Precursors of music and language?

Diagrammatic representation of the comparative approach. It shows a hypothetical phylogenetic tree that illustrates the evolution of several traits that humans may share with monkeys and birds. Filled shapes represent a hypothetical trait (such as vocal learning or beat perception); open shapes indicate the absence of that trait. The position on the phylogenetic tree dates the possible evolutionary origin of such a trait. N.B. Circle: homologous trait, present in human and monkeys, originating from a shared ancestor; Square: an independently evolved trait, similar in humans and birds by convergence.

Language and music are universal human traits, raising the question for their evolutionary origin. In a recent review, co-authored with Carel ten Cate (LU), we take a comparative perspective to address that question.

In the chapter (ten Cate & Honing, in press) we examine similarities and differences between humans and non-human animals (mammals and birds) by addressing whether and which constituent cognitive components that underlie the human ability for language and music can be found in non-human animals. It first provides an introduction to the nature and meaning of vocalizations and non-vocal communicative sounds in non-human animals. Next it reviews experimental and observational evidence of animal perception of various frequency and temporal dimensions of sounds. Many animal species show perceptual and cognitive abilities to distinguish between or to generalize auditory stimuli. This includes evidence of the presence of one or more of the constituent cognitive components on which the human abilities for language and music are based, or that may have served as precursors for these components. At the same time, there are also important differences among animal species in their abilities. Hence contrasts are not limited to those between humans and other animal species.  

We conclude that the differences between humans and other species, as well as those among non-human species, might result from specific biases and the weight or priority certain species give to attending to certain features of an acoustic signal, or because different species use particular mechanisms to different degree.

ten Cate, C. & Honing.H. (2023, in press). Precursors of music and language in animals. In Sammler, D. (ed.), Oxford Handbook of Language and Music. Oxford: Oxford University Press. doi: psyarxiv.com/4zxtr

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 

Do chimps like to listen to African and Indian music?

©2014, Emory University.

This week an interesting study, co-authored by primatologist Frans de Waal, appeared online in the Journal of Experimental Psychology: Animal Learning and Cognition. It was summarized in a Press Release as follows:

“While preferring silence to music from the West, chimpanzees apparently like to listen to the different rhythms of music from Africa and India, according to new research published by the American Psychological Association.” 

While the first part of this summary must be wrong (the study did not present any Western music to chimpanzees, neither did any other study), the study does provide intriguing evidence for a difference in preference between West-African and North Indian music on the one hand, and Japanese taiko music and silence on the other. Chimps apparently prefer the former sounds in their environment over the latter.

The paper is framed as a critical answer to an older study by McDermott and Hauser (2007) that showed nonhuman primates (i.e., cotton-top tamarins and marmosets) to prefer slow tempos and silence over music, but dislike music overall. But are these studies also an indicator of musical preference?

Here Frans de Waal is clear and precise:

“Our objective was not to find a preference for different cultures’ music. We used cultural music from Africa, India and Japan to pinpoint specific acoustic properties. Past research has focused only on Western music and has not addressed the very different acoustic features of non-Western music. While nonhuman primates have previously indicated a preference among music choices, they have consistently chosen silence over the types of music previously tested.” 

So the different stimuli were in fact used to test a sensitivity to a complex of acoustic properties. Because if one would like to test a musical preference, one needs to know what the chimps are listening for. Is it loudness, timbre, melody, rhythm, timing, etc.

Unfortunately the stimuli are not provided online, or described in such a way that the original recordings can be traced, very much against the notion of replicability common in most empirical research. Hence, we can not listen to them for ourselves or run computer algorithms to extract the musical and/or acoustic features for comparison. We have to do with a rather crude characterization of the stimuli (For example, the 'Japanese taiko stimulus' is characterized as atonal, with undefined pitch, and 1 strong beat per 1 weak beat) and guess what the acoustical differences were. Yet another strange detail: some of the music was slowed down artificially, this to bring all stimuli in the same tempo range. A peculiar transformation that humans would readily notice (see earlier entry).

The authors themselves have an intuition on what might have caused the difference. They make the observation that Japanse taiko (like Typical Western music) has a regular beat, and it might be that this regularity is what chimpanzees dislike:

“Chimpanzees may perceive the strong, predictable rhythmic patterns as threatening, as chimpanzee dominance displays commonly incorporate repeated rhythmic sounds such as stomping, clapping and banging objects” 

Sounds reasonable, not?

Well, the experiment was not designed such that it could show that it is indeed the rhythmic structure that these chimps were attending to. In fact, there is no convincing evidence as yet that chimpanzees, or any other nonhuman primate, can actually perceive rhythmic regularity (See earlier entry).

Although it is suggested that apes (as opposed to monkeys) might have some of the neural circuitry that is needed for beat perception (Merchant & Honing, 2014), it has never been shown that any of the great apes can perceive the beat in a rhythmically varying stimulus such as music (See discussion in earlier blogs on the topic of beat induction).

What has been shown, however, is that monkeys can be sensitive to the rhythm structure or rhythmic grouping (cf. Merchant & Honing, 2014). Hence it is more likely that it is the rhythmic structure (or rhythmic grouping) that the chimpanzees use to distinguish between the musical stimuli, instead of perceived regularity: the beat. Nevertheless, it could also be any of those many other features of music that makes the difference for them: dynamic contour, timbre, note density, melodic contour, timing, etc, etc.

[See related item in Dutch newspaper de Volkskrant.]
[See related item in Psychology Today.]

Mingle, M., Eppley, T., Campbell, M., Hall, K., Horner, V., & de Waal, F. (2014). Chimpanzees Prefer African and Indian Music Over Silence. Journal of Experimental Psychology: Animal Learning and Cognition DOI: 10.1037/xan0000032

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.

McDermott, J., & Hauser, M. (2007). Nonhuman primates prefer slow tempos but dislike music overall Cognition, 104 (3), 654-668 DOI: 10.1016/j.cognition.2006.07.011

Can bonobos synchronize to the beat?

A five-year-old bonobo (c) Reuters

Today the Daily Mail reports on an exciting new finding: Patricia Gray (University of North Carolina in Greensboro) and Ed Large (University of Connecticut) claim to have shown that bonobo's can synchronise to a beat.

According to Science News "the researchers gave a group of bonobos access to a specially tailored drum, then showed them people drumming rhythmically. Eventually three animals picked up the beat and were able to match tempos with the scientists. Bonobos were also found to prefer a faster pace than most people."


I'm still tracing the actual published paper. More in a few hours... I hope.

Update 20140218: It turns out the paper is still in preparation. While one of the authors was so kind to share a draft with me (confidentially that is), I guess we have to wait for the normal peer-review process to see whether the claims made in the Press Release – so confidently distributed via Reuters – can indeed be substantiated. Quite an unusual order of things, I have to say.

De Waal, Frans B.M. (1988). The Communicative Repertoire of Captive Bonobos (Pan Paniscus) Compared To That of Chimpanzees. Behaviour, 106 (3), 183-251 DOI: 10.1163/156853988X00269

Related press: See e.g., news item on Radio 1 België. 

P.S. In the Netherlands, bringing out facts as scientific, but that are not checked by peers (e.g., by journal peer-review), is considered bad practice. (In fact, it has lead in the past to several reprimands imposed by university representatives on the researchers involved.) These kind of 'incidents' cannot be good for the image of music cognition nor for science in general.

Differences in rhythm perception between human and non-human primates

[Press Release University of Amsterdam]  Despite their genetic proximity, human and non-human primates differ in their capacity for beat induction, which is the ability to perceive a regular pulse in music or auditory stimuli and accordingly align motor skills by way of foot-tapping or dancing.

Also referred to as ‘rhythmic entrainment’, this ability is specific to humans and certain bird species, but is surprisingly enough not obvious in non-human primates. These are the findings of researchers from the University of Amsterdam and the National Autonomous University of Mexico (UNAM), whose new hypothesis, the ‘gradual audiomotor evolution hypothesis’, was recently published in the scientific journal Frontiers in Neuroscience.

Gradual audiomotor evolution hypothesis

The gradual audiomotor evolution hypothesis accommodates the fact that non-human primates’ (i.e., macaques) performance is comparable to humans in single interval tasks such as interval reproduction, categorisation and interception, but show differences in multiple interval tasks such as rhythmic entrainment, synchronisation and continuation. The hypothesis is also in line with the observation that macaques can apparently synchronise in the visual domain, but show less sensitivity in the auditory domain. Finally, while macaques are sensitive to interval-based timing and rhythmic grouping, the absence of strong coupling between the auditory and motor system of non-human primates might explain  why macaques cannot rhythmically entrain in the way humans do.

Timing networks in the primate brain

Functional imaging studies in humans have revealed that the motor cortico-basal ganglia-thalamo-cortical circuit (mCBGT) is not only involved  in sequential and temporal processing, but also in rhythmic behaviours such as music and dance, where auditory modality plays a critical role. The mCBGT circuit, however, seems to be less engaged in audiomotor integration in monkeys than in humans. While in humans different cognitive mechanisms are 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.

Recent findings weaken the vocal learning hypothesis

The gradual audiomotor evolution hypothesis 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. Because recent empirical findings have challenged this hypothesis, an alternative was needed. 

Publication details

Merchant, H., & Honing, H. (2014; online). 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

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

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.

'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

Are monkeys capable of rhythmic entrainment?

Hugo Merchant Lab

On Friday 24 May 2013  Hugo Merchant (Institute of Neurobiology, Querétaro, Mexico) will give a CSCA Lecture with the title Neurophysiology of temporal and sequential processing during a synchronization-continuation tapping task. He will present a recent study investigating rhythmic entrainment in Rhesus monkeys (Macaca mulatta).

A recent study has shown that Japanese macaques (Macaca fuscata) are able to spontaneously synchronize their arm movements when they are paired and facing each other, suggesting that monkeys can coordinate their actions in a social setting and establish some level of rhythmic entrainment (Nagasaka et al., 2013; see earlier entry). However, the asynchronies between the pairs of tapping monkeys are positive, largely dependent on the visual input that the other monkey provides, and with little influence on the sounds that the monkeys made when tapping. The question remains of whether more closer human relatives such as the great apes, show a more sophisticated ability for rhythmic entrainment than macaques.

Macaca mulatta

Hugo Merchant will present a recent study in which two monkeys (Macaca mulatta) were trained in a synchronization-continuation tapping paradigm called a synchronization-continuation tapping task (SCT) in which auditory (A) or visual (V) cues were presented to construct the periodic target interval ranging from 0.45 to 1 second. Initially, animals synchronized their arm movements with a sensory cue by tapping on a push-button, followed by self-pacing of the target interval when the metronome was switched-off. In addition, the monkeys performed a single interval reproduction task (SIRT). We recorded the single-cell activity of 1500 neurons from the macaque medial premotor cortex (MPC) during the task performance.

The results suggest that distinct populations of cells in the MPC can encode different temporal and sequential aspects of the SCT and suggest that MPC is part of a core timing network that uses interval tuning as a signal to represent temporal processing in a variety of behavioral contexts where time is explicitly quantified.

Location: room DS.02, REC D, Nieuwe Achtergracht 129 (entrance through REC G, Nieuwe Prinsengracht 130), Amsterdam.

Time: 16:00 - 17:00 hrs, followed by informal drinks. Registration is not necessary.

For more information, see the website of the CSCA.

Nagasaka, Y., Chao, Z., Hasegawa, N., Notoya, T., & Fujii, N. (2013). Spontaneous synchronization of arm motion between Japanese macaques Scientific Reports, 3 DOI: 10.1038/srep01151

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