Monday, January 28, 2013

Can monkeys spontaneously synchronize to audio?

Setup for the three experiments (from discussed publication).
It was recently shown that rhythmic entrainment, long considered a human-specific mechanism, can be demonstrated in a select group of bird species, and, somewhat surprisingly, not in more closely related species such as nonhuman primates. This observation supports the vocal learning hypothesis that suggests that rhythmic entrainment is a by-product of the vocal learning mechanisms that are shared by several bird and mammal species, including humans, but that are only weakly developed, or missing entirely, in nonhuman primates. However, since no evidence of rhythmic entrainment was found in many vocal learners (including dolphins, seals, and songbirds), vocal learning may be necessary, but not sufficient for beat induction – the cognitive mechanism that supports the perception of a regular pulse from a varying rhythm (Honing et al., 2012).

Today a new study appeared in Nature Scientific Reports claiming to show rhythmic entrainment (or spontaneous synchronization as the authors refer to it) in the Japanese macaque (Macaca Fuscata). Intriguing! However, reading the paper it becomes clear quickly that the results might not be what they seemed at first sight.

[link to video for non-Flash supporting devices]

First, as was shown in several earlier studies, macaques can synchronize to an auditory metronome, but they tend to do this in reaction, and not in anticipation of the sound. They do not show the typical negative synchronization error: tapping or pressing a button slightly earlier than the actual sound, a sign that an anticipatory process (i.e. expectation) plays a role.

Second, it is unclear whether the experiments are evidence for rhythmic entrainment: it could well be imitative behavior. This hypothesis is actually confirmed by the third experiment in which the monkeys were asked to synchronize with a virtual monkey (see panel C above) of which the auditory and visual information was presented independently as well as combined. The monkeys performed better for the visual condition as opposed to the auditory condition. In contrast, in humans it is the opposite: rhythmic entrainment is much stronger in the auditory modality.

Lastly, the researchers only analyzed asynchronies between the button presses of the two monkeys sitting opposite to each other (see Panel B above). Therefore the results could well be simply support for an imitative, cq. reactive behavior instead of evidence for a periodic anticipatory reaction that is common to human rhythmic entrainment. 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

ResearchBlogging.orgHoning, 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


  1. I like the idea of the test seeing how monkeys are so closely related to humans. Was it at Random Selection that the monkeys were chosen, or were they in a controlled enviorment that they had constant exposure to they enviorment that they were to expierence during the test? I feel that this test would be a much more effective test if you took a correlational study route, by taking two groups of primates and tested the results in comparrison to the one group observed.

  2. So if monkeys spontaneously synchronize to audio when they were tested! Would cats and dogs be spontaneously synchronized to audio as well if tested? Even though it’s very rare to test dogs and cats.

  3. Post by Justin London (send by email):

    My take: it's temporal coordination, including some period adaptation, which, as you note, is rapid reaction rather than true anticipation. But it isn't full-blooded entrainment, as the experimenters did not use a phase correction task (inserting random phase perturbations in the metronome or VMonkey, and seeing if it leads to any change in the test monkey's behavior).

    This may show some capacity for temporal awareness, and coordinated pacing that is a pre-requisite to human rhythmic abilities, but it isn't the same thing.

  4. Post by Ed Large (by email):

    While the Nagasaka et al. study does not directly address the questions that have been discussed in the music literature, it seems to have been well conducted, and with an eye toward ecological concerns.

    I have a number of concerns about the parameters of the conversation -- not just here, but in the literature as well.

    First, I think this kind of synchrony has an important multimodal component. While vision vs audition is interesting to ask about for humans, it is a subtle to be worried about with nonhuman primates (and other animals) when we no next to nothing about the rhythmicity of their interactions with one another and with the natural world. One thing we know is that rhythms in the natural world are multi-modal.

    Second, on 'reaction' vs 'anticipation', far too much has been made of this in the literature. From a point of view of phase locking, it tells you something about the nature of the process that's doing the synchronizing, but there is no important qualitative distinction between the two. Add to this the fact that anticipation disappears for complex rhythms, and depends upon expertise, and I don't think that there is any conclusion that can be drawn on this basis about a qualitative difference between synchrony in macaques and humans.

    Third, we have found another bonobo population to work with. In analyzing the results of a first pilot study, we did find evidence for tempo matching in one bonobo (we only tested one), and we reported this result as SfN in October.

    Finally, it is important to keep in mind that the evidence for synchronization in Snowball or any other animal so far is actually pretty weak. Here it is important to recognize (and this is something that took me some time to realize) that circular statistics cannot prove synchronization. It was never meant for that purpose. It can only quantify mean angle and variability. A reassessment of Patel et al's criterion for Snowball
    with this caveat in mind tells me that Snowball came within +/- 10% of the song's tempo for short periods of time. Not as impressive as the result initially seemed. The criteria of Schachner et al is better, but these are YouTube videos, not controlled experiments. I many ways, the Zarco study is
    the strongest so far.

    A major issue for our bonobo (and children, by the way, according to Devin) appears to be tempo. Our bonobo strongly prefers fast tempi (around 5 Hz). I'd be surprised if macaques didn't have a similar bias (as Ghazanfar's data suggests). The difficulty with Zarco's macaque training (and the missing anticipation) may simply be

    Anyway, just a few things to keep in mind …


  5. Nice article, thanks for the information.

  6. Dear Ed and all: You are on to something about the inadequacy of circular statistics for these purposes, but in the Nagasaka et al. case it is even worse than that. Their conspicuously small asynchronies, some better than most humans (one was 1 ms if I recall correctly!) made me scrutinize their methods section carefully, only to discover that they used an illegitimate procedure for calculating asynchronies. One simply cannot do what they state they did, namely to select, for each event in the time series of the slower monkey, “the closest match in time from the other animal’s record as a basis for calculating asynchrony”. That is not even circular statistics, that is pure methodological error guaranteed to generate small asynchronies for a random time series, because some of the matching events will fall before and some after the events chosen from the slower record, and they will average out to zero asynchrony if continued long enough WITH REAL RANDOM NUMBERS. Results obtained in this way are a methodological artifact, and not evidence of anything except that numbers as likely to fall above as below a standard will average out to that standard, and generate zero asynchrony. I was aghast when I saw it, they state plainly what they did, so they are honest, but misguided. See also my recent Phil Trans. paper where I try to call this to people's attention (Doi:10.1098/rstb.2014.0095), in the section on entrainment, p. 5, right-hand column, middle paragraph.
    Best, Bjorn.