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Toward a Neuroscience of Attachment

August 2008

In book: Handbook of attachment: Theory, research, and clinical applications (pp.241-268)
Edition: 2nd
Chapter: 11
Publisher: Guilford Press

Project: Social Baseline Theory

Authors:

University of Virginia

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.

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FROM THE HANDBOOK OF ATTACHMENT:

THEORY, RESEARCH, AND CLINICAL IMPLICATIONS

JUDE CASSIDY AND PHILIP R. SHAVER, EDS.

2nd Edition

Pages 241 - 265

The Guilford Press, NY

TOWARD A

NEUROSCIENCE OF

ATTACHMENT

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: jcoan@virginia.edu • www.socialbaseline.com

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

scope.

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

constituents.

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

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-

tachment.

The Neural Constituents of

Attachment

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

Elements

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,

1994).

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 brain’s 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

persistent.

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

childhood.

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-

ance.

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

outcome.

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

threat.

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

figures.

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

volume).

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-

ships.

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

activities—including

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

savings.

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-

pothalamus).

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

accumbens).

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

gyrus).

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

investigation.

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

Conclusions

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

context.

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

relationships.

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-

poses.

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-

haviors).

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-

ble.

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-

laborative efforts will be embraced with great

enthusiasm.

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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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ATTACH HUM DEV

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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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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.

The Neurobiology of Social Affiliation and Pair Bonding

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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.

Situation-Behavior Profiles as a Locus of Consistency in Personality

Article

Apr 2002

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.

Personality Dimensions in Nonhuman AnimalsA Cross-Species Review

Article

Jun 1999

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.

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Susan M Johnson

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Article

Oct 1994
NATURE

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 and the study of attention.

Article

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)

Attachment in Adulthood: Structure, Dynamics, and Change

Article

Feb 2009
J NERV MENT DIS

Sharon Bond

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