Theta Synchronization of Phonatory and Articulatory Systems in Marmoset Monkey Vocal Production

Abstract

Human speech shares a 3-8-Hz theta rhythm across all languages [1-3]. According to the frame/content theory of speech evolution, this rhythm corresponds to syllabic rates derived from natural mandibular-associated oscillations [4]. The underlying pattern originates from oscillatory movements of articulatory muscles [4, 5] tightly linked to periodic vocal fold vibrations [4, 6, 7]. Such phono-articulatory rhythms have been proposed as one of the crucial preadaptations for human speech evolution [3, 8, 9]. However, the evolutionary link in phono-articulatory rhythmicity between vertebrate vocalization and human speech remains unclear. From the phonatory perspective, theta oscillations might be phylogenetically preserved throughout all vertebrate clades [10-12]. From the articulatory perspective, theta oscillations are present in non-vocal lip smacking [1, 13, 14], teeth chattering [15], vocal lip smacking [16], and clicks and faux-speech [17] in non-human primates, potential evolutionary precursors for speech rhythmicity [1, 13]. Notably, a universal phono-articulatory rhythmicity similar to that in human speech is considered to be absent in non-human primate vocalizations, typically produced with sound modulations lacking concomitant articulatory movements [1, 9, 18]. Here, we challenge this view by investigating the coupling of phonatory and articulatory systems in marmoset vocalizations. Using quantitative measures of acoustic call structure, e.g., amplitude envelope, and call-associated articulatory movements, i.e., inter-lip distance, we show that marmosets display speech-like bi-motor rhythmicity. These oscillations are synchronized and phase locked at theta rhythms. Our findings suggest that oscillatory rhythms underlying speech production evolved early in the primate lineage, identifying marmosets as a suitable animal model to decipher the evolutionary and neural basis of coupled phono-articulatory movements.