Hostname: page-component-745bb68f8f-s22k5 Total loading time: 0 Render date: 2025-02-11T14:54:12.878Z Has data issue: false hasContentIssue false

Differences in auditory timing between human and nonhuman primates

Published online by Cambridge University Press:  17 December 2014

Henkjan Honing
Affiliation:
Amsterdam Brain and Cognition, Institute for Logic, Language and Computation, University of Amsterdam, Amsterdam, The Netherlands. honing@uva.nlhttp://www.mcg.uva.nl/hh/
Hugo Merchant
Affiliation:
Department of Cognitive Neuroscience, Instituto de Neurobiología, Universidad Nacional Autónoma de México, Campus Juriquila, Querétaro, México. hugomerchant@unam.mxhttp://132.248.142.13/personal/merchant/members.html

Abstract

The gradual audiomotor evolution hypothesis is proposed as an alternative interpretation to the auditory timing mechanisms discussed in Ackermann et al.'s article. This hypothesis accommodates the fact that the performance of nonhuman primates is comparable to humans in single-interval tasks (such as interval reproduction, categorization, and interception), but shows differences in multiple-interval tasks (such as entrainment, synchronization, and continuation).

Type
Open Peer Commentary
Copyright
Copyright © Cambridge University Press 2014 

Ackermann et al. propose that the monosynaptic elaboration of the corticobulbar tracts, which played a selective role in the origins of speech, might also have provided the phylogenetic basis for “communicative musicality” (sect. 5.1). The term “musicality” is used here to indicate the cognitive and biological mechanisms that underlie the perception and production of music, as opposed to musical activities that are shaped by culture (Honing & Ploeger Reference Honing and Ploeger2012; Honing et al, in press b). Perceiving a regular pulse – the beat – in music is considered a fundamental component of musicality: It allows humans to dance and make music together. This skill has been referred to as beat perception and synchronization (Patel Reference Patel2008), beat induction (Honing Reference Honing2012), or pulse perception and entrainment (Fitch Reference Fitch2013). Furthermore, it is considered a spontaneously developing (Winkler et al. Reference Winkler, Háden, Ladinig, Sziller and Honing2009), music-specific (Patel Reference Patel2008) and species-specific skill (Fitch Reference Fitch2013).

Interestingly, beat perception and synchronization (BPS) has been observed in humans and a selected group of bird species (Hasegawa et al. Reference Hasegawa, Okanoya, Hasegawa and Seki2011; Patel et al. Reference Patel, Iversen, Bregman and Schulz2009b), but appears to show some but not all the behavioral finger prints in nonhuman primates (Honing et al. Reference Honing, Merchant, Háden, Prado and Bartolo2012; Zarco et al. Reference Zarco, Merchant, Prado and Mendez2009; but see Hattori et al. [2013] for some counter-evidence). This observation is in support of the vocal learning (VL) hypothesis (Patel Reference Patel2008), which suggests that BPS is a by-product of the VL mechanisms that are shared by several bird and mammal species, including humans, but that are only weakly developed, or missing entirely, in nonhuman primates. Nevertheless it has to be noted that, since no evidence of rhythmic entrainment was found in many vocal learners (including dolphins, seals, and songbirds; Schachner et al. Reference Schachner, Brady, Pepperberg and Hauser2009), vocal learning may be necessary, but clearly is not sufficient for BPS. Furthermore, recent evidence for BPS in a non-vocal learner (Cook et al. Reference Cook, Rouse, Wilson and Reichmuth2013) weakens vocal learning as a pre-condition for rhythmic entrainment.

The absence of synchronized movements to sound (or music) in certain species is no evidence for the absence of beat perception. With behavioral methods that rely on overt motoric responses (e.g., Hattori et al. Reference Hattori, Tomonaga and Matsuzawa2013; Patel et al. Reference Patel, Iversen, Bregman and Schulz2009b) it is difficult to distinguish between the contribution of perception and action; more direct, electrophysiological measures such as event-related brain potentials (ERPs) allow testing for neural correlates of beat perception (a pre-condition to rhythmic entrainment). To test this, we measured auditory ERPs in rhesus monkeys (Macaca mulatta) using the mismatch negativity (MMN) component as an index of (the violation of) rhythmic expectation (Honing et al. Reference Honing, Merchant, Háden, Prado and Bartolo2012). Rhythmic expectation was probed by selectively omitting parts of a musical rhythm, randomly inserting gaps at the first position of a musical unit (i.e., the “downbeat”). This oddball paradigm was used previously to probe beat perception in human adults and newborns (Honing et al., in press a; Winkler et al. Reference Winkler, Háden, Ladinig, Sziller and Honing2009). The results confirmed the behavioral studies discussed earlier, in that rhesus monkeys are not able to detect the beat in a complex auditory stimulus, although they can detect the start of a rhythmic group (Honing et al. Reference Honing, Merchant, Háden, Prado and Bartolo2012). In fact, a recent paper showed that macaques exhibit changes of gaze and facial expressions when a deviant of a regular rhythmic sequence is presented, supporting the notion that monkeys are sensitive to the structure of simple rhythms (Selezneva et al. Reference Selezneva, Deike, Knyazeva, Scheich, Brechmann and Brosch2013).

The question remains of whether more close human relatives, such as the great apes, show a more sophisticated ability for rhythmic entrainment than macaques. While the VL hypothesis predicts that no rhythmic entrainment should be found, a recent study (Hattori et al. Reference Hattori, Tomonaga and Matsuzawa2013) showed that at least one chimpanzee (Pan troglodytes), of the three that took part in the experiment, was capable of spontaneously synchronizing her movements with an auditory rhythm. Interestingly, this chimpanzee entrained her tapping behavior to an isochronous 600-msec interval stimuli metronome, but not to other tempos.

Based on these observations, we propose an alternative view: the gradual audiomotor evolution (GAE) hypothesis (Honing et al. Reference Honing, Merchant, Háden, Prado and Bartolo2012; Merchant & Honing Reference Merchant and Honing2014), which directly addresses the similarities and differences that are found between human and nonhuman primates (discussed in section 5.1 of the target article). This hypothesis suggests rhythmic entrainment (or beat-based timing) to be gradually developed in primates, peaking in humans but present only with limited properties in other nonhuman primates; while humans share interval-based timing with all nonhuman primates and related species. Thus, the GAE hypothesis accommodates the fact that the performance of rhesus monkeys is comparable to humans in single-interval tasks (such as interval reproduction, categorization, and interception; Mendez et al. Reference Mendez, Prado, Mendoza and Merchant2011; Merchant et al. Reference Merchant, Battaglia-Mayer and Georgopoulos2003), but differs substantively in multiple-interval tasks (such as rhythmic entrainment, synchronization, and continuation; Zarco et al. Reference Zarco, Merchant, Prado and Mendez2009).

Finally, 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 (Grahn & Brett Reference Grahn and Brett2007; Rao et al. Reference Rao, Harrington, Haaland, Bobholz, Cox and Binder1997; Teki et al. Reference Teki, Grube, Kumar and Griffiths2011; Wiener et al. Reference Wiener, Turkeltaub and Coslett2010), we suggest that the reverberant flow of audiomotor information that loops across the anterior prefrontal 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.

References

Cook, P., Rouse, A., Wilson, M. & Reichmuth, C. (2013) A California sea lion (Zalophus californianus) can keep the beat: Motor entrainment to rhythmic auditory stimuli in a non-vocal mimic. Journal of Comparative Psychology 127(4):412–27. doi: 10.1037/a0032345.Google Scholar
Fitch, W. T. (2013) Rhythmic syntax and rhythmic cognition in humans and animals: A computational and comparative perspective. Frontiers in Systems Neuroscience 7:68. doi: 10.3389/fnsys.2013.00068.Google Scholar
Grahn, J. A. & Brett, M. (2007) Rhythm and beat perception in motor areas of the brain. Journal of Cognitive Neuroscience 19(5):893906. doi: 10.1162/jocn.2007.19.5.893.Google Scholar
Hasegawa, A., Okanoya, K., Hasegawa, T. & Seki, Y. (2011) Rhythmic synchronization tapping to an audio–visual metronome in budgerigars. Scientific Reports 1(Article 120):18. (Online journal). doi:10.1038/srep00120.Google Scholar
Hattori, Y., Tomonaga, M. & Matsuzawa, T. (2013) Spontaneous synchronized tapping to an auditory rhythm in a chimpanzee. Scientific Reports 3(Article 1566):16. (Online journal). doi: 10.1038/srep01566.CrossRefGoogle Scholar
Honing, H. (2012) Without it no music: Beat induction as a fundamental musical trait. Annals of the New York Academy of Sciences 1252(1):8591. doi: 10.1111/j.1749-6632.2011.06402.x.Google Scholar
Honing, H., Bouwer, F. & Háden, G. P. (in press) Perceiving temporal regularity in music: The role of auditory event-related potentials (ERPs) in probing beat perception. In: Neurophysiology of temporal processing, ed. Merchant, H. & de Lafuente, V.. Springer.Google Scholar
Honing, H., Merchant, H., Háden, G. P., Prado, L. & Bartolo, R. (2012) Rhesus monkeys (Macaca mulatta) detect rhythmic groups in music, but not the beat. PLoS ONE 7(12):110. doi: 10.1371/journal.pone.0051369.Google Scholar
Honing, H. & Ploeger, A. (2012) Cognition and the evolution of music: Pitfalls and prospects. Topics in Cognitive Science 4:513–24. doi: 10.1111/j.1756-8765.2012.01210.x.Google Scholar
Honing, H., ten Cate, C., Peretz, I., & Trehub, S. (in press) Without it no music: Cognition, biology, and evolution of musicality. Philosophical Transactions B.Google Scholar
Mendez, J. C., Prado, L., Mendoza, G. & Merchant, H. (2011) Temporal and spatial categorization in human and non-human primates. Frontiers in Integrative Neuroscience 5(50):110. doi: 10.3389/fnint.2011.00050.CrossRefGoogle ScholarPubMed
Merchant, H., Battaglia-Mayer, A. & Georgopoulos, A. P. (2003) Interception of real and apparent circularly moving targets: Psychophysics in human subjects and monkeys. Experimental Brain Research 152:106–12.CrossRefGoogle Scholar
Merchant, H. & Honing, H. (2014) Are non-human primates capable of rhythmic entrainment? Evidence for the gradual audiomotor evolution hypothesis. Frontiers in Auditory Cognitive Neuroscience 7:274 doi: 10.3389/fnins.2013.00274.Google ScholarPubMed
Patel, A. D. (2008) Music, language, and the brain. Oxford University Press.Google Scholar
Patel, A. D., Iversen, J. R., Bregman, M. R. & Schulz, I. (2009b) Studying synchronization to a musical beat in nonhuman animals. Annals of the New York Academy of Sciences 1169:459–69. doi: 10.1111/j.1749-6632.2009.04581.x.CrossRefGoogle ScholarPubMed
Rao, S. M., Harrington, D. L., Haaland, K. Y., Bobholz, J. A., Cox, R. W. & Binder, J. R. (1997) Distributed neural systems underlying the timing of movements. Journal of Neuroscience 17:5528–35.Google ScholarPubMed
Schachner, A., Brady, T. F., Pepperberg, I. M. & Hauser, M. D. (2009) Spontaneous motor entrainment to music in multiple vocal mimicking species. Current Biology 19(10):831–36. doi: 10.1016/j.cub.2009.03.061.Google Scholar
Selezneva, E., Deike, S., Knyazeva, S., Scheich, H., Brechmann, A. & Brosch, M. (2013) Rhythm sensitivity in macaque monkeys. Frontiers in Systems Neuroscience 7:49. doi: 10.3389/fnsys.2013.00049.CrossRefGoogle ScholarPubMed
Teki, S., Grube, M., Kumar, S. & Griffiths, T. D. (2011) Distinct neural substrates of duration-based and beat-based auditory timing. The Journal of Neuroscience 31(10):3805–12. doi: 10.1523/jneurosci.5561-10.2011.Google Scholar
Wiener, M., Turkeltaub, P. & Coslett, H. H. (2010) The image of time: A voxel-wise meta-analysis. NeuroImage 49:1728–40.Google Scholar
Winkler, I., Háden, G. P., Ladinig, O., Sziller, I. & Honing, H. (2009) Newborn infants detect the beat in music. Proceedings of the National Academy of Sciences USA 106(7):2468–71. doi: 10.1073/pnas.0809035106.Google Scholar
Zarco, W., Merchant, H., Prado, L. & Mendez, J. C. (2009) Subsecond timing in primates: Comparison of interval production between human subjects and rhesus monkeys. Journal of Neurophysiology 102(6):3191–202. doi: 10.1152/jn.00066.2009.Google Scholar