Rhesus Monkeys (Macaca mulatta) Sense Isochrony in Rhythm, but Not the Beat: Additional Support for the Gradual Audiomotor Evolution Hypothesis

Abstract

Charles Darwin suggested the perception of rhythm to be common to all animals. While only recently experimental research is finding some support for this claim, there are also aspects of rhythm cognition that appear to be species-specific, such as the capability to perceive a regular pulse (or beat) in a varying rhythm. In the current study, using EEG, we adapted an auditory oddball paradigm that allows for disentangling the contributions of beat perception and isochrony to the temporal predictability of the stimulus. We presented two rhesus monkeys (Macaca mulatta) with a rhythmic sequence in two versions: an isochronous version, that was acoustically accented such that it could induce a duple meter (like a march), and a jittered version using the same acoustically accented sequence but that was presented in a randomly timed fashion, as such disabling beat induction. The results reveal that monkeys are sensitive to the isochrony of the stimulus, but not its metrical structure. The 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 showed no interaction between metrical position and isochrony. So, while the monkey brain appears to be sensitive to the isochrony of the stimulus, we find no evidence in support of beat perception. We discuss these results in the context of the gradual audiomotor evolution (GAE) hypothesis (Merchant and Honing, 2014) that suggests beat-based timing to be omnipresent in humans but only weakly so or absent in non-human primates.

Keywords: ERP; MMN; beat perception; music; rhythm.

Figure 1

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 (Adapted from Mendoza and Merchant, and Merchant and Honing, 2014).

Figure 2

Schematic diagram of the rhythmic stimulus patterns used in the experiment. (A) The two standard (S1 and S2) and two deviant patterns (D1 and D2), made up of three different sounds (A, accented; U, unaccented; and T, attenuated). An accented sound could occur either on the beat or offbeat, an unaccented sound was restricted to the offbeat position. An attenuated sound was used as a deviant in two positions (beat and offbeat) and in two conditions (isochronous and jittered). (B) Standard and deviant sound patterns were concatenated into a single rhythmic stream (their generation is visualized as a transition network in Figure 3). Sequences in the isochronous condition had an inter-onset interval (IOI) of 225 ms, in the jittered condition these were randomly chosen from the range 150–300 ms using a uniform distribution. Deviants were always preceded and followed by an accented sound, with a fixed IOI of 225 ms in both conditions (Adapted from Bouwer et al., 2016).

Figure 3

Rhythmic sequence generation visualized as a transition network. As noted in the text, this representation is a simplification in that it does not include certain constraints on which patterns can follow each other.

Figure 4

Electrode positions marked on the head of a rhesus monkey. (Adapted from Honing et al., 2012).

Figure 5

Event-related potentials at Cz for the isochronous condition. Deviants are marked with solid black lines, standards with dotted black lines. Difference waves (deviant ERPs minus standard ERPs) on the beat are represented with solid blue lines, offbeat with solid red lines, for Monkey A and Monkey B. The gray-shaded areas indicate the time windows used in the statistical analyses of the MMN and P3a. Dotted vertical lines indicate the start of the sound event, dashed vertical lines indicate the onset of the next sound event (at 225 ms). See Table 2 for details on time ranges used.

Figure 6

Event-related potentials at Cz for the jittered condition. Deviants are marked with solid black lines, standards with dotted black lines. Difference waves (deviant ERPs minus standard ERPs) on the beat are represented with solid blue lines, offbeat with solid red lines, for Monkey A and Monkey B. The gray-shaded areas indicate the time windows used in the statistical analyses of the MMN and P3a. Dotted vertical lines indicate the start of the sound event, dashed vertical lines indicate the onset of the next sound event (at 225 ms). See Table 3 for details on time ranges used.

Figure 7

Event-related potentials at Cz for all conditions. Standards in the isochronous condition (Top) and jittered condition (Bottom) for Monkey A and Monkey B. Standards on the beat are marked in blue and standards offbeat are marked in red.

Figure 8

Summary of the results. MMN and P3a in Monkey A (Top) and Monkey B (Middle). For comparison, the (Bottom) shows the mean results for humans (N = 34), unattended condition (see Table 1 in Bouwer et al., 2016). Note that the y-axes are different for the monkey and human data. Error bars represent one standard error of the mean. *Significant interaction.