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.

Rhythmic swaying induced by sound in chimpanzees (Pan troglodytes)

“…Primate Origins of Music and Dance. Concerning the evolutionary process of human musicality in primate lineage, the gradual audiomotor (GAE) hypothesis (41,42,54) claims that rhythmic entrainment (or beat-based timing) was gradually developed in primates, peaking in humans but present only with limited properties in other nonhuman primates. Conversely, another hypothesis ("vocal learning and rhythmic synchronization hypothesis") claims that advanced rhythmic ability, such as beat perception and synchronization (BPS), is a by-product of the complex vocal learning mechanisms that are shared by several bird and mammalian species including humans (16).…”

Interaction of music and emotional stimuli in modulating working memory in macaque monkeys

“…Previous studies in nonhuman primates have led to mixed results regarding the ability of nonhuman primates in distinguishing and perceiving different aspects of musicality, namely its pitch, harmony, and rhythmic elements. Monkeys exhibit abilities foundational to music perception such as perceiving acoustic patterns (Honing, Bouwer, Prado, & Merchant, ; Honing, Merchant, Háden, Prado, & Bartolo, ; Selezneva et al, ) as well as rhythmic entrainment (Gámez et al, ; Takeya, Kameda, Patel, & Tanaka, ). In a study with new world monkeys, tamarins and marmosets were allowed to retrieve reward from two different arms of a Y maze, which were associated with two types of music (slow tempo: 65 bpm; fast tempo: 369 bpm).…”

Motor and Predictive Processes in Auditory Beat and Rhythm Perception

“…The result being the formation of an additional beat-based mechanism with enhanced connection of the mCGBT to the auditory cortex via that same dorsal auditory stream in the human brain (Merchant and Honing, 2014). Recent neurophysiological evidence highlights the interconnectedness of interval and beat-based timing mechanisms proposed by GAE, indicating that even in passive listening, monkeys are able to detect isochrony in rhythm, due in part to extant interval-based timing mechanisms of the monkey motor system, but that monkeys cannot detect the underlying beat in a rhythmic stimulus, which requires auditory-motor beat-based timing mechanisms present in humans (Honing et al, 2018).…”

“…In addition to fMRI observation of motor activation in music listening and rhythm processing, the predictive and causal roles of specific motor structures highlighted by the ASAP and GAE hypotheses have been experimentally tested via electroencephalography (EEG) and transcranial magnetic stimulation (TMS). Specific Event Related Potentials (ERPs) relating to prediction errors evoked by rhythmic deviations in musical stimuli include the mismatch negativity (MMN) and P3a (Honing et al, 2018;Koelsch et al, 2019). These auditory event related components indicate violation of temporal expectations in oddball paradigms, with early responses related to bottom-up sensory processing and later responses reflecting top-down cortical processes (Garrido et al, 2007) and (perhaps conscious) attention to deviant stimuli (Sussman et al, 2003).…”