Music in our genes?

© ILLC Blog, Illustration by Marianne de Heer Kloots

 

 

"In 1984, a curious study on musicality in animals was published. The researchers from Portland, Oregon trained pigeons to distinguish two pieces of music – one by Bach, the other by Stravinsky. If the birds got it right, they were rewarded with food. Afterwards, the same pigeons were exposed to new pieces of music from the same composers. Surprisingly, they were still able to determine which piece was composed by which composer.

This finding confronted researchers with a new set of questions. To what extent are animals musical? What does it even mean for an animal to be musical? And what can this teach us about musicality in humans?" 

(From Music in our genes, ILLC Blog).

The interview is based on an episode of the podcast “Talk that Science” – an initiative started by students from the University of Amsterdam.

• Listen to the episode here (in Dutch);

• Link to the English transcript can be found here.

Empirical support for the GAE hypothesis?

Yesterday PNAS published a study by Yuko Hattori and colleagues entitled Rhythmic swaying induced by sound in chimpanzees. The study presents further support for the GAE-Hypothesis (see a detailed description in The Evolving Animal Orchestra, 2019, MIT Press, Chapters 4 and 5):

"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 suggests that the neural networks that enable beat perception in humans are absent or less developed in rhesus macaques (figure 4.1). 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. No study could be found to support this part of the hypothesis. It was therefore purely speculative."

Thanks to Yuko Hattori this idea is now much less of a speculation. Thanks for all the hard work!

See also, Science Magazine, The Guardian and NRC:

Hattori, Y., Tomonaga, M. (2019) Rhythmic swaying induced by sound in chimpanzees (Pan troglodytes). PNAS. doi: 10.1073/pnas.1910318116.

Honing, H., & Merchant, H. (2014). Differences in auditory timing between human and non-human primates. Behavioral and Brain Sciences, 27(6), 557-558 DOI: 10.1017/S0140525X13004056. [Alternative link: http://www.mcg.uva.nl/papers/Honing-Merchant-2014.pdf ]

Music, explained?

"Music is everywhere. We hear it in our cars, in coffee shops, on TV, and at church. We use it to learn, remember, feel, celebrate, and connect. Every known human culture has had some form of music. But in the rest of the animal world, the ability to understand and create music is rare. Where humans might hear rhythm and melody, rhesus monkeys, for example, just hear noise. So what makes music so universal among humans? How does sound become something more? And how does it evoke such a wide range of emotions?"

Joe Posner of Vox tackled these questions in a recent episode of the Netflix' Explained series. See Music, explained (Episode 20) here.

Visiting the The University of Tokyo and Primate Research Institute in Inuyama

I had a wonderful few days in Tokyo for a small symposium and workshop organized by Kazua Okanoya (e.g., ten Cate & Okanoya, 2012) and a full day at the Kyoto Primate Research Institute as a guest of Yuko Hattori (e.g., Hattori et al., 2013, Hattori et al., 2015)

In Tokyo I met with several researchers working on rhythm, time perception and music, including Shinichi Furuya (Sophia University, Japan), Yoshimasa Seki (Aichi University, Japan), Noriko Katsu (Osaka University, Japan), Florian Waszak (Université Paris Descartes, France), and Kazuo Okanoya (Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Japan). It was a great afternoon that was wrapped up with a diner in a local restaurant were, in a round of introductions of the about twenty people that were present, there was Nō singing, Japanse rap and a tenor version of Ave Maria! For abstracts of the workshop see here.

A few days later I visited the Primate Research Institute (KUPRI) in Inuyama. Yuko Hattori was a superb host, showing me the elaborate facilities and allowing me to attend several ongoing experiments on visual and auditory cognition. I met with Ai, Ayumu and Akira and several other chimpansees well-known from the literature (see earlier blogs). Meeting Ai for the first time, after reading so much about her, was quite an emotional moment. See Ai doing one of her famous experiments below:

 Try to remember the position of the numbers on the screen, and then tap them out in ascending order. First you see me doing the task, and then Ai. Impressive, not?

Hattori, Y., Tomonaga, M., & Matsuzawa, T. (2013). Spontaneous synchronized tapping to an auditory rhythm in a chimpanzee Scientific Reports, 3 DOI: 10.1038/srep01566

Hattori, Y., Tomonaga, M., & Matsuzawa, T. (2015). Distractor Effect of Auditory Rhythms on Self-Paced Tapping in Chimpanzees and Humans PLOS ONE, 10 (7) DOI: 10.1371/journal.pone.0130682

ten Cate, C., & Okanoya, K. (2012). Revisiting the syntactic abilities of non-human animals: natural vocalizations and artificial grammar learning Philosophical Transactions of the Royal Society B: Biological Sciences, 367 (1598), 1984-1994 DOI: 10.1098/rstb.2012.0055

Further support for the Gradual Audiomotor Evolution (GAE) hypothesis?

Chimpanzees (left: Chloe, right: Cleo) conducting a finger-tapping task.

Recently four chimpanzees –all born at the Primate Reserach Institute, Kyoto University–  participated in a finger-tapping experiment, using a paradigm that have been explored for decades with humans (Repp, 2005). Two chimps, Chloe and Cleo, showed signs of synchronization, according to a study that just came out in Scientific Reports (Yu & Tomonaga, 2015). Although the results may have limitations in generalizing to chimpanzees as a species, this might be further evidence for the Gradual Audiomotor Evolution (GAE) hypothesis (Merchant & Honing, 2014).

[See also earlier blog entry]

Merchant, H., & Honing, H. (2014). Are non-human primates capable of rhythmic entrainment? Evidence for the gradual audiomotor evolution hypothesis. Frontiers in Neuroscience, 7 (274) 1-8. doi 10.3389/fnins.2013.00274

Repp, B. (2005). Sensorimotor synchronization: A review of the tapping literature Psychonomic Bulletin & Review, 12 (6), 969-992 DOI: 10.3758/BF03206433

Yu, L., & Tomonaga, M. (2015). Interactional synchrony in chimpanzees: Examination through a finger-tapping experiment Scientific Reports, 5 DOI: 10.1038/srep10218

'Vocal mimicry hypothesis' falsified? [Part 2]

Figure (a) Ai tapped C4, (b) Ai tapped C5, (c) Time sequence of a test trial.

A few entries ago I uploaded a fragment from a study (Hattori et al., 2013) that discusses an intriguing experiment with three chimpanzees (Pan troglodytes) which were trained to tap regularly on a piano keyboard.

While the video below is convincing, the study reports that only one of the three chimps participating in the experiment was able to do the task: a chimp named Ai (See video).  Furthermore, Ai was only able to synchronize with stimuli at a rate of 600 ms (and not at rates of 400 or 500 ms). In addition, Ai did this in reaction (positive asynchrony) and not in anticipation of the beat (negative asynchrony).

This is similar to what has been found in studies with macaques (Zarco et al., 2009; Konoike et al., 2012) that also seem to opt for a strategy of to react instead of anticipating to a regular beat. All this in contrast with humans that can intentionally synchronize their tapping to various rates (ranging roughly from 200 ms to 1800 ms) of a varying rhythmic stimulus (and not simply a metronome) while showing a negative synchronization error, i.e. in anticipation of the beat.

Another point of a more methodological nature is that the experimentators used, next to sound, what they called 'light navigation' (see diagram above), a visual cue for the chimps to 'remind them' of which key to press. While the authors write "it was unlikely that the visual stimuli affected tapping rhythm by chimpanzees" we can not be sure this is evidence for rhythmic entrainment in the auditory domain.

Nevertheless, with behavioral methods that rely on overt motoric responses it is difficult to separate between the contribution of perception and action (beat perception vs beat production). This makes electrophysiological measures (such as event-related potentials) a more direct and hence attractive alternative. The latter method has been shown a worthwhile, non-invasive alternative in studying cognitive and neural processing in primates (see, e.g., Ueno et al., 2009) and it was used recently in a study probing beat perception in macaques (Honing, Merchant et al., 2012).*

And lastly, these and earlier observations have lead to the auditory timing dissociation hypothesis (Honing, Merchant et al., 2012). This hypothesis accommodates the fact that nonhuman primates performance is comparable to humans in single interval tasks (such as interval reproduction, categorization and interception), but differs substantively in multiple interval tasks (such as rhythmic entrainment, synchronization and continuation).

* N.B. We are eager to collaborate with a primate lab that is willing to do such a relatively simple listening experiment using EEG with chimpanzees; Would be great to compare the results we now have for human adults, newborns, and macaques with the perception of Great Apes ! Feel free to email me :-)

Hattori, Y., Tomonaga, M., & Matsuzawa, T. (2013). Spontaneous synchronized tapping to an auditory rhythm in a chimpanzee. Scientific Reports, 3 DOI: 10.1038/srep01566.

Hasegawa, A., Okanoya, K., Hasegawa, T., & Seki, Y. (2011). Rhythmic synchronization tapping to an audio–visual metronome in budgerigars Scientific Reports, 1 DOI: 10.1038/srep00120

Honing, H., Merchant, H., Háden, G., Prado, L., & Bartolo, R. (2012). Rhesus Monkeys (Macaca mulatta) detect rhythmic groups in music, but not the beat. PLoS ONE, 7 (12) DOI: 10.1371/journal.pone.0051369