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.

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.

Do rhesus monkeys (Macaca mulatta) sense the beat?

Although monkeys seem to notice regularity in rhythmic sounds, they are not able to detect the actual beat. This is the finding of a new study by researchers from the University of Amsterdam (UvA) and the National Autonomous University of Mexico (UNAM). The study, published on 16 July 2018 in the journal Frontiers of Neuroscience, lends further evidence to the hypothesis that beat perception is omnipresent in humans but only gradually developed in primates. 

The gradual audiomotor evolution (GAE) hypothesis. The GAE hypothesis suggests connections between medial premotor cortex (MPC), inferior parietal lobe (IPL), and primary auditory area (A1) to be stronger in humans as compared to other primates (marked with red lines), suggesting beat-based timing to have gradually evolved. Line thickness indicates the hypothesized connection strength.

Even a cursory glance at the animal kingdom shows that most animals exhibit some sort of rhythmic behavior, like walking, flying, crawling or swimming. Based on this behavior, it wouldn’t be outlandish to think that the perception and enjoyment of rhythm might be shared by most animals, and not only humans. While recent experimental research is finding some support for this view, studies also show that there are certain aspects of rhythm cognition that are indeed species-specific, such as the capacity to perceive a regular pulse (beat) in a varying rhythm and consequently being able to synchronize or dance to it.

A rhythmic sequence

Building on their earlier research, the researchers investigated whether rhesus monkeys (Macaca mulatta) are able to perceive beat through a s0-called auditory oddball paradigm, an experiment in which sequences of repetitive sounds are infrequently interrupted by a deviant sound. ‘Most existing animal studies on beat-based timing and rhythmic entrainment have used behavioural methods to probe the presence of beat perception, such as tapping tasks or measuring head bobs’, says Henkjan Honing, professor of Music Cognition at the UvA and lead author. ‘However, even if certain species do not show a physical ability to synchronise their movements to a regular beat, this doesn’t automatically mean they are incapable of perceiving it.’

For their study, the researchers instead used electroencephalography (EEG) to measure neural correlates of rhythm cognition, including beat perception. The researchers presented two rhesus monkeys with a rhythmic sequence in two versions: an isochronous version that was acoustically accented in such a way that it could induce a duple metre (like a march), and a jittered version using the same acoustically accented sequence but presented in a randomly timed fashion so as to disable beat induction.

No evidence of beat perception

The results showed that monkeys are sensitive to the isochrony of the stimulus, but not its metrical structure. This so-called mismatch negativity (MMN) was influenced by the isochrony of the stimulus, resulting in a larger MMN in the isochronous as opposed to the jittered condition. However, the MMN for both monkeys revealed no interaction between metrical position and isochrony. Honing: ‘Even though the monkey brain appears to be sensitive to the isochrony of the stimulus, we couldn’t find any evidence in support of beat perception.’

The findings further strengthen the Gradual Audiomotor Evolution (GAE) hypothesis (Merchant& Honing 2014), which suggests ‘beat perception’ to be gradually developed in primates, peaking in humans but present only with limited properties in other non-human primates. The GAE is an alternative to the well-known ‘vocal learning hypothesis’, which suggests that only species who can mimic sounds share the ability for beat induction.

Publication details

Henkjan Honing, Fleur L. Bouwer, Luis Prado and Hugo Merchant, ‘Rhesus monkeys (Macaca mulatta) sense isochrony in rhythm, but not the beat: additional support for the gradual audiomotor evolution hypothesis’ in Frontiers in Neuroscience, 16 July, 2018. Doi: 10.3389/fnins.2018.00475

Difference between the GAE and VL hypothesis?

Summary diagrams of vocal systems in songbirds, humans, monkeys, and mice. 
(Figure 1 from Petkov & Jarvis in Ackermann et al., 2014).

Today a commentary was published in BBS in which the gradual audiomotor evolution (GAE) hypothesis (Honing & Merchant, 2014) is proposed as an alternative interpretation to the auditory timing mechanisms discussed in the target article by Ackermann et al. (2014).

While often a link is made between vocal learning (VL) and a species' auditory timing skills (e.g., 'entrainment'), the GAE and VL hypotheses show the following crucial differences.

First, the GAE hypothesis does not claim that the neural circuit that is engaged in rhythmic entrainment is deeply linked to vocal perception, production, and learning, even if some overlap between the circuits exists.

Second, the GAE hypothesis suggests that rhythmic entrainment could have developed through a gradient of anatomofunctional changes on the interval-based mechanism to generate an additional beat-based mechanism, instead of claiming a categorical jump from non-rhythmic/single-interval to rhythmic entrainment/multiple-interval abilities.

Third, since the cortico-basal ganglia-thalamic (CBGT) circuit has been involved in beat-based mechanisms in imaging studies, we suggest that the reverberant flow of audiomotor information that loops across the anterior pre-frontal CBGT circuits may be the underpinning of human rhythmic entrainment.

Finally, the GAE hypothesis suggests that the integration of sensorimotor information throughout the mCBGT circuit and other brain areas during the perception or execution of single intervals is similar in human and nonhuman primates.

Ackermann, H., Hage, S., & Ziegler, W. (2014). Brain mechanisms of acoustic communication in humans and nonhuman primates: An evolutionary perspective Behavioral and Brain Sciences, 1-84 DOI: 10.1017/S0140525X13003099
 
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 ]

 
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 

Rhythm cognition in humans vs monkeys explained?

This week a theoretical paper will come out in Frontiers in Neuroscience that reviews the literature on rhythm and timing in humans and nonhuman primates observing different species to species behavior in interval-based timing versus beat-based timing.

In this paper we propose the gradual audiomotor evolution hypothesis as an alternative to the vocal learning hypothesis (Patel, 2006) that was recently challenged as a pre-condition to beat perception and rhythmic entrainment (see earlier blogs on rhythmic entrainment in, e.g., chimpansees and sea lions).

The gradual audiomotor evolution hypothesis (Merchant & Honing, 2014; Honing & Merchant, in press) accommodates the fact that nonhuman primates (i.e. macaques) performance is comparable to humans in single interval tasks (such as interval reproduction, categorization, and interception), but show differences in multiple interval tasks (such as rhythmic entrainment, synchronization and continuation). Furthermore, it is in line with the observation that macaques can, apparently, synchronize in the visual domain, but show less sensitivity in the auditory domain.  And finally, while macaques are sensitive to interval-based timing and rhythmic grouping, the absence of a strong coupling between the auditory and motor system of nonhuman primates might be the reason why macaques cannot rhythmically entrain in the way humans do.

Dorsal auditory stream (light blue) and mCBGT in primates (from: Merchant & Honing, 2013).

Functional imaging studies in humans have revealed that the motor cortico-basal ganglia-thalamo-cortical circuit (mCBGT; see Figure) is involved not only on sequential and temporal processing, but also on rhythmic behaviors such as music and dance, where the auditory modality plays a critical role. However, the mCBGT circuit seems to be less engaged in audiomotor integration in monkeys as opposed to humans. While in humans different cognitive mechanisms can be shown to be active for interval-based timing versus beat-based timing, with beat perception being dependent on distinct parts of the timing network in the brain, the anterior prefrontal CBGT and the mCBGT circuits in monkeys might be less viable to multiple interval structures, such as a regular beat.

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 (Pre-Print).

Honing, H., & Merchant, H. (in press). Differences in auditory timing between human and non-human primates. Behavioral and Brain Science.

Can rhesus monkeys detect the beat in music?

Beat induction, the ability to pick up regularity – the beat – from a varying rhythm, is not an ability that rhesus monkeys possess. These are the findings of researchers from the National Autonomous University of Mexico (UNAM) and our group in Amsterdam, which are published today in PLOS ONE.

It seems a trivial skill: children that clap along with a song, musicians that tap their foot to the music, or a stage full of line dancers that dance in synchrony. And in way, it is indeed trivial that most people can easily pick up a regular pulse from the music or judge whether the music speeds up or slows down. However, the realisation that perceiving this regularity in music allows us to dance and make music together makes it less trivial a phenomenon.

Previous research showed that not only adult humans, but also newborn babies can detect the beat in music. This proved that beat induction is congenital and can therefore not be learnt. In their experiments with rhesus monkeys, the researchers used the same stimuli and experimental paradigms from previous research conducted on humans and babies. They measured electrical brain signals using electrodes while the participants were listening.

These research results are in line with the vocal learning hypothesis, which suggests that only species who can mimic sounds share the ability of beat induction. These species include several bird and mammal species, although the ability to mimic sounds is only weakly developed, or missing entirely, in nonhuman primates.

In addition, the results support the dissociation hypothesis, which claims that there is a dissociation between rhythm perception and beat perception. This new research suggests that humans share rhythm perception (or duration-based timing) with other primates, while beat induction (or beat-based timing) is only present in specific species (including humans and a selected group of bird species), arguably as a result of convergent evolution.


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