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’.

Linking the genomic signatures of human beat synchronization and learned song in birds

“…In the light of this framework, our results provide, to our knowledge, the first molecular support of the prediction about shared genetic architecture generated from the revised vocal learning and rhythmic synchronization hypothesis [26]. As pointed out by Patel, although it is not yet known if zebra finches possess the totality of auditory, motor and social components (e.g.…”

“…We then further explored potential evolutionary precursors of beat synchronization, by identifying a subset of top-associated human beat genes that were also common across the three significant birdsong sets, and then imputing gene expression ( per [45]) in the cortex and basal ganglia tissues. Taken together, these findings provide novel molecular genetic support for specific predictions of evolutionary hypotheses linking vocal learning to beat perception and synchronization [1,12,26,30,55].…”

“…Even in the absence of beat synchrony behaviours, some avian vocal learners still exceptionally possess some of the foundational features of beat processing, including aspects of motor circuitry specialized for predicting the timing of events, and even more specifically, temporal prediction of auditory periodicities. These observations form the basis of Patel's revised vocal learning and rhythmic synchronization hypothesis, which posits that these sophisticated temporal sensitivities and motor circuitry in vocal learning birds constitute an evolutionary pre-adaptation of human beat synchronization [26].…”

“…In particular, they are an interesting avenue for comparative genetics of rhythm because: (i) they have a developed vocal communication system with rhythmic characteristics and hierarchically structured features with parallels to human communication traits, (ii) their brains and genomes have been thoroughly studied, and (iii) songbird vocal learning is a promising model of the genetic architecture of human communication, hence offering the promise of analogous or even deep homologous features to human rhythm [19][20][21][22][23][24]. The specialized auditory-motor circuitry underlying complex vocal learning in songbirds shares notable neural processes with beat synchronization [26], even when typically human levels of synchronization are not directly observed. These shared resources open the possibility of the similar genetic architecture underlying such neural processes across these two related traits and species.…”

Synchrony and rhythm interaction: from the brain to behavioural ecology

“…Here, comparison with human language-another universal capacity in which rhythm and rhythm interaction play critical roles-can be helpful. Both capacities integrate innate and cultural factors, the latter leading to expression in myriad ways [7]. Musical and language expression also require exposure and practice during development, but, unlike language, musical practice is very uneven among individuals, which probably generates extreme intra-population variation in musical ability.…”