Such collaborations enrich the science,
and often richly reward the scientists who take
part. When such efforts are focused on a ques-
tion as fundamentally important as the neuro-
science of attachment, it is expected that col-
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... Interestingly, attachment to parental gures is inherently awed, because parents do not satisfy infants' every affective requirement in an effort to build their self-suf ciency (Mayseless & Popper, 2007). As a result of this awed relationships, certain affective needs remain unmet and a desire for an ideal attachment gure is created, which in turn sets the foundation for an individual's attachment style (Coan, 2008). Parents as attachment gures and ultimate in uencers affect how individuals confront identity-constructing dilemmas (Berzonsky, 2011), which also impacts the way a leader-follower relationship will be constructed (Yip et al., 2018). ...
... Seeking proximity in times of distress is a natural reaction (Mawson, 2005), because the calming effect of being close to attachment gures stimulates dopamine and reduces negative emotions and anxiety that panic or uncertainty causes (Coan, 2008). Individuals seek relatedness in their interpersonal relationships; therefore, leaders perceived as attachment gures can become idealized, depending on the combination of attachment styles (Davidovitz et al., 2007). ...
... That study found that anxious-depressive emotions in thirteen-to-sixteen-year-olds were lower in the presence of a close other, but did not differ between the adolescent being alone or with peripheral company. These findings were interpreted as reflecting the importance of social support in coping, and as evidence that, within a close relationship, even entirely passive social support (i.e., 'supportive presence') aids emotion regulation (Beckes & Coan, 2011;Coan, 2008;Coan et al., 2006). ...
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The frequency, intensity and variability of emotional experiences increase in early adolescence, which may be partly due to adolescents’ heightened affective sensitivity to social stimuli. While this increased variability is likely intrinsic to adolescent development, greater mood variability is nevertheless associated with the risk of internalising psychopathology. Early adolescents (N = 58, ages 13–14) reported their social context and mood when prompted by a smartphone application. Valence, arousal, and their variability were compared across social contexts using multilevel regression models. Social contexts were defined by the presence of close others, peripheral others, both, or neither. Arousal was lower when alone. Valence was lower and more variable, and arousal was more variable when alone than in either close or peripheral company. This is the first time that level and variability of valence and arousal in adolescent affect have been shown systematically to differ for the same individual in different daily-life social contexts.
... Similarly, the original focus on attachment to parental figures has been expanded to encompass romantic partners, parents, siblings, children and friends (Doherty and Feeney, 2004), adult relationships (Allen and Land, 1999;Heffernan and Fraley, 2015;Overall et al., 2015) and the ways in which attachment influences parenting styles (Jones et al., 2015;Young et al., 2017). The neuroscience of attachment has also been progressively developed (Insel and Young, 2001;Insel and Fernald, 2004;Montague and Lohrenz, 2007;Coan, 2008;Neumann, 2008;Coan, 2010;Panksepp, 2011;Gillath, 2015;Feldman, 2017). Attachment theory is now central to research and academic agendas within clinical applications (Fonagy and Campbell, 2015), adult psychopathology (Ein-Dor and Doron, 2015), and more recently learning (Luyten et al., 2017a,b) and pedagogy (Csibra and Gergely, 2009). ...
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Attachment theory is one of the key theoretical constructs that underpin explorations of human bonding, taking its current form in John Bowlby's amalgamation of ideas from psychoanalysis, developmental psychology and ethology. Such a period of interdisciplinary exchange, and Bowlby's interest in Lorenz' concept of imprinting in particular, have been subject to rather historical and biographical studies, leaving a fine-grained theoretical scrutiny of the exact relationship between imprinting and attachment still pending. This paper attempts to remedy such an omission by exploring the relationships between these two constructs. It critically reviews the theories of imprinting in general, of human imprinting in particular, and of attachment; analysis of the links between these processes bring to the foreground the distinction between supra-individual vs. individual aspects of bonding, the relevance of 'proto-attachment' phases before 'proper' Bowlbyan attachment is attained, and the role of communicative signals during such early phases. The paper outlines potential benefits of considering such elements in the study of early social cognition, particularly in respect of the study of the gaze and the infant-directed communicative register.
... Duygu düzenleme, çiftlerin bu olumsuz durumları sağlıklı şekilde atlatmalarını sağlar. Çiftten birinin duygu düzenleyebilmesi, kendi duygusal uyarılmasının yanı sıra eşininkinin de dengelenmesine yardımcı olabilir (Coan, 2008;Diamond ve Aspinwall, 2003;Kappas, 2011). ...
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In this study, interpersonal emotion regulation strategies and intolerance of uncertainty levels of individuals were investigated. A descriptive study was conducted and the relational screening method was used. The study group of the research consists of 320 individuals. As data collection tools, "Personal Information and Questionnaire Form", to determine individuals' emotion regulation strategies "Interpersonal Emotion Regulation Scale (IERS)", to measure the intolerance of uncertainty levels "Intolerance of Uncertainty Scale (IUS-12)" were employed. In addition to the descriptive statistics (mean, standard deviation, frequencies), independent samples t-test, one-way ANOVA, Pearson's Product-Moment Correlation and multiple linear regression analyses were conducted since the assumptions of the parametric tests were met. As a result of the statistical analyses, while no statistically significant difference was yielded in all sub-dimensions of interpersonal emotion regulation based on the individuals' mean scores according to the gender variable, a significant difference was revealed regarding the sub-dimension of gaining a perspective in favour of the 41-50 age group in terms of the age variable, and in favour of married individuals with respect to the marital status variable. It was detected that there is a negative relationship between intolerance of uncertainty and the sub-dimensions of interpersonal emotion regulation. In addition, it was observed that as sub-dimensions of the intolerance of uncertainty, %10 of the variation in the concern for the future, and %3 of the variation in the inhibitory anxiety are predicted by interpersonal emotion regulation variable.
Change agents influence employee attitudes in order for organizations to change. In an effort to unravel this influence mechanism, we examined the change leader-recipient relationship. More specifically, how change leaders’ championing (independent variable) relates to recipients’ readiness to change (dependent variable). Our conceptual model of change leaders’ prosocial sensegiving is based on adult attachment theory operationalized through storytelling. To test our model, we surveyed 164 change recipients undergoing organizational change in various industries. Results confirm the first part of our model: psychological need satisfaction partially mediates the relation between change leaders’ championing and recipients’ readiness to change. In other words, prosocial change leaders act as attachment figures alleviating anxiety caused by ambiguity addressing change recipients’ proximity-seeking behaviour. Despite what has been described in scholarly works, change leaders’ methods of persuasion seem to be a more accurate indicator of recipients’ readiness for change. Part two of our hypothesized model could not be confirmed: moderation effects of leader influence and narrative intelligence could not be confirmed. We conclude that prosocial change leaders’ who demonstrate narrative intelligence use stories to elicit an emotional response from change recipients, effectively increasing their perceived psychological need satisfaction, ultimately affecting their readiness to change. MAD statement Our research aims to deconstruct the underlying mechanics of prosocial organizational change leadership. We study how change leaders utilize championing, narrative intelligence and leadership influence tactics in an effort to influence change recipients’ change-related attitudes and affect their individual readiness to change. We confirm that change recipients’ psychological need satisfaction partially mediates this relationship and that the direct application of leadership influence tactics is a better predictor, contrary to what literature suggests. We recommend practitioners create compelling narratives in an effort to enhance message reception, and utilize specific leadership influence tactics to ensure the message is received.
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This introduction aims to set out the potential as well as some of the pitfalls of the newly emerging area of the Social Neuroscience of Human Attachment (SoNeAt). To organize and interconnect the burgeoning empirical studies in this line of research, including those in this special issue, we outline a programmatic framework including an extension of our conceptual proposals NAMA and NAMDA to guide future research. We hope that this special issue will act as a stimulus for redoubling our efforts advancing the newly emerging SoNeAt area bridging attachment theory and social neuroscience.
Background Insecure attachment style (anxious and avoidant) predisposes to the development of depression and has been linked to hippocampal alterations in healthy individuals. However, it is unclear if there are alterations of the hippocampus and the parahippocampal cingulum (PHC) in patients with depression. Methods Forty-eight patients with major depressive disorder and 18 healthy controls underwent MP2RAGE and diffusion-weighted magnetic resonance imaging. Attachment characteristics were assessed with the revised adult attachment scale. Patients were classified into subgroups with low (anxious: n = 27; avoidant: n = 21) and high (anxious: n = 20; avoidant: n = 28) attachment characteristics. Bilateral PHC were reconstructed using manual tractography. Hippocampal volumes, mean fractional anisotropy and mean diffusivity (MD) in bilateral PHC were compared between attachment subgroups and healthy controls. Results Patients had higher scores of anxious and avoidant attachment, which were associated with depression severity. Patients with high avoidance had decreases in hippocampal volumes in comparison to patients with low avoidance. Furthermore, patients with high avoidance had increased MD in bilateral PHC in comparison to patients with low avoidance and in comparison to healthy controls. Limitations Assessment of attachment characteristics may be influenced by cognitive biases due to depressive symptoms Conclusions High attachment avoidance in patients with depression is associated with volume reductions in the hippocampus and impaired PHC-microstructure.
In the field of child development, attachment theory is one of the most visible and empirically grounded conceptual frameworks. This chapter explores key tenets of attachment theory in an applied context to give its theoretical underpinnings concrete meaning for understanding caregiver-child attachments across racially, ethnically, and socioeconomically diverse individuals and families, as well as diverse family and nonrelative relationships. Attachment theory is of particular interest for contemporary families given the dynamic and complex nature of the relationships that children form with caregivers both inside and outside the family, and across the lifespan.
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An integrated model of the development of attachment behavior and verbal behavior is presented. Both phenomena are described developmentally in terms of the emergence of other persons as learned, social reinforcers. Attachment behavior impacts social network preferences, and verbal behavior entails skills for effectively navigating those networks.
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Reviews studies of frontal EEG asymmetry as a measure of state and trait indices of positive and negative emotions, and the interactions with the functioning of the left and right cerebral hemispheres. Future directions of the research are also discussed. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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Stressful life experience can have significant effects on a variety of physiological systems, including the autonomic nervous system, the hypothalamic-pituitary-adrenal axis, and the immune system. These relationships can be bidirectional; for example, immune cell products can act on the brain, altering mood and cognition, potentially contributing to depression. Although acute physiological alterations may be adaptive in the short term, chronic or repeated provocation can result in damage to health. The central dogma in the field of stress research assumes a stereotyped physiological response to all stressors (the generality model). However, increasing evidence suggests that specific stressful conditions and the specific way an organism appraises these conditions can elicit qualitatively distinct emotional and physiological responses (the integrated specificity model). For example, appraisals of threat (vs. challenge), uncontrollability, and negative social evaluation have been shown to provoke specific psychobiological responses. Emotional responses appear to have specific neural substrates, which can result in differentiated alterations in peripheral physiological systems, so that it is incorrect to presume a uniform stress response.
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Social neuroscience is a new, interdisciplinary field devoted to understanding how biological systems implement social processes and behavior. Social neuroscience capitalizes on biological concepts and methods to inform and refine theories of social behavior, and it uses social and behavioral constructs and data to inform and refine theories of neural organization and function. We focus here on the progress and potential of social neuroscience in the area of mental health. Research in social neuroscience has grown dramatically in recent years. Among the most active areas of research we found are brain-imaging studies in normal children and adults; animal models of social behavior; studies of stroke patients; imaging studies of psychiatric patients; and research on social determinants of peripheral neural, neuroendocrine, and immunological processes. We also found that these areas of research are proceeding along largely independent trajectories. Our goals in this article are to review the development of this field, examine some currently promising approaches, identify obstacles and opportunities for future advances and integration, and consider how this research can inform work on the diagnosis and treatment of mental disorders. © 2007 Association for Psychological Science.
Positive social interactions, including affiliations and social bonds, dominate the behavioral repertoire of humans and many higher vertebrates. Pair bonding is an evolved trait and may play a critical role in reproduction, as well as in individual and species survival. The neurobiology of pair bonding or other forms of social affiliation are most readily understood in this context. The purpose of this chapter is to examine mechanisms underlying social affiliation and social bonds, including research from rodents, sheep, and primates. We also discuss these findings in light of phylogeny, ontogeny, and the clinical implications of social bonding. Various forms of positive social behaviors, including pair bonding and maternal-infant behavior, rely on shared neural and endocrine systems. Steroid hormones, although integral to social and maternal bonding, do not exclusively code for these events; they also influence sexual behavior, feeding behavior, and exploratory behavior and thus have the recruiting capacity for a wide range of neural as well as somatic systems. Steroid hormones have their action in the brain by binding to DNA motifs at the promoter regions of certain genes, many of which code for neuropeptides and their receptors. Among the neuropeptides that support the formation and coordinate the autonomic and behavior states associated with bonding are oxytocin, endogenous opioids, vasopressin, and corticotropin-releasing hormone.
Traditional approaches have long considered situations as “noise” or “error” that obscures the consistency of personality and its invariance. Therefore, it has been customary to average the individual's behavior on any given dimension (e.g., conscientiousness) across different situations. Contradicting this assumption and practice, recent studies have demonstrated that by incorporating the situation into the search for consistency, a new locus of stability is found. Namely, people are characterized not only by stable individual differences in their overall levels of behavior, but also by distinctive and stable patterns of situation-behavior relations (e.g., she does X when A but Y when B). These if … then … profiles constitute behavioral “signatures” that provide potential windows into the individual's underlying dynamics. Processing models that can account for such signatures provide a new route for studying personality types in terms of their shared dynamics and characteristic defining profiles.
The evolutionary continuity between humans and other animals suggests that some dimensions of personality may be common across a wide range of species. Unfortunately, there is no unified body of research on animal personality; studies are dispersed across multiple disciplines and diverse journals. To review 19 studies of personality factors in 12 nonhuman species, we used the human Five-Factor Model plus Dominance and Activity as a preliminary framework. Extraversion, Neuroticism, and Agreeableness showed the strongest cross-species generality, followed by Openness; a separate Conscientiousness dimension appeared only in chimpanzees, humans' closest relatives. Cross-species evidence was modest for a separate Dominance dimension but scant for Activity. The comparative approach taken here offers a fresh perspective on human personality and should facilitate hypothesis-driven research on the social and biological bases of personality.
Substantial evidence from animal studies suggests that enhanced memory associated with emotional arousal results from an activation of beta-adrenergic stress hormone systems during and after an emotional experience. To examine this implication in human subjects, we investigated the effect of the beta-adrenergic receptor antagonist propranolol hydrochloride on long-term memory for an emotionally arousing short story, or a closely matched but more emotionally neutral story. We report here that propranolol significantly impaired memory of the emotionally arousing story but did not affect memory of the emotionally neutral story. The impairing effect of propranolol on memory of the emotional story was not due either to reduced emotional responsiveness or to nonspecific sedative or attentional effects. The results support the hypothesis that enhanced memory associated with emotional experiences involves activation of the beta-adrenergic system.
Functional magnetic resonance imaging (fMRI) affords an unprecedented window onto function in the intact human brain. This chapter describes imaging methods using the blood oxygenation level dependent (BOLD) technique of fMRI. Experimental designs and image analysis methods for examining neural activity related to attention are discussed. Attention-related neural changes can reflect either: (1) different modulatory effects on information processing, or (2) the activity of control systems that invoke and regulate those modulatory effects. At the current stage of fMRI research, only some effects in the former category have been reported. Although the latter category has not been studied with fMRI, appropriately designed fMRI studies may help to identify the components of attentional control systems. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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