CHAPTER FIVE

“SOLE MATES”: THE BIOLOGY OF ATTACHMENT AND TRUST

I just wanted to say thank you . . . I was stuck in the same old job, barely making ends meet . . . I tried Liquid Trust and I finally got a very nice corporate job . . . While I was using Liquid Trust my relationship with my girlfriend wasn’t going well. Without really knowing what was going on it went from bad to wonderful. Best of all, she asked me to marry her! I would highly recommend this product . . .

—JOE^*

WHAT IF THERE REALLY WAS A POTION THAT COULD make people love you, trust you, believe in you just by applying a perfumelike spray when you got dressed in the morning? That’s the promise of Liquid Trust, “the world’s first trust-enhancing spray.”

Skeptical? Maybe you forgot to spritz yourself this morning.

In a time-honored tradition, marketers have taken a grain of science, mixed it with a serving of hype, and created a product that can “instantly build relationships that were never possible before!” The active ingredient, oxytocin, is a hormone doctors have administered to thousands of women over the past thirty years. Where did the idea that oxytocin could enhance trust and relationships come from?

Research on the biology of trust and relationships has become one of the most provocative frontiers of neuroscience (and may have made the marketing of such potions inevitable). In this chapter, we’ll explore the nature of attachment—the social glue that binds us together and the foundation of our capacity to love.

The drive to attach, to affiliate, and to bond with other people begins from the earliest moments of life. It is one of those essential functions that our brains are wired to perform. Our lives are organized around attachments—first with our parents, then friends, lovers, and our children. Recent research shows that all of these bonds may share an underlying biology that involves a symphony of hormones and brain circuits.

THE GLAND THAT ROCKS THE CRADLE

THE STORY OF ATTACHMENT STARTS AS THE MOMENT OF BIRTH APPROACHES. It’s a little like prepping for a blockbuster event—the opening ceremony of the Olympics, a state dinner, the Oscars—a million details have to be coordinated in just the right sequence. Behind the scenes, a cascade of hormones, enzymes, and neurotransmitters have been preparing the mother’s body and brain for the remarkable task of extruding another human being and then making sure the helpless newborn survives.

And after eons of experience, natural selection has put a big burden for the event planning on the shoulders of a little peptide called oxytocin. Made from a string of just nine amino acids, oxytocin helps the mother push out the baby, gets the breast milk flowing, and makes the mother’s brain see the squirming, crying infant as a bundle of joy. As the due date draws near, a series of chemical brakes come off the mother’s pituitary gland, allowing it to make increasing amounts of oxytocin, which are released in pulses into her bloodstream.¹ As she goes into labor, oxytocin stimulates uterine contractions, bringing the painful process of childbirth into full swing. At the same time, oxytocin from the mother’s blood (and maybe also from the fetal brain), prepares the baby for its own ordeal. It dials down the metabolic demands of the fetal brain, protecting it from a drop in oxygen and glucose that might occur during the birth process.² Meanwhile, other hormones, including estrogen and prolactin, have been stimulating the mother’s breasts to fill with milk. After the baby is born and begins to suckle, oxytocin triggers the milk to drop into the canals in the breast and nipple so that it can be delivered to the infant.

Meanwhile, the sight, smell, and touch of the baby stimulate the release of oxytocin in the mother’s brain, priming her to love and care for her infant. How? The answer seems to be that oxytocin stimulates the brain’s reward circuits that give us feelings of pleasure. One has to marvel at the economy and efficiency of the whole thing.

Scientists and physicians have known for a century oxytocin played a crucial role in delivery and breastfeeding. Since the 1950s, obstetricians have used intravenous oxytocin (a.k.a. Pitocin) to accelerate delivery when labor is dangerously prolonged or to induce labor when a fetus is too far past its due date. But only recently have we learned that oxytocin is a key factor in maternal care, leading to the remarkable discovery that this same hormone may be a key player in how we form attachments, develop trust, and nurture our relationships with our friends, lovers, and spouses.

MOTHER’S LITTLE HELPER

IT TURNS OUT THAT UNTIL THEY HAVE OFFSPRING OF THEIR OWN, many mammals have very little interest in infants. Virgin rats, for example, typically ignore or even reject pups. But in the 1980s researchers found that, by infusing oxytocin into a virgin rat’s brain, they could bring out her inner mother, switching on the full spectrum of maternal instincts.³ Conversely, blocking oxytocin receptors prevents the normal triggering of maternal behavior in rats, while mice in whom the oxytocin gene has been removed don’t even recognize their own infants.⁴ In the years that followed, increasingly sophisticated experiments have confirmed that oxytocin is a potent “mommy hormone” in species as diverse as sheep, monkeys, and even humans.

How does it work? The evidence suggests that oxytocin participates in at least two chemical shifts that occur in the mother’s brain and help her fall in love with her baby. One is a subtle change in her threshold for approach vs. avoidance. Oxytocin binds to receptors in the amygdala and other regions of the brain’s limbic (emotional) system to reduce social fears and aversions. It acts like a kind of social Valium—making her more responsive to her infant’s distress. Human mothers are acutely attuned to the cries of an infant and respond with approach behaviors whereas nonmothers often find the sound of a baby crying aversive.⁵

But that doesn’t account for the passion mothers feel when they see, smell, and touch their newborn infants. Rat studies have shown that, in the presence of other reproductive hormones like estrogen, oxytocin receptors sprout and activate dopamine pathways in the brain’s reward circuits. Dopamine is well known as the key neurotransmitter in the brain’s pleasure centers—the same chemical responsible for the euphoric effects of cocaine. In essence, the rat pup now acts like a drug, and this “baby buzz” provides a powerful motivator for maternal behavior. Pups are actually more potent than drugs: shortly after giving birth, rat mothers prefer pups to cocaine and even food. Mothers will even cross an electrified grid to get to their pups.⁶

It’s not entirely clear if the same story plays out in humans, but there is mounting evidence that it may. They may have been born yesterday, but infants are no dummies when it comes to giving off cues that captivate their moms. As the ethologist Konrad Lorenz observed, a baby’s face is a powerful “releaser” of maternal care and nurturing. Lorenz defined the prototype of cute (which he referred to as Kindchenscema, or “baby schema”): protruding cheeks, high forehead, large eyes below the midline of the skull, and a small nose and mouth. If that sounds like Mickey Mouse, it’s no coincidence.

According to recent studies, reproductive hormones actually bias the female brain to perceive and respond to cuteness. Women are better than men at identifying Kindenschema (that is, cuteness) features, and premenopausal women (especially those on oral contraceptives) do best, suggesting that female reproductive hormones prime a woman’s brain to respond to cute signals.^7, 8 And, consistent with the animal studies, brain-imaging studies of women have shown that smiling babies and cute babies activate the brain’s reward system.^9, 10 In addition, when mothers are shown videotapes of their infant in distress, brain regions involved in mind reading, empathy, and emotional vigilance are also powerfully engaged, reflecting a deep attunement to their baby’s feelings and the powerful impulse to comfort and protect.¹¹

LOVE POTION #9

SO THE CONNECTION BETWEEN REWARD CIRCUITS AND REPRODUCTIVE hormones like oxytocin is crucial to bonding mothers and their babies. But that’s not all. The same systems seem to help bond us to our soul mates.

Beavers, bats, and marmosets are members of an exclusive clique—“The 3 Percent Club.” Only about 3 percent of mammals are monogamous.¹² In modern neuroscience, a rodent known as the prairie vole has become an icon of monogamy. Prairie voles form pair-bonds, and males resemble the ideal husband: they make a lifelong commitment and share equally in parenting the children. If one mate dies, the survivor is unlikely ever to seek a new partner. By comparison, their close relatives, the montane vole and the meadow vole, are cads: males and females are promiscuous, uncommitted, and even abandon their young. What is going on in the brain that makes some animals “true blue” and others hopeless philanderers? The evidence points to oxytocin and to its sister hormone, vasopressin (also known as arginine vasopressin [AVP]).

Oxytocin and vasopressin are both made in and released from the hypothalamus, the master regulator of most hormone systems in the body. The genes for these two peptides sit near each other on chromosomes in all vertebrate species (including us). And that’s no coincidence. Somewhere before vertebrates and invertebrates diverged in evolutionary history, an event that scientists refer to as gene duplication happened. In some ancient ancestor of vertebrate animals, a DNA copying error was made that inserted an extra copy of the original gene next door. Over time, mutations in the two sister genes resulted in two distinct hormones. Both oxytocin and vasopressin consist of nine amino acids, but they differ by two, a difference that has had profound effects on animal life.¹³

In the early 1990s Sue Carter at the University of Maryland and scientists at Emory University, including Thomas Insel and Larry Young, began a series of studies that have given scientists the most detailed picture yet of the biology of affiliation and attachment. When they put a male and female vole together and allowed them to cohabitate or mate, they found a remarkable difference between prairie voles and montane voles. For prairie voles, the act of mating or cohabitating triggers a profound bond—the couple will prefer each other to other voles. But to montane voles, the time they spent together and the sex they had means nothing. The reason involves oxytocin and vasopressin—but in ways that depend on the sex of the animal.

For females, the major love potion is oxytocin; for males, it’s vasopressin. Injecting oxytocin in the brain of a female prairie vole triggers pair bonding by activating oxytocin receptors in reward centers. In the natural setting, that’s essentially what cohabitating and mating do—they cause the release of oxytocin, which binds to receptors in the nucleus accumbens, a key node in the brain’s reward circuit where dopamine signals pleasure.¹⁴ Sound familiar? That’s essentially the same story I told you about mothers bonding to their infants. In both cases, an event (nursing or mating) stimulates oxytocin release, which in turn stimulates pleasure centers that stamp “joy!” all over the experience of the other (baby or mate). Female prairie voles have more oxytocin receptors in the nucleus accumbens than do nonmonogamous species like meadow voles (and rats and mice),¹⁵ and that may explain why female prairie voles make better partners.

In males, though, vasopressin is the major player in pair-bonding. After a male prairie vole mates with a female, vasopressin induces him to bond with her, fight off other males, and, later, care for their offspring. And the action is, once again, in the receptors. The vasopressin 1a receptor (known as AVPR1A) is more abundant in reward circuits of prairie voles than in their promiscuous cousins, the montane and meadow voles. Larry Young’s group at Emory was able to turn gigolos into gentlemen by increasing AVPR1A in a reward region of the male meadow vole brain. The male meadow voles now bonded to their female partners, just like prairie voles do.

The astounding implication of this work is that a single gene might make the difference between something as complex as whether an animal spends its life in a committed relationship or playing the field. While a postdoctoral fellow in Thomas Insel’s lab, Larry Young discovered a subtle but important difference in the gene that makes the AVPR1A receptor in prairie voles and montane voles. The part that carries the instructions for making the protein is identical in the two species. The difference lies in the DNA sequence of the gene’s promoter—the part of the gene that determines where and when the gene will turn on. The prairie vole gene, they found, has extra repeated sequences in the promoter. When they took the prairie vole gene and inserted it into mice (who are not the most socially engaging of animals), the mice became more interested in other mice. Differences in this promoter sequence of the gene seem to determine how much of the vasopressin receptor is made and correlates with how socially monogamous voles are.^*

Research on voles hasn’t fully answered the question of how mammals (even voles) end up building a family. But it has given us a fascinating account of how natural selection has engineered a system for solving an adaptive problem—that is, how to bond mammals to their infants and their mates. The answer, admirable in its efficiency, has been to “double-dip.” Take a neuropeptide that likely evolved to facilitate female childbirth and lactation (oxytocin) and one that promoted male guarding of offspring and mates (vasopressin) and link them to dopamine-dependent reward systems in the brain. The result: mothers and fathers who care for their young and commit to each other.

But does the vole story tell us anything about human love and attachment? The answer is we don’t know yet, but there are certainly clues that it might. Humans have genes for oxytocin, vasopressin, and their receptors that are very similar to those in other mammals. And, like its vole counterpart, the human AVPR1A gene also has repeated DNA sequences in the promoter region that differ among people. Could these genetic variations affect male pair-bonding in humans?

Researchers at the Karolinska Institutet in Sweden tested that hypothesis in a study of more than 550 couples.¹⁸ They had the couples complete a questionnaire that measured partner bonding, with questions like: How often do you kiss your mate? How often are you and your partner involved in common interests outside the family? Have you discussed a divorce or separation with a close friend?

Men who carried one variant of the AVPR1A gene reported lower partner-bonding scores and were more likely to be unmarried or to have major marital problems.

Oxytocin also seems to affect how couples interact. In one study, researchers asked forty-seven couples to pick two areas of their relationship that were a source of conflict.¹⁹ They then had the couples inhale a nasal spray that contained either oxytocin or a placebo and asked them to discuss the conflict issues for ten minutes while trained observers rated their verbal and nonverbal behavior using standardized scales. The couples who had inhaled oxytocin had more positive interactions and lower levels of the stress hormone cortisol. Other studies have found that variation in the oxytocin receptor gene are associated with partner-bonding and romantic closeness among couples.²⁰

Brain-imaging studies support the idea that romantic love and mother-infant bonding rely on shared brain biology. In a British study, volunteers who claimed to be “truly, deeply, and madly in love” underwent fMRI scans while they looked at pictures of their beloved.²¹ When the results were compared to scans of women looking at pictures of their babies, the overlap was striking. Both romantic love and maternal love activated brain regions rich in oxytocin and vasopressin receptors and those involved in reward circuitry.²²

Larry Young has even speculated that if the neural foundations of romantic love involve tweaking systems that evolved for maternal-infant bonding, we might need a new perspective on human love and sexuality. “The stimulation of the cervix and nipples during sexual intimacy are potent releasers of brain oxytocin,” he points out, “and may function to strengthen the emotional tie between partners.” Is this why some men are so ga-ga over women’s breasts? Could foreplay be about turning on those “ancient maternal bonding systems”?”²³ If you need proof that there’s some kind of link, consider this: according to an unscientific search of Billboard.com, there are more than forty thousand songs with the word baby in their title—and most of them are not about infancy. Let’s just say that “Hit Me Baby One More Time!” is not an ode to maternal masochism.

In a funny way, modern neuroscience may be turning Freud’s ideas on their head. Freud’s claim was that infants’ relationships to their mothers are based on sexual desires; neuroscience suggests that mothers’ sexual relationships are based on their love for their infants. Either way, we’re probably going to need a lot of therapy.

So it may well be that natural selection used this basic blueprint for wiring both maternal love and pair-bonding in mammals as diverse as voles and humans. Of course, no one would claim that that’s all there is to human relationships. Human love is undoubtedly much more “splendored” than neuropeptides and dopamine. But it may have roots in the bond between a mother and her baby.

ATTACHING IMPORTANCE

IN THE PAST 150 YEARS, PSYCHOLOGISTS AND PSYCHIATRISTS have proposed innumerable theories of how the human mind works. Most of them are born and die in obscurity. But every so often, one of these ideas takes hold and changes the way we view ourselves in some fundamental way—shifting paradigms and launching whole new directions for research and, sometimes, clinical practice. The most powerful of these ideas move beyond the rarified world of science to shape popular conceptions of human nature. Those ideas that survive usually have two features: a persuasive champion and an explanatory model that seems at once contrarian and profoundly clarifying, and then self-evident. Often there is a third element: the idea seems to arrive at a moment when it resonates with the social politics of its age. Sigmund Freud was a prolific and brilliant communicator of his psychoanalytic theories. His claim that we are endowed from infancy with sexual and aggressive drives that explain our dreams, desires, fears, and neuroses at first seemed absurd and even scandalous. But the explanatory power of psychoanalytic theory eventually triumphed and became a dominant paradigm by which both professionals and later the public came to see human behavior.

Behaviorism, the main competitor to Freudian psychoanalytic models, grew out of the work of John Watson, B. F. Skinner, and others who claimed that the human mind is a blank slate on which experience writes the scripts for our behavior. The idea that all behavior is learned—by conditioning, reinforcement, and punishment—and therefore is eternally malleable fit well with the American ideals of equality, pragmatism, and opportunism. The appeal of learning theory broadened with the backlash against biological determinism that developed in the aftermath of the racist eugenics of Hitler’s Germany.

But in the 1950s another paradigm-shifting idea about human development began to take hold. Its leading proponents were John Bowlby, a British psychiatrist and psychoanalyst, and his colleague Mary Ainsworth, an American psychologist. In the 1940s, Bowlby wanted to understand the effect of early maternal separation on child development. It was a question that had become particularly poignant in the wake of World War II after untold numbers of children were left motherless. In fact, Bowlby had been commissioned by the World Health Organization to prepare a report about the outcomes of children without families and as he researched the issue, he found psychoanalytic concepts wanting.

In 1952 Bowlby’s colleague Jimmy Robertson made a powerful but low-budget film called A Two-Year-Old Goes to the Hospital, about a healthy two-and-a-half-year-old little girl named Laura who is admitted to the hospital for a minor operation. As was the custom, her mother leaves the child in the care of the hospital team. Using a handheld camera, Robertson simply documented the eight days of her stay without narration. But no narration was needed. As the days go by, Laura becomes visibly shaken and frightened, with plaintive cries of “I want my mummy” and “I want to go home.” She begins to be more withdrawn at her mother’s visits. On the eighth morning, “she is shaken by sobs.”²⁴ The film was instrumental in changing hospital policies to allow visiting and overnight stays by parents to minimize separation distress.

Psychoanalytic theory and behaviorism could scarcely have had a more different view of child development, but neither of them showed much interest in concepts like love and attachment per se. In fact, their explanation for the infant’s bond to its mother was ultimately similar: it was a side effect of gratification. To the psychoanalyst, it was about satisfying the child’s oral desires for the breast; to the behaviorist, the child’s apparent affection was simply behavior reinforced by feeding and other pleasurable stimuli. But those accounts seemed incomplete to Bowlby. They didn’t capture something fundamental about the child’s attachment to its mother, and he began to look for other explanations.

He found them in part in the work of ethologists who had been writing about their observations of animal behavior. He knew of Konrad Lorenz’s work showing that goslings had an innate capacity to “imprint” on their mothers. But even more relevant was the work of an American psychologist named Harry Harlow, who had been studying maternal deprivation in rhesus monkeys. Harlow’s experiments have since become part of the canon of developmental psychology—familiar to almost anyone who has taken an introductory psychology course in the past fifty years.

A MOTHER OUT OF WHOLE CLOTH

HARLOW WAS TRYING TO IDENTIFY THE ACTIVE INGREDIENT IN maternal-infant bonding. Where Freud famously asked “What does a woman want?” Harlow wanted to know “What does a baby want?” What was the infant seeking by attaching to its mother? To answer that, he took sixty newborn rhesus macaque monkeys away from their mothers on the first day of life and raised them in a laboratory. Harlow and his team soon noticed that the infants developed a strong connection with the cheesecloth blankets that lined the floors of their wire cages.²⁵

When the blankets were taken away, the monkeys became violently emotional and oppositional. Was there something about the contact with the cheesecloths they craved? Were these motherless babies findings some “mother-ness” in the softness of the blankets? Harlow decided to create two kinds of “mother surrogates” and mount them in the infant’s cages to see what effect they would have. The cloth mother was a cylinder of wood covered in terry cloth, and the wire mother was a wire-mesh cylinder of the same size. Bottle holders were installed in the upper part of the “mother” to provide milk. The only real difference between the cloth mother and the wire mother was a layer of cloth—a soft exterior that would provide some comfort to the touch. But that difference was anything but small.

In Harlow’s classic experiments, half the monkeys were fed by the cloth mother and the other half by the wire mother. He observed the infants with their surrogate mothers for about six months. Regardless of which mother fed them, the infants spent almost all of their time holding on to the cloth mother. When Harlow introduced a series of fear-evoking stimuli (e.g., a moving toy bear), infants raised on the cloth mother ran and clung tightly to her. After a few minutes, they were soothed and relaxed and start exploring. But the infants raised by the wire mother clutched themselves, rocked back and forth, and cried out, unable to settle.

In another set of experiments, he gave the infants a choice between a wire mother with a milk bottle and a cloth mother without. Once again, they preferred the cloth mother and clung to her when they were afraid. The implication was clear: baby monkeys would rather have a mother who could comfort them than a mother who could feed them.

Harlow’s studies seemed to rebuke the prevailing idea that infants bond to their mothers because mom is associated with satisfying basic needs like thirst or hunger. Rather, they supported a conclusion that John Bowlby had already begun to draw: infants have an innate need to attach. Attachment isn’t a by-product of fulfilling basic drives like hunger—it’s an end in itself. As Harlow put it, “man cannot live by milk alone” (p. 677).²⁶

Bowlby’s view of attachment was influenced greatly by an evolutionary perspective. The central idea was that natural selection has helped animals develop an attachment behavioral system for ensuring an infant’s safety and survival. We don’t know much about the details of life in our hunter-gatherer past, but it’s pretty clear that safety was an issue. There were predators, rival social groups, and the ever-present risk of malnutrition and dehydration. Staying close to and bonding with your parents would have had obvious survival value. The attachment behavioral system would motivate infants to stay close to their caregivers and establish a relationship that would allow them to safely explore the environment, knowing that someone had their back.

One of Bowlby’s most powerful insights might seem paradoxical: attachment is liberating. With a secure attachment in place, you are freed to go out into the world and learn what you need to learn. Without it, you need to either expend a lot of energy managing your relationship to your caregivers or go it alone and deal with your own distress. The instinctive nature of attachment means that children will try to form attachments regardless of how responsive or unresponsive their caregivers are. The poignant fact is infants will even become attached to abusive caregivers.

MOMMIE DEAREST

WHY? ANIMAL STUDIES SUGGEST THAT PART OF THE REASON babies will attach even to a hostile caregiver has to do with a biological switch in the infant brain.

If you’re a newborn mammal, say a rat pup, bonding with your mom requires connecting to her, staying close, suckling, and letting her do what she needs to do to protect you. But moms have their own challenges. They have to drag their infants around, make sure they eat, keep them warm, and sometimes hide them from predators. So, if you’re a helpless newborn, sometimes you’re going to be jostled, dragged, stepped on, pinched, or have any of a variety of other unpleasant experiences. And that creates a problem. Normally you want to steer clear of situations and individuals that cause pain. As we know, rats, humans, and other mammals have fear circuits that are dedicated to helping us avoid pain and discomfort. When something threatens or hurts us, these circuits can be life-saving by helping us learn to avoid the danger: once bitten, twice shy. But forming an attachment to your mother is also lifesaving when you’re a totally dependent infant. And you don’t want to avoid her even if she tramples or bites you from time to time. So how is a baby supposed to act?

Research by Dr. Regina Sullivan and her colleagues at New York University suggests that natural selection helped mammals handle this dilemma by creating a sensitive period in which the infant’s fear circuits are dialed down while circuits that drive approach behaviors are allowed to fire on all cylinders. Sullivan and her colleagues found that shortly after a rat pup is born, Mom’s presence has a soothing effect that lowers the infant’s levels of a key stress hormone, corticosterone. The low stress hormone levels keep the infants’ fear circuits in the off position,²⁷ and the rat pup will even endure electric shocks to get to its mother. This shift in how the brain learns creates a protected time for bonding and “allows the infant to attach to the caregiver at all costs.”²⁸

Separation from Mom, which normally happens as weaning begins, triggers a rise in stress hormone levels and the fear conditioning system switches on, allowing the infant to begin learning to avoid danger as it ventures out into the world.

There are two unsettling implications of Sullivan’s work. First, early-life stress can disrupt the biology that normally bonds mother and infant. As long as Mom is around, she provides a buffer that keeps the corticosterone level low and lets the attachment process proceed normally. But prolonged separation or a chronically stressed and unavailable mother can increase this stress hormone level, prematurely closing the window for forming stable attachments and disrupting the mother-infant bonding process.²⁹

The second implication is that the “attachment neural circuit” is basically blind to the quality of care. That means the infant will bond to a caregiver regardless of how nurturing she is. A wide variety of mammals—from rats to dogs to monkeys and humans—appear to have this kind of innate push to approach their caregivers with a blind trust, to give them the benefit of the doubt no matter how they are treated in return.

In humans, the strange phenomenon of attachment even in the face of danger has provided some of the oddest and most compelling stories of the past thirty years. In a comment on Sullivan’s findings, the biologist Robert Sapolsky drew a parallel to the ordeal of Jaycee Dugard, the girl whose story captivated the nation when she was freed from eighteen years of brutal captivity. She had been abducted at age eleven and kept by her deranged captor, Phillip Garrido, in a hidden backyard compound where she was raped and gave birth to two of his children. And yet, she seems to have had many opportunities to flee and chose not to. The “family” traveled in public and in later years she worked as the graphic artist in Garrido’s print shop, interacting with customers, making phone calls, and writing e-mails. When she was first interviewed by Garrido’s parole officers, she described him “as a ‘great person’ who was ‘good with her kids.’ ”³⁰ In her private diaries she expressed her anguished yearning for freedom, but also wrote, “I don’t want to hurt him, sometimes I think my very presence hurts him . . . I will never cause him pain if it’s in my power to prevent it.”³¹

The stories of Jaycee Dugard, Patricia Hearst, and other high-profile abductees who seemed to form a bond with their captors are sometimes labeled examples of Stockholm syndrome, a phenomenon that was described following a six-day hostage ordeal in a Swedish bank in 1973. When the hostages were released, they kissed and hugged their captors.³² Actions like these suggest that our need for attachment might, in some cases, be more powerful than reason.

Attachment in human infants may not have the distinct sensitive periods that Sullivan finds in her rats, but it does involve a kind of “perceptual narrowing” that we’ve seen with other sensitive periods. Recall that with vision, language, and emotion perception, young children’s minds go from a state of being broadly receptive to more narrowly committed. Attachment in infancy follows a similar path. For the first few months of life, newborns can be comforted by a variety of people. By seven or eight months, they begin to discriminate, focusing their attachment behaviors on their primary caregivers. They can tell the difference between “mommy” and a stranger, and they want mommy. And over the next several months, they show more and more distress on separation. After all, their sense of time and the future is fuzzy—it’s not clear that when mommy leaves, she’s ever coming back. There are two key signs that an infant is attached: he becomes fearful around strangers (stranger anxiety) and he shows distress when his caregiver leaves (separation protest and separation anxiety). And so, over the first year of its life, the baby narrows its attachment system to focus on its primary caregiver.

And then, in the two to three years that follow, attachment behaviors come into full focus and center on what John Bowlby identified as three key functions: (1) maintaining proximity and avoiding separation; (2) using the caregiver as a secure base from which to explore; and (3) using the caregiver as a safe haven to which the child can turn for comfort and support.

STRANGER IN A STRANGE ROOM

DEVELOPMENTAL PSYCHOLOGISTS WHO STUDY ATTACHMENT HAVE relied heavily on an experimental paradigm called the Strange Situation that was developed in the 1960s by Mary Ainsworth, a longtime colleague of Bowlby’s. It typically lasts about twenty minutes and takes place in a room with toys and two chairs. The mother and her twelve- to eighteen-month-old toddler go through a series of episodes that are designed to be mildly and progressively stressful for the child. The idea is that threatening situations—encountering strangers, being abandoned, being injured or ill—activate the child’s attachment system. The goal of the Strange Situation is to create an environment in which the nature of the child’s attachment is revealed. And it includes two scenarios that ought to powerfully trigger our evolved attachment systems: being left alone in an unfamiliar place and being left with a stranger.³³

The Strange Situation involves eight standardized periods, each lasting one to three minutes, in which the child is observed interacting with her mother (or other primary caregiver) and a stranger who is part of the research team. Twice during the procedure, the mother leaves the room. For the first separation, the mother leaves the child with the stranger and, for the second, the child is left alone. Later, the mother returns, and the researchers gauge how the child responds to reunions.

Based on this simple but evocative series of episodes, Ainsworth and her colleagues were able to classify the child’s behavior into one of three main attachment patterns.^34, 35 Most children (about 55 to 60 percent) fell into the “secure attachment” group. These children use their mothers as a secure base from which they can explore the environment. When the mother leaves the room, the child may become distressed, but when she returns the child is happy to see her or is easily comforted and quickly returns to playing and exploring.

The remaining groups are classified as “insecure attachments.” About 20 percent of children exhibit avoidant attachment—they readily explore the room and don’t show much interest in Mom. When left alone, they don’t cry or seem distressed, and when she returns, they don’t engage with her and even actively avoid her. If Mom picks the child up, the child may stiffen and pull away, seeming to want to keep his distance and go back to the toys. And finally, about 10 percent of children are classified as ambivalent. They are wary about exploring and often have a good deal of stranger anxiety. They’re extremely upset when Mom leaves, and are ambivalent at the reunion—seeking comfort from her but continuing to be distressed and angry with her.

In later years, it became clear that about 15 percent of infants had a profile that didn’t fit well into these groups, prompting the creation of a fourth “disorganized/disoriented” category.³⁶ These were children who seemed to lack any coherent strategy for responding to separation or reunion with their caregiver. They seemed overwhelmed and frightened, and their responses often seemed contradictory or idiosyncratic. They might scream for Mom to come back only to freeze or drop to their knees and rock back and forth when she appeared. Or cling to her while also pulling away.

Although the details of this attachment typology have been debated, it’s proven remarkably durable. These same basic attachment patterns appear in Europe, America, Africa, and Asia, even though the cultural traditions of how caregivers and children interact may be quite different.

But even if attachment behaviors in infancy are innate and universal, the quality of the attachment depends crucially on the nature of nurturing. Given the chance, all infants will form attachments, but the particular style of the attachment will be determined by how the caregiver and the infant interact. Caregivers who are sensitive and responsive to their baby’s needs are likely to foster secure attachments in their children. They offer consistency and predictability in their interactions with their children. And bolstered by that steady presence, the child learns to regulate his own emotional states, when to seek comfort and when he can handle things on his own.

As we saw with temperament in Chapter 2, though, attachments depend on the dynamic interplay between caregivers and their children—the goodness of fit. A child whose nervous system tends to be highly excitable or who is temperamentally needy or fearful will challenge the patience and nurturing capacities of her parents. And if the mother is stressed, lonely, or excitable herself, the result may be an insecure attachment.

John Bowlby argued that a central component of the attachment process is the development of what he called “internal working models.” Through their daily interactions with their caregivers, infants and children develop a mental representation of their primary relationship and their place in it. Is Mother^* trustworthy and responsive? Is she erratic, frightening, or unpredictable? What effect do I have on her? Am I lovable? In the reflection of this relationship, we begin to discern who we are and what we can expect of others. As we grow, this template may be updated and revised, but it provides the scaffold on which we build our other attachments throughout life. It shapes whom we seek for friends and lovers, and creates a lens through which we interpret their behavior. It is the root of our assumptions about the comfort or the pain that attachments entail.

Secure attachment is the norm, but all these organized attachment patterns are normal—that is, they are adaptive responses to different kinds of care. Rather than attachment gone wrong, insecure attachment behaviors might be strategic compromises. One solution to life with an unpredictable or erratic caregiver might be the alternating attachment behaviors that characterize the ambivalent pattern: be vigilant for signals of abandonment, be dramatic in demanding attention, resist intrusive behavior. Or, if you’re born to parents who are unavailable or rejecting, the self-reliant style of avoidant attachment might be your best bet: don’t make too many demands on a standoffish parent, keep your distance, find other outlets for stimulation. So natural selection may have equipped the infant mind with a menu of attachment strategies that would be sensitive to cues about the circumstances of our family environment.³³

Insecure attachment is not a disorder, but understanding the psychobiology of childhood attachment helps us understand how things can go awry. Almost all conditions that we recognize as psychiatric disorders involve relationships and attachments in some way. But are there disorders of attachment per se? That is, are there disorders in which we can say that the fundamental problem is one of attachment? It seems so.

When the process of attachment is catastrophically fractured, the result can be a devastating inability to bond and form relationships. In the most extreme case, some children are simply never given the opportunity to form an attachment. We enter life biologically prepared and primed to form an attachment to a caregiver. Our brains expect some kind of caregiver with whom we can identify and bond. But what if that caregiver never comes? Without the opportunity to attach, children can be profoundly disturbed.

The diagnosis of “reactive attachment disorder” (RAD) is reserved for children whose early caregiving environment was one of persistent neglect, abuse, or chaos and who have gross distortions in their ability to form social bonds. Much of what’s known about the disorder emerged from studies of children who spent their infancies in Romanian orphanages and other bleak institutional settings. RAD is relatively uncommon, affecting less than 1 percent of children; but up to 30 to 40 percent of institutionalized children or children who have landed in foster care because of abuse or neglect show signs of the disorder.³⁷

Children with RAD can be emotionally withdrawn. Often, they are unable or even afraid to seek comfort from other people when they are upset. Or they may be indiscriminately sociable with no primary attachment but “seemingly willing to seek and accept comfort from almost anyone, including strangers.”³⁷

While RAD exemplifies a tragedy of the human experience, it also underscores the remarkable resilience of the human mind. Despite the profound impairments that children with this condition suffer, their situation is not hopeless if they are given a chance. Most children with RAD who are adopted out of institutions into supportive homes no longer meet criteria for RAD after time has passed, although they may still bear scars.

But as we’ll see, the dramatic deprivation that causes RAD is not the only way disruptions in early attachment can cause long-lasting pain.

“WHY SHOULD I TRUST ANYONE?”

THE BEEP! BEEP! BEEP! WOKE ME UP WITH MY HEART POUNDING. I looked at the clock. 3:30 a.m. I groped for the pager on my bedside table and looked at the message. There was a phone number and the message “Sandra—emergency—please call.” It was the third time in the past three weeks that an emergency page had come from that number. The pounding was subsiding as I began to gather my thoughts and dialed, not sure what to expect.

“Hello, it’s Dr. Smoller answering a page.”

Sandra was crying on the other end of the line. “I don’t know what to do.” I’d been Sandra’s psychopharmacologist for several years.

“Can you tell me what’s going on?”

“I don’t have a therapist!” she said angrily.

A month earlier, Sandra had told me she’d fired her therapist of three years because she felt the therapist wasn’t listening to her and was cold and unfeeling.

“I know, and I know that’s been very difficult for you.” But I calmly reminded her that we had agreed that when these panicky feelings came on, she would write them down and we would talk about them at our next meeting.

“I don’t know if I’ll be there,” she said.

“What do you mean?”

“Oh nothing. Fine—have a nice vacation!” she said sarcastically and hung up. Our next appointment was two weeks away, after my return from a ten-day vacation.

Two weeks later, I found myself sitting in my office waiting for Sandra. The clock was winding down on our appointment and I began to worry. She had told me she might not make the appointment. But what did she mean by that? Several months earlier, I’d gotten a page from a colleague in the emergency room. Sandra had made a suicidal gesture by taking a week’s worth of her antidepressant and antipsychotic medication after a disagreement with her therapist. As she would have known, it was a nonlethal overdose. But that incident ran through my mind as I tried to figure out how to respond to her absence. Had she done something self-destructive? Or worse? With ten minutes left in the appointment, Sandra arrived, looking annoyed. “The bus was late,” she said with exasperation. I was relieved.

In the weeks that followed, we talked about the events around my vacation. She acknowledged that she had felt abandoned—by her therapist, by me, by everyone. Over time, the rift healed. But she remained on guard and fragile. “Why should I trust you? Why should I trust anyone?”

Sandra had survived a chaotic childhood. Her mother was unpredictably moody and suffered from depression on and off for most of Sandra’s early years. In Sandra’s childhood memories, her mother was often in bed, waking up to bark orders or asking Sandra to comfort her. She recalled her father, a successful businessman, as aloof and incessantly critical. He had a drinking problem, and when he drank he was loud and scary. In elementary school, she had problems sleeping and frequent nightmares. When the nightmares were bad, she would go to her parents’ room and ask to get into bed with them, but her mother always ordered her back to her room. In high school, she began to drink, sometimes ending up having casual sex after a bout of binge drinking. She had a series of painful relationships that often began with sex. She would fall desperately in love with boys who expressed interest in her, idealizing them and then feeling devastatingly abandoned and betrayed when it became clear that they were just interested in a good time. The agonizing sense of mistrust and loneliness that she had begun to feel as a child grew more and more entrenched. What had been a wound became a scar that kept reopening.

Sandra suffered from a condition that psychiatrists and psychologists call borderline personality disorder (BPD). The term borderline was first coined in the mid-twentieth century, when psychoanalysis dominated psychiatric practice and the main diagnostic question was “Who should be analyzed?” In the Freudian tradition, psychoanalysis developed as a treatment for neuroses. Patients with psychoses, like schizophrenia, were considered poor candidates for analysis. John Gunderson, a pioneer in the classification and treatment of BPD, noted that the borderline label was originally a term of art, loosely used to describe patients who were at the boundary of neurosis and psychosis and who were liable to regress into psychotic states during analysis.³⁸ But beginning in the 1960s and 1970s, psychiatrists began to see borderline personality as a syndrome in and of itself, and in 1980 it achieved the status of an official diagnosis, borderline personality disorder, in the DSM-III.

Unfortunately for many people, the iconic example of BPD is Fatal Attraction’s notorious Alex Forrest, played by Glenn Close, who seduces and then terrorizes Michael Douglas’s character. As a rule, people with BPD are not bunny-boiling stalkers, but then Hollywood tends to favor boffo box office over nuanced narratives. Still, the signs and symptoms of BPD can be dramatic. Those affected are prone to torrents of emotional pain that are often expressed as rage, panic, and self-destructive behavior. They may experience intolerable feelings of emptiness and have a hypersensitivity to perceived rejection, betrayal, and abandonment—feelings that can trigger emotional storms and frantic efforts to avoid being alone. Sometimes these episodes culminate in self-injury, including cutting themselves or attempting suicide. One in ten succeed.

A hallmark of the disorder is a pattern of unstable and intense personal relationships. People with BPD may alternate between idealizing (“you’re the only one who understands me”) and angrily devaluing caregivers (“you never cared about me!”). These shifts are typically triggered by separation or perceived abandonment. For friends and family, being on the other end of a relationship with someone with BPD can be a bewildering roller coaster, leaving them walking on eggshells to avoid provoking another crisis.

BPD has had a certain notoriety in clinical circles as well. It’s sometimes used as a synonym for “the difficult patient.” And that can be an obstacle to compassionate care. In 1978, an influential paper by James Groves, entitled “Taking Care of the Hateful Patient,” appeared in the New England Journal of Medicine and challenged physicians to recognize the ways in which patients with borderline and related personality traits trigger doctors’ own unconscious negative impulses (or, as psychoanalysts would say, negative countertransference). Because of their hostile dependency and emotional volatility, these were patients “whom most physicians dread to treat.”

That image has begun to change for at least two reasons. First, newer, more effective psychotherapies have been developed specifically for BPD, providing an antidote to therapeutic hopelessness for patients and clinicians. And second, long-term follow-up studies have shown that the prognosis for BPD is much better than anyone had thought, with improvement rates of up to 85 percent by ten years of follow-up.^38, 39

Still, there is controversy over the disorder. Some have argued that it’s simply a misnomer for unrecognized depression, bipolar disorder, or posttraumatic stress disorder. Others have gone even further to claim that the whole notion of personality disorders is a muddled concept without a clear scientific or medical basis.

Regardless, it’s clear that the diagnosis of borderline personality disorder captures some kind of enduring pattern of unstable emotions and relationships that can wreak havoc on affected individuals and those around them. And, as with most psychiatric disorders, genes play a role. Based on twin studies, variations in genes account for anywhere from 35 to 70 percent of BPD risk in the population.^40–42

In some ways, BPD is a perfect storm of many of the phenomena we’ve talked about so far. The vulnerable child may start life with a genetic endowment that creates a temperamental bias toward emotional reactivity. Then major adversity or a hostile or erratic home environment may program the stress hormone system in ways that make it even harder for the child to regulate her emotions. They may also bias her brain toward perceiving and feeling negative emotional states. These perceptions in turn affect the development of theory of mind and empathic skills resulting in a tendency to misread other people’s intentions and feelings and a hypersensitivity to signs of threat and loss. But there is increasing evidence that much of this plays out in the process of attachment.

Studies have consistently found a strong association between insecure attachment and BPD.⁴³ It’s been said that “BPD is typically not a disorder of the unloved but a disorder of those who were loved inconsistently.”⁴⁴ In one of the few prospective studies that have followed children from infancy to adulthood, Harvard psychologist Karlen Lyons-Ruth and her colleagues identified several steps along the trajectory from insecure attachment to adult borderline personality. Initially, researchers observed twelve-month-old children in the Strange Situation procedure. As Lyons-Ruth’s team coded the videotaped interactions, they found an interesting pattern. Children who went on to develop borderline traits tended to have mothers who displayed a pattern of withdrawal and emotional distance when they reunited with their infants after a separation. The children also tended to seek more contact than the average child. That combination—a child with a heightened need for contact and a mother who, out of fear or trouble handling her own distress, tends to withdraw when her infant expresses a need to be close—spelled trouble.

In one typical videotaped interaction, we see the mother come back into the room and stand still rather than approach her crying child. The child runs over to his mother who picks him up and begins to comfort him. She kisses his cheek and walks him over to some toys on the floor and stays by his side while he begins to play. So far, so good. But after a few moments, she moves away and sits on a seat several feet away. He seems confused and toddles over to her. She offers him a toy. The little boy’s distress begins to show, but instead of comforting him, she puts the toy in his little hand. He begins to cry and slowly moves away. And then something odd happens. He freezes. He seems bewildered and dazed, almost as though he’s retreated into his own world, as he stares at the toy. This goes on for nearly thirty seconds until he brings the toy to his mouth and begins to soothe himself. The interaction is subtle and perhaps unremarkable—but for a developmental psychologist, it’s revealing. Over countless small daily interactions, this combination of maternal withdrawal and disorganized attachment behavior seemed to nudge children in Lyons-Ruth’s study along a path toward borderline traits later in life. But whether they continue on that path depends in part on what happens next.

In the face of an inconsistent or withholding caregiver, some children develop strategies to control the relationship. They may become caretaking themselves, trying to smooth things over and make sure mother isn’t upset or angry. Or they may become more dramatic in their demands for caretaking, responding to distance or separation with emotional tantrums as if to say “I will not be ignored!” And, when the subjects in the Lyons-Ruth study reached middle childhood, this kind of controlling behavior on the part of the child proved to be another step along the trajectory toward borderline traits and a tendency to engage in self-injury later in life.

Through a collision of genetic vulnerability and inconsistent caregiving, a child at risk for BPD may form an “internal working model” of attachment figures as untrustworthy and liable to disappoint or harm them. Instead of developing an ability to regulate her own emotions and needs, she becomes preoccupied with controlling the emotional states of others.

The need to monitor and control the mental states of others may reinforce the hypersensitivity to emotional signals that’s characteristic of BPD.⁴⁵ Brain-imaging studies find that individuals with BPD have a hypersensitive response of the amygdala and other limbic regions when they’re shown emotional faces.^46, 47 This exquisite sensitivity may have enduring effects on the development of their theory of mind and empathic capacities. On the one hand, some studies have shown an enhanced ability to read the mental states of other people. One study used a test developed by Simon Baron-Cohen called the Reading the Mind in the Eyes Test.⁴⁸ It works like this: subjects are shown a series of pictures of faces that include only the eyes and the regions right around them. They are then asked to choose which of four words correctly describes what the person in the photograph is thinking or feeling: “panicked,” “cautious,” “friendly,” “regretful,” and so on. Compared to healthy controls, subjects with BPD were significantly more accurate at reading mental states from the photographs.⁴⁹

On the other hand, studies have shown that those with BPD have a subtle bias toward reading negative affect in others—especially anger and fear. It as though the gain is turned up on their affect detectors—they see anger and other negative emotions faster than other people, but they are also prone to see them when they’re not there.⁴⁶ As we saw in Chapter 3, victims of child abuse and neglect show this same hypersensitivity to reading negative emotions; remarkably, childhood histories of abuse and neglect are reported by up to 90 percent of individuals with BPD.^47, 50

TRUST ME

ALL OF US ARE BORN WITH BRAINS THAT EXPECT TO ENCOUNTER a caregiver and are prepared to form an attachment to that person (usually Mom). Barring a catastrophe—severe deprivation, for example—we will attach over the course of the next two or three years. But normal variations in attachment behavior and temperament, coupled with particular styles of caregiving can set a trajectory toward healthy relationships on the one hand or unstable ones on the other.

The key ingredient underlying all of this is the establishment of a sense of trust. Trust is the glue that bonds relationships—from personal friendships to geopolitical alliances. Check out your favorite source of news, and you’ll realize that it’s at the core of most stories that capture our attention: sex scandals (from Tiger Woods to John Edwards), finance (from Bernie Madoff to the Wall Street backlash), and global conflict (from the brinksmanship with Iran to the Arab-Israeli conflict). Of course, trust is also fundamental to forming attachments. Our basic sense of trust in others emerges early in life, as infants experience their caregivers and come to see the world as basically stable and safe or precarious and threatening.

The influential psychoanalyst Erik Erickson (1968) put the development of a basic sense of trust versus mistrust at the very foundation of personal development, calling trust “the cornerstone of a vital personality.” As Erikson put it, “Mothers create a sense of trust in their children by that kind of administration which in its quality combines sensitive care of the baby’s individual needs and a firm sense of personal trustworthiness within the trusted framework of their community’s lifestyle. This forms the very basis in the child for a component of the sense of identity which will later combine a sense of being ‘all right,’ of being oneself, and of becoming what other people trust one will become” (pp. 103–104).⁵¹

BRAIN TRUST

LATER IN LIFE, THE MENTAL MACHINERY OF TRUST BECOMES MORE complex—we use theory-of-mind skills and emotion-detection skills to gauge another person’s intentions and to see if they are deceiving or cheating us. But only recently has trust itself become the subject of scientific study. And research on the biology of trust is once more implicating our old friend oxytocin.

In a groundbreaking experiment, a team of scientists at the University of Zurich had volunteers play a simple two-person game.⁵² Both players start out with twelve units of money. One player, the investor, makes the first move by giving none, some, or all of his money to the other player (the trustee). The trustee can give the investor anything from zero to all of his money back. The catch is that, going into the game, the researchers tell the players that they will triple any money the investor gives the trustee. The more money the investor gives, the more money there is for the two players to split. If the trustee can be trusted to give some money back, it’s a win-win situation.

Before the game began, players were given a single dose of a nasal spray that contained either oxytocin or placebo. Investors who inhaled the oxytocin became much more trusting—that is, more likely to give others money in the belief that their generosity would be reciprocated. Interestingly, oxytocin only worked when subjects were interacting with other people. When the oxytocin-snorting investors played against a computer algorithm, there was no increase in their trust behavior. It also wasn’t a matter of their just being nicer (what psychologists call prosocial), because trustees who were given oxytocin didn’t increase the amount they gave back to an investor.

The study spawned a wave of research that suggested oxytocin is central to the biology of trust and attachment. Later studies found that inhaling oxytocin can increase positive communication between couples,¹⁹ enhance generosity,^53, 54 and make hostile faces seem more familiar.⁵⁵ Now you see how the business model for Liquid Trust was born.

THE FEEL-GOOD HORMONE OF THE YEAR?

BUT HOW EXACTLY COULD OXYTOCIN—JUST A LITTLE STRING OF nine amino acids—tweak our brains to see others as more trustworthy and make us more cooperative and even loving? The answer seems to involve three related brain systems that are familiar by now: maternal care, social cognition, and harm avoidance.

First, as the work with rats and voles suggested, natural selection made use of the maternal functions of oxytocin and expanded them to create a mechanism for bonding to others. Start with a peptide hormone—oxytocin—that kicks in when a newborn arrives—just when nurturing needs to start. Now hitch that peptide up to the brain’s emotion and reward circuits and you can coordinate childbirth with childcare. The motivation and reinforcement for caring for an infant was in place. In humans, with our complex cognitive and emotional capacities, that bonding became something more profound—love. And so it may have been a relatively small evolutionary step to translate a system for maternal love into other bonds and attachments, including romantic love.

But that’s not the whole story of how oxytocin connects us to other people. It also seems to help us tune into the thoughts and feelings of other people by enhancing mind reading and empathy. After inhaling oxytocin nasal spray, people are more likely to fixate on the eye region of faces⁵⁶ and do better on tests of reading emotional cues.⁵⁷ People who carry a particular variant of the oxytocin receptor gene have a similar advantage in reading emotional expressions.⁵⁸ And perhaps the most striking evidence that oxytocin augments mind reading are studies showing that oxytocin can help people with autism spectrum disorders become better at recognizing emotional cues from other people’s faces and voices.^59, 60

The third element of oxytocin’s effect may be the most fundamental to trust, and it has to do with fear. It turns out that the amygdala is loaded with oxytocin and vasopressin receptors and that they have opposite effects on fear behavior.⁶¹ Oxytocin turns down the amygdala’s fear response and vasopressin turns it up. Together, they appear to create a balance that helps determine where an animal sits on the approach/avoidance continuum. Dialing up oxytocin nudges the brain toward approach by dialing down fears and inhibitions. But oxytocin seems to have its greatest effect on reducing fears of other people. Several studies have now shown that oxytocin dampens the amygdala’s reactions to people’s faces^62–64 and biases us to see positive aspects of other people.^65, 66 In some ways, the effect of oxytocin on how we see others is the opposite of the effects of trauma and early adversity. Earlier we saw that children who have suffered abuse and neglect are biased to see negative emotions.⁶⁷ If early trauma puts dark shades over our mind’s eyes, oxytocin seems to give us rose-colored glasses.

The ability to reduce fear is crucial, because if oxytocin merely enhanced our mind reading, that might not do much for trust—it might even make us less trusting. After all, if you are more sensitive to what people are up to, you might be more vigilant about getting scammed. But once you add in the attachment-promoting and fear-reducing effects, now you’ve got something that just might add up to trust. In other words, one interpretation of oxytocin’s trust-enhancing power is that it helps us tune in to other people while bathing them in the warm glow of goodness. It’s like what some people describe when they take Ecstasy (“I love you, man”)—and yes, Ecstasy stimulates oxytocin.^68, 69

So oxytocin reduces our fears about other people and pushes us to give them the benefit of the doubt. It’s a kind of anticynicism effect—we expect the best of other people. And at the same time, it makes us less sensitive to betrayals of trust. In an elegant study, the University of Zurich team took the trust game one step further. Their original study of oxytocin’s effect on investors in the trust game was missing a key element of how we decide to trust in real life: we develop trust over a number of interactions by seeing what people do and learning how trustworthy they are. In the new study, the researchers went one more round. After inhaling oxytocin or placebo, subjects played the role of the investor in the trust game with a human partner. After the initial round, the investors were given feedback about how their investments fared: they were told that the investee gave back money only about 50 percent of the time.

Now what would you do if you were the investor in the trust game and you were given another opportunity to play the game? You trusted some guy with your money, hoping he’d reciprocate and make you both richer. But half the time, the selfish jerk kept the money for himself. You’d probably be much less willing to trust him again. And that’s exactly what happened in the experiment for those given placebo—on the second round, they offered their trustees much less money. But those who were given oxytocin had no drop-off in their trust behavior after being betrayed—that is, oxytocin seemed to make people insensitive to betrayal.

While the subjects played the game, their brains were being scanned by an fMRI. After learning that their trust had been betrayed, subjects who got placebo had a much stronger response in the amygdala and related fear circuits compared to those who got oxytocin. Previous studies had shown that the amygdala is, among other things, a trust sensor: it lights up when people are shown faces that look untrustworthy⁷⁰ and patients with amygdala damage tend to view others as more trustworthy and approachable.⁷¹ The placebo group also had activation of the caudate nucleus, a region shown to be involved in adapting to another person’s behavior in trust games.⁷² But the oxytocin group didn’t have these activations of the amygdala and caudate. By damping down the brain’s social fear and social judgment circuits, people with oxytocin on board continued to see their beneficiaries as trustworthy even after they’d been double-crossed.

SURVIVAL OF THE SKITTISH

LIKE ATTACHMENT, MIND READING, AND HARM AVOIDANCE, TRUST has obvious implications for survival. Could our minds have evolved specialized mechanisms for determining how much we trust others? After all, trust is essential to the success of our relationships and to the scores of social encounters we participate in every day. Every time you buy something from a salesperson, confide in a colleague, or make an investment, you are choosing to trust someone—someone who might take advantage of you. The consequences of being cheated could be devastating, depending on when and in whom you placed your trust.

That situation was no different for our hominin ancestors. In evolutionary terms, a person’s survival (and opportunity to pass on their genes) could easily depend on being right about whom he trusted. For example, females, who need to commit to investing lots of resources in bearing and caring for offspring, would have been strongly motivated to select mates who could be trusted to stick around and contribute. Males, who can never be certain about the paternity of their offspring, needed to know when a female was unfaithful. And any time you take a risk by cooperating in a dangerous situation or sharing your resources, your very survival may depend on the trustworthiness of your collaborators. Given how high the stakes are, it might be worth dedicating some of the brain’s operating system to the task of detecting trustworthiness and monitoring the outcomes of social exchanges.

And that seems to be the case. Our brains are exquisitely adept at detecting violations of trust. We make judgments about trustworthiness at warp speed and with very little information. For example, we can detect when someone is being authentic or insincere just based on how they smile.⁷³

In an elegant series of experiments, the evolutionary psychologists Leda Cosmides and John Tooby showed that people are remarkably good at “cheater detection.” Most of us are not very facile with formal logic or reasoning. In fact, when presented with a standard logical problem in which people are asked to decide what information is needed to determine whether a logical rule has been violated, the vast majority of people get it wrong. But when the problem involves determining whether someone has violated a rule by cheating in a social exchange, we suddenly become expert logicians—60 to 85 percent of people get it right. Our cheater detection skills, like our theory of mind skills, have the hallmarks of an evolved mental mechanism, and Cosmides and Tooby have argued that these skills are part of our “universal human nature.”⁷⁴ By age three or four, children from industrialized Europe to rural Nepal understand when someone has violated a social contract,⁷⁵ and hunter-gatherers from a remote region of the Ecuadorean Amazon perform just as well on cheater detection tasks as Harvard undergraduates.⁷⁶

There is also at least some evidence that the human mind’s ability to detect cheaters is rooted in particular brain areas. In one study, psychologist Valerie Stone, along with Cosmides and Tooby gave reasoning tests to R.M., a patient who had been in a bicycle accident that extensively damaged his limbic system, including the orbitofrontal cortex and both his right and left amygdalae.⁷⁷ They found that compared to healthy controls and other patients with brain damage, R.M. reasoned just fine about most kinds of rule violations, but when it came to detecting social contract violations, he was lost.

The evidence so far suggests that trusting and avoiding betrayal involve two mental components. One is more about emotional judgments and relies on subcortical brain regions like the amygdala and striatum, where oxytocin and vasopressin help calibrate our willingness to trust, our expectations about other people’s behavior, and our wariness of being betrayed.^{64, 72, 78} The other is more about reasoning and seems to involve higher cortical circuits,^{77, 78} providing an innate set of mental algorithms that determine when someone has broken a social contract.

DYS-TRUST

“WHY SHOULD I TRUST ANYONE?” SANDRA’S QUESTION BECAME A focus of our discussions over the next several months. I encouraged her to reengage in therapy and had given her several referrals, but she never followed through. What was standing in the way? I asked. “I’ve had it,” she said. She had come to see her relationships, including those with her therapists, as a series of disappointments and betrayals. In her early twenties, she had hooked up with a man named Mark, whom she’d met at a club. She was wary of getting involved, and the more time they spent together, the more fearful she became. She was almost paralyzed by a sense that she was going to do something that he’d use as an excuse to leave her.

But it didn’t happen and “after a while, I let my guard down and I let myself fall in love.” Everything was fine at first. He seemed genuinely interested and would listen and comfort her when she was upset. One day they came up with a business idea—he was a talented chef and she knew some people in the food industry, and they decided to launch a business catering for parties. Unfortunately, that was a catalyst for conflict. They argued and fought about almost everything, with Sandra often erupting into angry outbursts, accusing him of devaluing her ideas and treating her like a child. Finally, Mark told her he couldn’t take it anymore and ended the relationship. She was devastated and her anguish took the form of relentlessly hounding him and demanding he explain why he had lied to her and used her.

In Sandra’s mind, Mark had made promises he never intended to keep. When he cut off all communication with her, she upped the ante. She sent him an angry e-mail that included a threat to sue him. And then she took a knife and cut up her forearms. She called Mark to tell him what he’d made her do, but he didn’t answer the phone. And so she paged her therapist, who convinced her to go to the emergency room.

The next crisis happened a few years later. Her therapist at the time had apparently tried to make Sandra feel secure by encouraging her to call anytime if she needed to. She had even given Sandra her home phone number. As Sandra told it, the therapist became more of a friend than a therapist. Sandra did feel a sense of calm knowing that her therapist was always available. But one night, Sandra was feeling lonely and was ruminating about whether “alone” would be her fate forever. She began to feel panicky. She picked up the phone and called her therapist. But there was no answer. She left a distraught message, asking her therapist to call immediately. As one hour and then another passed, Sandra became overwhelmed. She began drinking and then began cutting. Finally, she called an ambulance and by the next morning, she was in the hospital. “Now do you see why I don’t exactly feel like I should trust you?”

I’ve argued that BPD is a disorder of attachment. But from another angle, it’s a disorder of trust. Individuals with BPD are exquisitely sensitive to signs of betrayal, insincerity, and abandonment—and, as we’ve seen, neuroimaging studies suggest that, like victims of child abuse more generally, there is a perceptual bias toward seeing other people as hostile and threatening. The residue of their insecure attachments and the experience of inconsistent love would only fuel the presumption that relationships are fraught with danger. They yearn to connect but have learned to beware.

And since trust is the foundation of cooperation, maintaining stable relationships is a challenge. What would you see if you asked individuals with BPD to play the trust game? Read Montague and his colleagues at Baylor College of Medicine asked this question by having healthy volunteers play a multiround trust game with trustees who were either other healthy volunteers or individuals with BPD. Using fMRI, they were able to capture brain images of the players in action. The healthy pairs got into a rhythm of cooperation and trust: investors transferred money and trustees reciprocated. If an investor made a low offer, signaling a possible loss of faith in his partner, the trustees often increased the amount they returned as if to coax the investors to trust them again. These gestures of goodwill usually worked, restoring the cooperative relationship and the flow of money. But when the trustee was someone with BPD, the social exchange often broke down. The BPD partners didn’t try to repair the relationships with gestures of goodwill, and soon the exchange collapsed.

What happened? When asked, the BPD subjects reported much lower trust than the healthy volunteers. When healthy trustees were faced with a low offer, brain scans revealed heightened activity in the insula, a region of the limbic cortex previously implicated in violations of social norms and the sense of being exploited. But the BPD trustees didn’t have the same insula response. It was as though they weren’t surprised by a low offer. They expected to be screwed. Of course, one study doesn’t prove the case, but it does fit with the idea that BPD involves a neural bias to mistrust and to expect the worst from relationships.

ONLY CONNECT

WE’VE SEEN THAT THERE ARE EVOLUTIONARY AND BIOLOGICAL INFLUENCES on human relationships: from maternal love and attachment to romantic love and trust. And as varied and complex as these phenomena are, there are unifying threads running through them. At one level, they all reflect one of the most profoundly enriching features of the human mind: our ability to connect. We not only cooperate, we care for each other. Our connections to other people begin from the moment of birth and set the trajectory of whom we become and how we live. Love, commitment, cooperation, estrangement, and grief: these are the chapter headings for the story of our lives. They clearly cannot be reduced to biology. But it’s also clear that biology is at work.

In a circuitous way, our capacity to love is the reward we get for having a brain that does much of its developing after we’re born. The mature human brain is big. Literally too big to bear. To deliver a head that contained a full-grown human brain, the female pelvis would have to be radically restructured. You might say there was a “goodness of fit” problem. So human infants have relatively small heads that grow over a period of years to accommodate the developing brain. We are an altricial species—born helpless and vulnerable. We need nurturing and protection. Our ancestors undoubtedly faced strong selection pressures to find a way to keep infants alive until they could fend for themselves. The solution was twofold: (1) use hormone systems and reward circuits to motivate maternal nurturing and cement pair-bonds between parents so they protect and support their infants; and (2) endow the infant with an innate drive to attach and make use of that caregiving. And, happily, those same systems provide a biological foundation for connecting with one another throughout our lives.

So here’s the remarkable thing: our relationships are always, directly or indirectly, under the spell of these two biological imperatives—parent-child bonding and child-parent attachment. The connections we later forge are not only psychologically but even biologically rooted in that first bond. The very circuitry and chemistry of parenting, attachment, trust, and romance are linked.

We are all endowed with the biological drive and equipment to connect. Even in the face of life’s challenges, we usually manage to attach and find love. But the manifold variety of how it all plays out depends on the particulars of who and what we find along the way: the goodness of fit in our earliest attachment and the catalogue of triumphs and traumas that we encounter in childhood and beyond. As these accumulate, they rework our models and bias our perceptions and interpretations of other people. Variations in our genes may influence how we respond to these experiences. But for some of us, adversity takes a toll that is hard to overcome, distorting the trajectory of our capacity to love and to trust. Sometimes the result is a disorder of attachment: reactive attachment disorder in children or borderline personality disorder in adults.

Oxytocin seems to be one key player throughout the life cycle, promoting rewarding relationships, enhancing trust, and buffering our social fears. Maybe the idea of bottling oxytocin as liquid trust isn’t so far-fetched after all. Except, of course, there’s a problem. It’s hard to see how spritzing oxytocin on yourself each morning would have the intended effect of “making the people around you have a strong feeling of trust,” as the website claims. Wouldn’t it be the reverse? You spray on oxytocin on your shirt and go on a date—presumably you’re the one who’s more likely to be the easy mark. You’d have to wonder, as Aretha Franklin once poetically put it, “Who’s zoomin’ who”?

There’s another wrinkle in the story that makes the prospects of giving people oxytocin more complicated than we might hope: its effects may depend on your attachment history. For example, in one study, people with borderline personality disorder who were given oxytocin before playing a version of the trust game actually became less trusting and cooperative.⁷⁹ It may be that, by making people more attuned to social cues, oxytocin can heighten concerns about trust and intimacy in those who’ve had a history of insecure and painful attachments.

And yet, oxytocin’s use as a therapeutic aid may not be far off. Larry Young, the neuroscientist whose work has helped establish oxytocin and vasopressin as social peptides, thinks so: “I think that we probably will see a time when some target, some drug, is used to stimulate the oxytocin system . . . to increase social perception or social cognition.”

The brightest hope right now has been oxytocin’s potential to enhance social cognition in people with autism spectrum disorders. In small short-term studies, oxytocin has been shown to enhance their ability to read mental states, make eye contact, experience trust, understand social cues, and engage in social interactions.^{59, 60, 80} There are few options available to ameliorate autism, so this seems like a welcome advance, even though much work remains to be done.

And what about more mundane problems? Studies suggesting that oxytocin can reduce marital conflict are also intriguing. As Young commented, “People go to a marital therapist to try to solve the problems that they have in a relationship. If oxytocin is helping you tune in to other people, making you more empathetic, better able to perceive the emotions of the other person, it seems like it might be useful” for couples therapy. And, as we will see in Chapter 7, there is a precedent for using drugs to tweak the brain in ways that make therapy more effective.

How far can we go with this? The limitations of Liquid Trust notwithstanding, what would it mean if there were a drug that could be used to make us more loving and trusting? Who knows—it might be the solution to bipartisan gridlock. And yet the question can’t help but evoke Orwellian fantasies. An opiate for the masses? A weapon of war?

If only we could trust each other not to go there.

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* http://www.verolabs.com/default.asp (accessed January 2, 2010)

* Of course, in the wild, it’s not quite so simple. Some prairie voles have been found to sneak sex with females on the side.¹⁶ And some studies have found that in their natural habitat, the AVPR1A promoter sequence doesn’t always predict monogamy.¹⁷

* I am using “Mother” as a shorthand for caregiver. While early attachment theorists focused predominantly on the mother-child relationships, subsequent research has shown that fathers and other caregivers can also be the object of our primary attachments.