Attunement occurs tacitly, as part of the rhythm of relationship. Stern has studied it with microscopic precision through videotaping hours of mothers with their infants. He finds that through attunement mothers let their infants know they have a sense of what the infant is feeling. A baby squeals with delight, for example, and the mother affirms that delight by giving the baby a gentle shake, cooing, or matching the pitch of her voice to the baby's squeal. Or a baby shakes his rattle, and she gives him a quick shimmy in response. In such an interaction the affirming message is in the mother more or less matching the baby's level of excitement. Such small attunements give an infant the reassuring feeling of being emotionally connected, a message that Stern finds mothers send about once a minute when they interact with their babies.
Attunement is very different from simple imitation. "If you just imitate a baby," Stern told me, "that only shows you know what he did, not how he felt. To let him know you sense how he feels, you have to play back his inner feelings in another way. Then the baby knows he is understood."
Making love is perhaps the closest approximation in adult life to this intimate attunement between infant and mother. Lovemaking, Stern writes, "involves the experience of sensing the other's subjective state: shared desire, aligned intentions, and mutual states of simultaneously shifting arousal," with lovers responding to each other in a synchrony that gives the tacit sense of deep rapport.8 Lovemaking is, at its best, an act of mutual empathy; at its worst it lacks any such emotional mutuality.
THE COSTS OF MISATTUNEMENT
Stern holds that from repeated attunements an infant begins to develop a sense that other people can and will share in her feelings. This sense seems to emerge at around eight months, when infants begin to realize they are separate from others, and continues to be shaped by intimate relationships throughout life. When parents are misattuned to a child it is deeply upsetting. In one experiment, Stern had mothers deliberately over-or underrespond to their infants, rather than matching them in an attuned way; the infants responded with immediate dismay and distress.
Prolonged absence of attunement between parent and child takes a tremendous emotional toll on the child. When a parent consistently fails to show any empathy with a particular range of emotion in the child—joys, tears, needing to cuddle—the child begins to avoid expressing, and perhaps even feeling, those same emotions. In this way, presumably, entire ranges of emotion can begin to be obliterated from the repertoire for intimate relations, especially if through childhood those feelings continue to be covertly or overtly discouraged.
By the same token, children can come to favor an unfortunate range of emotion, depending on which moods are reciprocated. Even infants "catch" moods: Three-month-old babies of depressed mothers, for example, mirrored their mothers' moods while playing with them, displaying more feelings of anger and sadness, and much less spontaneous curiosity and interest, compared to infants whose mothers were not depressed.9
One mother in Stern's study consistently underreacted to her baby's level of activity; eventually her baby learned to be passive. "An infant treated that way learns, when I get excited I can't get my mother to be equally excited, so I may as well not try at all," Stern contends. But there is hope in "reparative" relationships: "Relationships throughout life—with friends or relatives, for example, or in psychotherapy—continually reshape your working model of relationships. An imbalance at one point can be corrected later; it's an ongoing, lifelong process."
Indeed, several theories of psychoanalysis see the therapeutic relationship as providing just such an emotional corrective, a reparative experience of attunement. Mirroring is the term used by some psychoanalytic thinkers for the therapist's reflecting back to the client an understanding of his inner state, just as an attuned mother does with her infant. The emotional synchrony is unstated and outside conscious awareness, though a patient may bask in the sense of being deeply acknowledged and understood.
The lifetime emotional costs of lack of attunement in childhood can be great—and not just for the child. A study of criminals who committed the cruelest and most violent crimes found that the one characteristic of their early lives that set them apart from other criminals was that they had been shuttled from foster home to foster home, or raised in orphanages—life histories that suggest emotional neglect and little opportunity for attunement.10
While emotional neglect seems to dull empathy, there is a paradoxical result from intense, sustained emotional abuse, including cruel, sadistic threats, humiliations, and plain meanness. Children who endure such abuse can become hyperalert to the emotions of those around them, in what amounts to a post-traumatic vigilance to cues that have signaled threat. Such an obsessive preoccupation with the feelings of others is typical of psychologically abused children who in adulthood suffer the mercurial, intense emotional ups and downs that are sometimes diagnosed as "borderline personality disorder." Many such people are gifted at sensing what others around them are feeling, and it is quite common for them to report having suffered emotional abuse in childhood.11
THE NEUROLOGY OF EMPATHY
As is so often the case in neurology, reports of quirky and bizarre cases were among the early clues to the brain basis of empathy. A 1975 report, for instance, reviewed several cases in which patients with certain lesions in the right area of the frontal lobes had a curious deficit: they were unable to understand the emotional message in people's tone of voice, though they were perfectly able to understand their words. A sarcastic "Thanks," a grateful "Thanks," and an angry "Thanks" all had the same neutral meaning for them. By contrast, a 1979 report spoke of patients with injuries in other parts of the right hemisphere who had a very different gap in their emotional perception. These patients were unable to express their own emotions through their tone of voice or by gesture. They knew what they felt, but they simply could not convey it. All these cortical brain regions, the various authors noted, had strong connections to the limbic system.
These studies were reviewed as background to a seminal paper by Leslie Brothers, a psychiatrist at the California Institute of Technology, on the biology of empathy.12 Reviewing both neurological findings and comparative studies with animals, Brothers points to the amygdala and its connections to the association area of the visual cortex as part of the key brain circuitry underlying empathy.
Much of the relevant neurological research is from work with animals, especially nonhuman primates. That such primates display empathy—or "emotional communication," as Brothers prefers to say—is clear not just from anecdotal accounts, but also from studies such as the following: Rhesus monkeys were trained first to fear a certain tone by hearing it while they received an electric shock. Then they learned to avoid the electric shock by pushing a lever whenever they heard the tone. Next, pairs of these monkeys were put in separate cages, their only communication being through closed-circuit TV, which allowed them to see pictures of the face of the other monkey. The first monkey, but not the second, then heard the dreaded tone sound, which brought a look of fear to its face. At that moment, the second monkey, seeing fear on the face of the first, pushed the lever that prevented the shock—an act of empathy, if not of altruism.
Having established that nonhuman primates do indeed read emotions from the faces of their peers, researchers gently inserted long, fine-tipped electrodes into the brains of monkeys. These electrodes allowed the recording of activity in a single neuron. Electrodes tapping neurons in the visual cortex and in the amygdala showed that when one monkey saw the face of another, that information led to a neuron firing first in the visual cortex, then in the amygdala. This pathway, of course, is a standard route for information that is emotionally arousing. But what is surprising about results from such studies is that they have also identified neurons in the visual cortex that seem to fire only in response to specific facial expressions or gestures, such as a threatening opening of the mouth, a fearful grimace, or a docile crouch. These neurons are distinct from others in the same region that recognize familiar faces. This would seem to mean that the brain is designed from the beginning to respond to specific emotional expressions—that is, empathy is a given of biology.