Mothers and Others

by Sarah Blaffer Hrdy

  ONCE WE LEARNED THAT OTHER APES BOTH GAZE AND IMITATE . . .

  Years ago, Darwin noted that it is not incorrect ideas that impede scientific progress but “false facts.” In the case of the wrong hypotheses, other researchers “take a salutary pleasure in proving their falseness,” and they are soon corrected. But when wrong facts get enshrined in the literature, they “often long endure.”60 The problem for those of us thinking about comparative infant development in apes was that for many years we wrongly assumed that face-to-face gazing and imitation did not occur in other apes. This turns out to have been an error, albeit one that in retrospect is understandable.

  Systematically monitoring the visual gaze of a nonhuman ape is no easy task. Not only are ape mothers extraordinarily protective, but throughout the first months of life baby chimpanzees mostly sleep or suck on their mother’s nipples, and they rarely fuss or fidget. Baby apes are actively alert to the world around them for only about 10 percent of each day.61 In spite of such difficulties, in 1991 the psychologist Hanus Papousek undertook the first-ever comparative study of mother-infant eye gazing in humans, captive gorillas, and bonobos. Based on what he was able to see, Papousek reported that “eye-to-eye gaze for prosocial purposes was unique to humans.”62 Since this discovery was pretty much what psychologists had expected, Papousek’s initial finding went unchallenged for another decade. As late as 2002 (and in some circles to this day) it was taken for granted that the long, loving, reciprocated “extended mutual gaze” was “a human-specific adaptation . . . essential for developing a rich understanding of others’ mental states, often called ‘a theory of mind.’”63 But, once again, closer scrutiny of other apes under more empathetic conditions compelled scientists to rethink the differences between other apes and us.

  The psychologist Kim Bard, currently director of the Centre of the Study of Emotion at the University of Portsmouth in England, was among the first to challenge the conventional wisdom. She began to systematically study mutual gazing in chimpanzees at a time when most of the rest of us still assumed such behavior did not occur. She learned that chimpanzee mothers spend about 12 minutes of every hour looking at their newborns. Half of the time the mother seemed to peer directly into her baby’s face. Some mother chimpanzees looked at their babies even longer. Occasionally mothers would use one hand to turn their infant’s head toward their own face while continuing to gaze. Approximately ten times an hour the infant peered back.64

  In addition to their mother’s face, some babies looked into the eyes of their human keepers. The chimpanzee babies most prone to extended eye-to-eye contact with humans were the ones who had been separated from their mothers and were especially eager to reestablish any kind of contact. Since the chimpanzee babies who had been seeking eye contact in her studies also tended to be reared by mothers who themselves had spent a lot of time in close association with humans, Bard proposed that eye gaze in chimpanzees was “culturally” regulated and depended on circumstances.65 That is, chimpanzees were adopting some of the interpersonal styles of the people they spent time with. The more exposure to human caretakers young apes had, the closer their sociocognitive responses came to those of human children in realms like intention-reading, give-and-take games involving objects, or engagement with others about their responses to objects.66

  Bard’s suspicions about the importance of rearing context were strengthened by what her colleagues in Japan were learning.67 To this day the prize for the most intimate and expressive gazing goes to a baby chimpanzee named Ayumu. He was born in 2000 to a female chimpanzee named Ai, who had been born in Africa in 1977 and brought to Japan. From 1978 onward, Ai worked closely with the psychologist Tetsuro Matsuzawa at the Primate Research Institute at the University of Kyoto. Abandoning conventional laboratory protocols, Matsuzawa (who referred to his star chimpanzee pupil as his “partner” rather than his research subject) treated the chimpanzees he studied as friends. In the process, he pioneered a more intuitive approach for probing the perceptual and cognitive abilities of our closest primate relatives.

  In addition to the usual greetings and reassurances that any good psychologist would provide his animal subjects, Matsuzawa’s collaboration with Ai was punctuated by hugging, cuddling, mutual grooming, and scratching as well as long bouts of just hanging out together. The gentle and debonair lab director spent hours with a brush, patiently combing the hairs down Ai’s back. Over a 30-year-long relationship, Ai has learned to trust Matsuzawa as a close associate who behaves more calmly, benevolently, and predictably than any of the more impulsive members of her own species.

  So completely did Matsuzawa gain Ai’s trust that in 2000 when she gave birth for the first time, she rewarded her human friend with unprecedented access to her newborn, access denied even her closest chimpanzee relations. Over the years, Matsuzawa’s methods were used with other chimpanzees as well, leading the Kyoto team to dogma-shattering insights into the sensibilities and capabilities of Pan troglodytes. Chimpanzees raised by both their mothers and human others not only proved to be far more engaging as newborns than anyone had previously realized but mastered an impressive array of cognitive tasks. With special training, four-year-old Ayumu and his peers were actually better than university students at memorizing number sequences and then rapidly punching them onto a computer screen.68

  Prior to Matsuzawa, scientists seeking to observe or film a baby chimpanzee face-to-face had to first remove the baby from its mother and rear it under highly artificial conditions. Never before had anyone other than the mother been allowed such privileged access to a newborn chimpanzee actually being reared by its own mother. Days after Ayumu’s birth, Matsuzawa became the first person to observe and film the ephemeral “fairy” smiles that flit across the pale pink face of a newborn chimpanzee during Rapid Eye Movement sleep. Prior to that moment, neonatal smiles (which thanks to Matsuzawa we now know begin in utero) had been presumed to be uniquely human.69

  Born smiling, chimpanzees keep right on doing so. Two months after Ayumu’s birth, Matsuzawa and his team videotaped the baby chimpanzee’s wildly enthusiastic (and infectious) “social” smiles in response to photographs affixed above the lens that portrayed either his mother’s face or the face of his mother’s very responsive human friend, Matsuzawa, who had become the baby’s trusted friend as well. Baby Ayumu’s response to his mother was the same gleeful greeting that Ai reserved for Matsuzawa himself, only there was no camera behind Matsuzawa’s eyes to film it. In line with Peter Hobson’s assessment of how much relationships matter for the development of social cognition in children, Matsuzawa showed that early relationships matter for chimpanzees as well.

  When Matsuzawa looked into his face, Ayumu returned his gaze, with eyes lighting up, radiating infectious glee. It would be impossible for another ape, chimpanzee, or human not to respond. Just watching Matsuzawa’s videos, my own countertransference was complete. Needless to say, I smiled back. (Nancy Enslin/T. Matsuzawa)

  INTERACTIVE FOUNDATIONS WITH A NEW DIMENSION

  Could a baby chimpanzee, gazing into someone else’s face and interacting with others, also identify with—perhaps even empathize with—others sufficiently to imitate the expressions on their faces the way human babies do? Neural equipment dedicated to registering eye gaze is built into the brains of most vertebrates, but it is especially well developed in humans. Within days of birth, human newborns seek out eyes and will look longer at any face if there are eyes there looking back. Soon after, babies spontaneously smile or laugh on making contact. By six months of age, little humans not only are attracted to eye gaze but also begin to evaluate just what the person observed is gazing at.70 A direct gaze produces stronger neurological responses than an averted one.71 Visually engaging eyes and face-to-face gazing play a key role in the mind reading and imitation process among infants. It has even been suggested that gazing’s importance may help explain why children born blind are prone to difficulties developing connections with others.72

  As
if Ayumu’s revelations were not enough, another little chimpanzee was born at Matsuzawa’s institute, and unfortunately, as not infrequently happens with apes artificially reared in captivity, the mother failed to care for her. Within 24 hours of birth, the keepers transferred the newborn to an incubator for bottle-feeding. Masako Myowa, one of the students working with Matsuzawa, saw in this tragic separation an opportunity to find out just what the imitative capacities of a baby chimpanzee actually are. Myowa already knew that apes readily learn to use tools and solve problems by first watching others and then imitating the way others solve the same problem.73 Indeed, chimpanzees reared by people may be even better at imitating what people do than human babies are.74 From watching Matsuzawa with Ai, Myowa understood how important the relationship between subject and investigator could be, and also (in line with Bard’s research) realized that human-reared chimpanzee newborns were likely to react to human facial expressions. Chimpanzees reared by humans were probably going to be even more prone to respond to facial expressions than those raised by their own mothers. Thus, Myowa reasoned, if other apes possess any capacity to respond to or imitate facial expressions, the little female she was rearing would be a good prospect to prove it.

  Myowa’s hunch paid off, resulting in an astonishing series of photographs. Literally aping Meltzoff and Moore’s famous experiment, the photos chronicled a wide-eyed baby chimpanzee responding to the funny faces Myowa made by sticking out her tongue, opening her mouth, protruding her lips, and to all appearances enjoying this process very much. Myowa’s little apprentice turned out to be even more persistent in responding to mouth movements than human babies are.75

  At least that’s how the little chimpanzee behaved at first. By 12 weeks after birth, however, the baby who had previously seemed so responsive and eager to imitate Myowa lost all interest in doing so. She had begun to respond at about five weeks and continued through eleven weeks, and then bam! Myowa contorted her face in all sorts of odd configurations, but got no response. The game had lost its appeal. In subsequent experiments, other baby chimpanzees followed the same course.76 Then in 2006, a team of cognitive neuroscientists claimed to have demonstrated that newborn monkeys (rhesus macaques) also imitate facial expressions. But once again, the urge to do so faded by day seven.77 Even though other primates are turning out to be far better at reading intentions than primatologists initially realized, early flickerings of empathic interest—what might even be termed tentative quests for intersubjective engagement—fade away instead of developing and intensifying as they do in human children.78

  In 1996, following the same format used by Meltzoff in 1977, Masako Myowa showed that a human-reared female chimp between 5 and 11 weeks of age would respond to a human experimenter who stuck out her tongue, opened her mouth, or protruded her lips by doing likewise. (M. Myowa-Yamakoshi)

  The documentation of facial imitation in nonhuman primates leaves many questions unanswered. Were the little macaques separated from their mothers really imitating the experimenters or just desperate to engage somebody, anybody, by making contact any way they could? Even though chimpanzee and human newborns stick out their tongues in response to someone else doing so, is this really what we mean by intentional imitation?79 Are the responses seen in very new babies really continuous with the more self-conscious and elaborate imitation human children exhibit at older ages? Recent findings by the psychologist Susan Jones suggest they may not be.

  Jones studied how willing 162 infants aged 6 to 20 months would be to imitate as their parents put a hand on their heads, stuck out their tongues, tapped on a table, wiggled their fingers, clapped their hands, or made funny little “eh, eh” noises. Overall, children younger than 12 months seemed to her less involved in “behavioral matching” than in responding to novel and interesting stimuli in their environment. It took most of the first two years, she determined, for true imitative ability to develop. Rather than a single “competency” present at birth, Jones proposed that this more self-conscious imitative capacity only emerges over time as children acquire an understanding about their body parts and what they can do.80 In other words, the responsiveness that is present at birth in humans—and also, we now know, in chimpanzees (and perhaps macaques)—is not the same imitative capacity apparent in human infants later on. By the second year of life, the human child has developed a sense of self and begun to combine it with new understanding about bodily competencies in ways that other apes never do.

  Interpreting such experiments is fraught with difficulties. For one thing, we lack anything like a complete understanding of what the neurological differences between chimpanzees and humans actually are. Nor can we be sure that the common ancestors of both chimpanzees and humans possessed the requisite neural basis for early processing of facial expressions, but my guess is that they did.

  Both ape and human newborns exhibit a powerful urge to connect with and engage others. Almost all spontaneously stick out their tongues, and some percentage of human and chimpanzee neonates are more prone to do so if they see someone else do it. Apes raised by humans may be especially susceptible, but humans (also of course raised by humans) are prone to develop such traits even further. Over time, human infants become increasingly sophisticated at learning not just what attracts attention but what appeals to others, which may be what is happening with imitation. All the same, if chimpanzees are less prone to imitate and learn from others by observing, if they are not as good at mind reading as children are, the difference cannot be attributed to a lack of the basic brain equipment.

  For example, consider dogs and why they do not copy their masters’ facial expressions. These domesticated descendants of wolves happen to be unusually good at reading human cues, perhaps even more sensitive to human cues like pointing to where a treat is hidden than many chimpanzees are.81 Nevertheless, dogs are no good at imitating a protruding tongue or other weird facial expressions, and this surprises no one. Dogs descend from cooperatively breeding wild ancestors, after all, and subsequently coevolved with humans and became dependent on bipedal alloparents for provisioning. But the basic neuromuscular underpinnings for this sort of facial imitation are simply not present in canines.

  We now know that some other primates possess mirror neurons and also look into the faces of those near to them, engage in deep mutual gazes, and imitate what they see there. They may even experience rudimentary empathy for the travails and suffering of others and (so long as it does not require giving up desirable food) voluntarily help others or share food with them. Since we’ve learned that such capacities are present (even if not always employed or expanded upon), we are confronted with a conundrum that until recently scientists did not even realize we had. We are challenged to explain why prosocial impulses became so much more developed in the line leading to the genus Homo. Why us and not them?

  A BIZARRE DIGRESSION

  Neither in humans nor any other ape does the initial impetus to connect need to be learned. Rudimentary wiring for intersubjective engagement seems to be there. But by seven weeks little humans up the ante, vocalizing with vowel sounds, and by ten weeks begin to laugh. Children spontaneously seek to engage others and do not need to be coached or bribed to do so.82 Although it is frequently assumed that such smiling and other facial expressions occur only in response to social stimuli or else must be learned, even babies born blind, who have never seen anyone make faces, start to smile around six weeks of age in response to touch, bouncing, or the sounds of a familiar voice.83 It seems possible then that even in a social vacuum human babies would spontaneously practice smiling and other means of social engagement. The closest demonstration of this point is an appalling experiment that I came across while trolling through the old psychological literature on smiling.

  Back in the 1930s, an American psychologist named Wayne Dennis and his wife managed to adopt one-month-old twin girls through the Social Services Department of the University of Virginia Hospital and then proceeded to rear the babies in virtual isolation
, out of sight of one another, visited only by the experimenter/adoptive parents. Whenever the Dennises were in the same room with the babies, they made every effort to keep their faces blank and deliberately refrained from giving the babies expressive templates to imitate. For their first 26 weeks, no one ever smiled or spoke to either Del or Ray, as the babies were called. Yet the normal onset of smiling in the socially deprived twins was only slightly delayed. From the fifteenth week onward the babies almost invariably greeted the still-faced experimenters “with a smile and a vocalization” whenever one of them opened the door and entered the room. Only after the twins were six months old did the psychologists decide to return the infants’ smiles and speak to them.84

  I was unable to learn anything about what became of these unfortunate children. After wrestling with myself over the advisability of including this story together with all its ethical and scientific lapses, I decided that it was in some ways instructive. Although the experiment is (mercifully) unlikely to be repeated, the observations are consistent with the premise that, like the fairy smiles of newborn chimpanzees and humans, social smiles and laughter emerge spontaneously, although social smiles (unlike neonatal smiles?) are triggered by some stimulus in the environment (including even a nonresponsive blank-faced caretaker entering the room). More conclusive work on this subject will require the kind of ingenuity, empathy for other apes, and patience so beautifully demonstrated by Matsuzawa and his colleagues, scientists keenly aware that it is no less cruel or distorting of natural inclinations to separate a nonhuman primate baby from an attachment figure than to rear human babies in isolation.