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 

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.