"The Evolving Animal Orchestra: In Search of What Makes Us Musical" By Henkjan Honing (MIT Press/Getty/Robbie Ross)

How playing music for rhesus monkeys is teaching us about our own brains

I study music cognition in primates — here's what it's teaching us about the biological evolution of music


Henkjan Honing
March 4, 2019 12:30AM (UTC)
Adapted from "The Evolving Animal Orchestra: In Search of What Makes Us Musical", by Dr. Henkjan Honing, translated by Sherry Macdonald, The MIT PRESS, 2019.

As a music cognition researcher interested in whether primates conceive of music, I was curious to understand more about the significance of sound for rhesus macaques in their natural habitat. Although they are confronted with sounds on a daily basis in the laboratory, it struck me as important to examine the role of sound and musicality in their life in the wild.

Not all primate researchers agree, but it appears that, generally speaking, most Old World primates show little interest in sound, let alone music. Of all their senses, seeing and smelling have much more important functions. Numerous studies of rhesus macaques indicate that their limited repertoire of noises serves mainly to signal either a threatening or a submissive stance. The noises they make play a significant role in determining and maintaining hierarchy in the group. Stare straight into the eyes of a rhesus macaque, as I did with Capi, and it will instantly feel threatened. The animal will grimace, bare its teeth, and start growling. The emotions of rhesus macaques can be read easily from their faces (by humans and rhesus macaques, that is), and their vocalizations add little to this picture.

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Rhesus macaques are social creatures. They make friendly noises, such as lip smacking. This behavior is particularly important as it signals friendly intentions. A lot of lip smacking occurs when two rhesus macaques approach each other, as well as during grooming and in other social situations.

In addition to growling and lip smacking, female rhesus macaques make another distinct noise, known as a “girney.” It is a soft, nasal, melodic cry which they use to attract the attention of the offspring of other female rhesus macaques, probably to assure their mothers that they mean no harm. The girney is sometimes compared to the human behavior of talking to infants and small children with an exaggeratedly rhythmic and highly melodic intonation, known in the jargon as infant-directed speech (IDS). All these noises, in both rhesus macaques and humans, may be remnants of what, in evolutionary terms, is an extremely old phenomenon, one we share with many other animal species—a precursor of language and music that allows us to exchange emotions and warn or reassure other members of our species. This interpretation can be viewed as further support for Darwin’s assumption.

It is also possible, though, that girneys are merely an expression of excitement at seeing an unknown youngster, because, strangely enough, rhesus macaques do not use girneys when communicating with their own offspring. Girneys may simply be a way of staying on good terms with other mothers: “What a lovely child you have!” With their own offspring, mothers usually limit themselves to the lip-smacking sounds of friendly intentions. Together, these three types of speech sounds — growling, lip smacking, and girneys — represent an extremely small repertoire compared with that of other vocalizing animals.

Acknowledging that sound is relatively insignificant for rhesus macaques makes any question about their possible musical preferences seem rather farfetched. Nonetheless, small-scale research has been conducted on the potential musical preferences of nonhuman primates. The best-known article, by researchers at Harvard University, has the revealing title “Nonhuman Primates Prefer Slow Tempos but Dislike Music Overall.” If nonhuman primates are made to choose between different types of sound—marmosets and tamarins were the test subjects here—they prefer the slow rhythmic chatter of other members of their own species. They show no interest at all in music. The same result emerged from studies with other species of primates. Gorillas, for example, in the Buffalo Zoo in New York state became restless when piano compositions by Frederic Chopin were played in their enclosures, whereas they were calmer than normal when exposed to ambient sounds such as those of the rain forest.

Although scientists often cite the Harvard research article, it has also been heavily criticized. The cotton-top tamarins were not exposed to the right music. The experiment used only human and Western music, from pop music to Mozart, but also German folk songs. The tamarins avoided Mozart the most. This may be disappointing news for human music lovers, but, of course, we do not know what these monkeys really hear and appreciate. The primatologist Frans de Waal was also bothered by the Harvard study’s choice of music samples and the conclusions it drew based on them. Together with his student Morgan Mingle, de Waal investigated how chimpanzees react to non-Western music. In his view, the findings of the Harvard study were not generally applicable because the experiments always used the same type of (Western) music. In a press release issued simultaneously with his research group’s article, de Waal proposed that chimpanzees may dislike or be put off by Western music only.

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De Waal’s research group alternately played African, Indian, and Japanese music near the chimpanzees’ outdoor enclosures for twelve consecutive days. In one part of the enclosure, the chimpanzees were exposed to the music for about forty minutes a day, while at other locations the music was almost inaudible. By observing where the chimpanzees stayed while the music was playing, the researchers were able to draw conclusions about how pleasurable (or irritating) the chimpanzees found it. It turned out the chimpanzees were neither bothered by, nor attracted to, the African or the Indian music but they clearly avoided the locations where the Japanese music could be heard.

The reader undoubtedly has some notion of what African, Indian, or Japanese music sounds like, but I doubt very much if the same is true for chimpanzees. As with the Harvard study, the research methods used by de Waal say nothing about the basis for the primates’ preferences. Exactly what they listened to is still unclear.

Nevertheless, the Harvard researchers were adamant in their interpretation and conclusions. According to them, the primates avoided the music of the Japanese taiko drummers because, like so much Western music, it was regular and rhythmic. That regularity could be perceived as threatening because it evokes associations with the rhythmic pounding, such as chest beating, which chimpanzees themselves sometimes display when they wish to assert their dominance.

This is, however, just the researchers’ interpretation, not one that is substantiated by the experiment itself. It is unclear which aspects of the music the chimpanzees found appealing, irritating, or tolerable. It could have been anything: melody, timbre, rhythm, timing, or the dynamic development of the music. For this reason, one cannot speak of musical preferences in chimpanzees. What was tested here was not so much a preference for the music of a particular culture as a sensitivity to a whole range of acoustic features. In this sense, the article’s title, “Chimpanzees Prefer African and Indian Music over Silence,” was an overstatement. The chimpanzees probably had no idea at all what African or Indian music did or could even sound like.

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An important question therefore remains: when does what we humans consider to be music sound like “music to the ears” of other primates?

Monkey Keeps the Beat

In 2011, when I first visited Mexico, the notion that nonhuman primates have beat perception was far from proven. In fact, the few studies conducted up until then indicated quite the opposite. Hugo Merchant, for example, had already demonstrated in 2009 that a rhesus macaque could not be taught to move a joystick back and forth synchronously to the sound of a metronome. Rhesus macaques cannot anticipate the way humans can.

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Other researchers, however, including me, remained convinced that nonhuman primates must have beat perception. Some researchers worked hard on experiments to demonstrate this theory. Others were less patient and presented their first impressions at conferences.

Patricia Gray of the University of North Carolina, Greensboro, is a case in point. She has a long-standing interest in music and biology and is convinced that nonhuman primates, particularly bonobos, experience a pleasure comparable to that of humans when they are beating a drum, and that they can clearly synchronize to the beat of music.

To demonstrate this idea, she had a special “bonobo-proof” drum built, one that was resistant to jumping, biting, and other similarly boisterous behavior. She then let the bonobos spontaneously drum along with human drummers sitting in an adjacent room. The heading of the press release issued later by Reuters read: “Bonobos, like Humans, Keep Time to Music.” It was big news and received worldwide coverage. Nonhuman primates have beat perception too!

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However, when I asked the authors for the original article because I was curious about the methodological details, to my surprise it turned out not to have been published. Despite repeated attempts, it had not been accepted by a scientific journal. Apparently it had not been found sufficiently convincing by colleagues.

This made our listening experiment with rhesus macaques all the more urgent. After all, we still faced several outstanding questions: Can a nonhuman primate hear the regularity (the pulse) in a varying rhythm, as we had already shown adult humans and newborns to be capable of? Or would rhesus macaques listen to music as if it were ambient sound, with no attention to the regularity that humans appear to consider so important?

Thessaloniki, Greece, July 26, 2012. I am sitting in a stifling hotel room, preparing my lecture for tomorrow. As I put the finishing touches on the text, several swifts skim past my balcony at eye level. Their extreme maneuverability and piercing calls always give me a feeling of intense joy.

This week I am attending an international conference on the theme of music cognition. At six o’clock tomorrow evening, I will present the preliminary findings of our research in a special session on rhythm perception. I think back on the conversations I have had with colleagues during the past week. One of them, Jessica Grahn, an American neuroscientist, also has plans to study rhythm perception in rhesus macaques and, in particular, the architecture and location of the neural networks involved. She, too, suspects that there is a fundamental difference between perceiving and processing regular and irregular rhythms. It may be that the network that recognizes regular, beat-based rhythms is missing in rhesus macaques.

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Jessica drew my attention to a recently published article from Japan, concerning a study that replicated the behavioral experiments conducted earlier in Hugo’s laboratory with rhesus macaques. The article reveals that two individuals from a related species of macaque (Macaca fuscata) can tap along to regular rhythms containing intervals of approximately one second but not much less. Again, however, they can only do this reactively and without anticipating.

I add a reference to this study to the slide show that I am preparing, then reread my notes. Will other colleagues at the conference agree with our interpretation of the findings? Might we have touched on something that further substantiates a difference between rhythm perception and beat perception? This was a difference I had already discussed with Hugo in Leipzig in 2011, based on the observation that, in humans, different neural networks are involved in processing regular (beat-inducing) and irregular rhythms. Or was it too good to be true?

In the final slide, I summarize the results of our three experiments. The finding of the first experiment should convince everyone. It shows that we can measure an MMN in a rhesus macaque. It is a new finding and is demonstrated for the first time in our study. If it also helps to increase the popularity of this noninvasive method, that would be a wonderful secondary result.

The second experiment, with the unexpected rest, is also convincing. Although we still need to replicate the effect in at least one other rhesus macaque now that Capi’s test results have turned out to be unusable, Yko’s brain appears to register unexpected silences.

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Together, the first two experiments bring us to the right starting point for the third experiment, in which we let Yko listen to a complex, varying rhythm (as we had done earlier with the newborns). In this experiment, we detect no difference in the brain signals in reaction to any silence. For Yko, all the silences appear to be equally unexpected. He notices all of them, unlike the newborns, who had only noticed a silence on the downbeat. This means that Yko is insensitive to the regularity that human listeners perceive in the rhythm, and the “loud rest” is as imperceptible to him as all the other “silent” rests.

Although the findings are based on a series of experiments involving only one rhesus macaque, the conclusion we will present tomorrow will be the same as the one we reached in Queretaro last January, namely, that  rhesus macaques do not have beat perception.

Amsterdam, November 6, 2012. This morning, rather mischievously, I send Hugo an e-mail with the sound of a champagne bottle being uncorked. Our article has been accepted! It will be published in a few weeks’ time, under the title “Rhesus Monkeys (Macaca mulatta) Detect Rhythmic Groups in Music, but Not the Beat,” precisely one year after my first visit to Mexico.

Since adding the results for Aji, the third rhesus macaque who by now had taken part in our listening experiments, we have a clear conclusion: rhesus macaques do not perceive regularity in a varying rhythm.

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I am proud of the result, even if it is not what I had expected. After all, with Darwin as the great inspiration, I had anticipated that rhesus macaques would have beat perception. Our research also demonstrated that the “heartbeat as the source of beat perception” hypothesis was improbable. After all, all mammals (including rhesus macaques and humans) hear the heartbeat in the womb. It seems more likely that specific neural networks enable beat perception, and that these networks are weaker or absent in rhesus macaques.

This finding also seems congruent with the theory of speech evolution. Research had recently demonstrated that the reason humans can talk while nonhuman primates cannot, is not because nonhuman primates lack an anatomical adaptation (such as a larynx, a tongue, or lips) but rather because they lack the neural control mechanisms that make speech possible. Here, too, it is the brain that makes the difference.

While all of this may appear to be a negative outcome—rhesus macaques cannot do something that humans can—the insights contributed greatly to the advancement of theories about the biological basis for language and music. The ongoing challenge was to combine methods and techniques from different disciplines to achieve new insights. When our ten-page article appeared in the scientific journal PLOS One, I also realized it would only be a temporary milestone in what would undoubtedly still be a long journey to trace beat perception in nonhuman animals. It was now a question of waiting for the first replications and the detailed nuances of the research findings.

Apart from possible nuances, our article made the case for using noninvasive electrophysiological techniques in neurocognitive research. With these kinds of techniques, it should also be possible to take measurements outside the laboratory, in situations more natural than those when animals are raised in captivity. Take, for example, the type of EEG headsets now commonly used when playing computer games. In other words, even if the results of replication studies do not, or only partially, remain unchallenged, then at least I will not have subjected Aji, Capi, and Yko to my rhythms in vain.

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Gradual Evolution

In the following months, I work with Hugo to reinterpret the abundant literature appearing on the subject of beat perception. Although Darwin suspected that all animals with a nervous system would have beat perception, this turned out not to be true, at least not for all primates. Should beat perception therefore be seen as a capacity that had developed only recently and gradually in the evolution of primates?

Rereading and reinterpreting the recent literature culminated in the formulation of what we called the “gradual audiomotor evolution (GAE)” hypothesis. Admittedly, it is not the most inspired name, but we based our hypothesis on the existing neurobiological literature, which suggested that the neural networks that enable beat perception in humans are absent or less developed in rhesus macaques. In humans, this network connects the auditory system (hearing) with the motor system, which controls the movements of our limbs and mouth, such as clapping, dancing, or singing. Even if you leave test subjects lying motionless in a functional magnetic resonance imaging (fMRI) scanner and let them listen to metrical and nonmetrical rhythms, activity is still visible in the motor cortex as a result of the metrical, beat-inducing rhythms. Clearly, an information exchange takes place between the auditory and motor systems.

The absence of a strong connection between the auditory cortex and the motor cortex in most nonhuman primates may well be the reason why humans do and other nonhuman primates do not (or only to a lesser degree) have beat perception. We also proposed that this connection would likely be present in rudimentary form in chimpanzees, and therefore that chimpanzees would probably have beat perception in an embryonic form. If what we proposed was true, then we could date the origin of beat perception in primates to the time of the common ancestor of chimpanzees and humans, some five to ten million years ago. Of course, no study could be found to support this part of the hypothesis. It was therefore purely speculative. Nevertheless, in my eyes, the GAE hypothesis still offered an attractive alternative to the “beat perception is uniquely human” hypothesis, which

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I thought was considerably less likely. After all, a striking number of the neural structures and networks that humans have at their disposal also exist in rhesus macaques and other nonhuman primates. In addition, rhesus macaques are no less skilled at “interval timing” than humans. Macaques can reproduce the interval between two clicks properly and accurately and also have no problem classifying a time span as either long or short.

What appears to be missing in rhesus macaques is the ability to perceive several intervals in succession. If a rhesus macaque is asked to perform a task in which not one but multiple intervals demand attention—as is necessary for recognizing a regular rhythm—it turns out to be difficult, if not impossible, for the macaque. A strong connection between the motor and auditory systems appears to be vital for beat-based timing or beat perception.

Synchronizing

The musicality research agenda was gradually becoming more clearly defined, and interest in the cognitive and biological origins of musicality was growing, especially in the phenomenon of beat perception. More and more primatologists and other animal researchers were prepared to devote their precious research capacity to further probing this aspect of musicality. Their underlying motivation was to disprove the notion that beat perception was uniquely human. For that question, too, still remained: is beat perception uniquely human or not?

One example of researchers dedicated to investigating musicality is Yasuo Nagasaka and his colleagues at the Riken Brain Science Institute in Wako, Japan. They devised an experiment designed to assess the extent to which the ability to perceive “natural” or spontaneous regularity is present in the behavior of nonhuman primates. To this end, they placed two Japanese macaques (Macaca fuscata) in primate chairs on opposite sides of a table facing each other and taught them to alternately press the left and right buttons on the panel in front of them. If they did this regularly and at least ten times in succession, they were rewarded with a scattering of nuts or a piece of apple.

The researchers were interested in entrainment, a natural phenomenon in which two oscillating systems match their periods and phases after a period of time. The Dutch physicist Christian Huygens (1629–1695), the presumed discoverer of this phenomenon, described it in 1665 after noticing that the motion of the pendulums of two wall clocks synchronized over time.

Entrainment can be demonstrated clearly with two metronomes, often used by musicians who are learning to play at the proper tempo. When two metronomes are set at the same tempo, they move back and forth at the same speed, or period. Rather than being synchronized at the beginning, they will be out of phase: the pendulum of one metronome, for example, will have swung only halfway across, while the pendulum of the other will already be swinging back. Surprisingly, if both metronomes are placed on a plank, itself resting on a surface that can move back and forth freely— for example, on two soft-drink cans lying on their side—after a short time the two pendulums will move into phase. For the remainder of the time, while rocking gently on the plank, they will continue to tick in perfect unison. This resembles the phenomenon of unconsciously walking to the beat of music that one hears on the street, regardless of whether one likes the music or not.

What is intriguing about such a complex and dynamic system is that it can be described clearly in mathematical terms. Calculations can be performed, precise predictions made, and specific observations assessed to see whether they meet the criteria of a similar system of coupled oscillators—in this case, the movements of two Japanese macaques.

The question here was: Could the macaques synchronize or “entrain” with the sound they heard in the same way that coupled oscillators do? And if so, did the macaques do so under the influence of what they saw, what they heard, or a combination of the two?

When the findings were analyzed, it appeared that the sound had virtually no impact on the synchronization. The Japanese macaques were therefore insensitive to the regularity of the sound. They did synchronize with the sound, however, when they were able to see the other macaque. In other words, the macaques were able to synchronize on the basis of what they saw, but not on the basis of what they heard. In this kind of experimental context, noise also turns out to be insignificant in terms of what Japanese macaques pay attention to.

In the months following the publication of this and other studies in 2013, the discussions that took place on the various scientific forums focused mainly on the question of whether the absence of beat perception in animals was categorical—some animals have it, while others do not—or whether there were gradations. If rhesus macaques, or macaques in general, did not have beat perception, then surely, I thought, chimpanzees and other anthropoids did. I went off in search of a research group interested in rhythm perception in chimpanzees. Two years later, I found it.

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Adapted from "The Evolving Animal Orchestra: In Search of What Makes Us Musical", by Dr. Henkjan Honing, translated by Sherry Macdonald. Published by The MIT Press, 2019.


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