Vocal learning as a preadaptation for the evolution of human beat perception and synchronization

Abstract

The human capacity to synchronize movements to an auditory beat is central to musical behaviour and to debates over the evolution of human musicality. Have humans evolved any neural specializations for music processing, or does music rely entirely on brain circuits that evolved for other reasons? The vocal learning and rhythmic synchronization hypothesis proposes that our ability to move in time with an auditory beat in a precise, predictive and tempo-flexible manner originated in the neural circuitry for complex vocal learning. In the 15 years, since the hypothesis was proposed a variety of studies have supported it. However, one study has provided a significant challenge to the hypothesis. Furthermore, it is increasingly clear that vocal learning is not a binary trait animals have or lack, but varies more continuously across species. In the light of these developments and of recent progress in the neurobiology of beat processing and of vocal learning, the current paper revises the vocal learning hypothesis. It argues that an advanced form of vocal learning acts as a preadaptation for sporadic beat perception and synchronization (BPS), providing intrinsic rewards for predicting the temporal structure of complex acoustic sequences. It further proposes that in humans, mechanisms of gene-culture coevolution transformed this preadaptation into a genuine neural adaptation for sustained BPS. The larger significance of this proposal is that it outlines a hypothesis of cognitive gene-culture coevolution which makes testable predictions for neuroscience, cross-species studies and genetics. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

Keywords: beat; evolution; gene-culture coevolution; rhythm; synchrony; vocal learning.

Figure 1.

The vocal learning continuum hypothesis, from Petkov & Jarvis [57], updated by Jarvis [60]. Diagram of hypothesized stepwise continuous ability of vocal learning among vertebrates (right y-axis), from simple to more complex forms (x-axis). As vocal learning complexity increases, there are a decreasing number of species with the ability (left y-axis). (A–H) Proposed example species at each step on the continuum. The continuum ranges from lizards that do not vocalize and have no vocal learning, to nonhuman primates with limited vocal learning, to songbirds with complex vocal learning, to parrots and humans with high vocal learning. (Figure and caption modified from [60] with permission from the author.) (Online version in colour.)

Figure 2.

Schematic of the vocal system in a parrot brain, adapted from Chakraborty & Jarvis [116] with permission from the authors and The Royal Society. Red regions, core song system (similar to songbirds); yellow regions in pallium/cortex, shell song system (unique to parrots). The shell system is proposed to have evolved out of a partial duplication of the core song system. Black solid arrows, posterior vocal motor pathway; white solid arrows, anterior vocal motor pathway; dashed arrows, connections between core and shell systems. Not all connections are shown for simplicity. See caption of the original figure in [116] for definitions of acronyms. (Online version in colour.)

Figure 3.

(a,b) Dual stream model of spoken language processing, adapted from Hickok & Poeppel [119]. Colours in the functional modules of (a) are matched to brain regions in (b), which shows neural pathways with dashed lines. Acronyms in (b): PMC, premotor cortex; IFG, inferior frontal gyrus; SPT, sylvian parieto-temporal area; AC, auditory cortex; STS, superior temporal sulcus; MTG, middle temporal gyrus; ITG, inferior temporal gyrus AT, anterior temporal cortex. (c) A more detailed view of dorsal stream pathways involved in spoken language (from [50], adapted from [122]). Of particular interest for BPS are connections shown in orange and blue: orange connections link secondary auditory regions in the posterior superior temporal gyrus/middle temporal gyrus (pSTG/MTG) and parietal regions near the angular gyrus (AG), and blue connections link regions near the angular gyrus to the dorsal premotor cortex (dPMC). These connections correspond to two branches of the superior longitudinal fasciculus (SLF): the temporo-parietal branch (SLF-tp) and the second branch (SLF II). Both tracts appear to play a role in sound-to-articulation mapping, which is part of vocal learning, and have been proposed to support auditory–motor interactions serving beat perception [38]. Other acronyms in (c): PTL, posterior temporal lobe; SMG, supramarginal gyrus; vPMC, ventral premotor cortex; 44, Brodmann area 44 (part of Broca's area). (Online version in colour.)

Figure 4.

An optimized hierarchical artificial neural network for recognition of sounds as speech or music, after Kell et al. [172]. Auditory input is shown at the left (spectrogram-like representation of sound). Lower level processing stages shared by speech and music are shown in black and white, higher level stages and streams unique to each domain are shown in colour. (Online version in colour.)