Singing and moving to the rhythm: song-entangled gestures in a vocal learning songbird

Abstract

When humans speak, we use rhythmic hand and head gestures that are closely coordinated with the temporal structure of speech to emphasize words and phrases. Similarly, human singing is often accompanied by rhythmic body movements that are aligned with the timing and prosodic structure of the vocal sequence. This rhythmic synchronization of bodily gesture with vocal production is thought to be a shared feature of vocal-learning species. How do these two sensorimotor systems develop, coordinate, and synchronize with precise timing to support multimodal communication? The mechanisms underlying this rhythmic entrainment remain poorly understood, and no established animal model to date captures the human combination of speech and co-speech gesture. Here, we show that a vocal-learning songbird, the zebra finch, has evolved song-entrained head gestures. These co-song gestures rhythmically align with acoustically complex song syllables and are developed and produced independently of other innate, stereotyped, song-entangled courtship displays. Even when the song remains largely the same, co-song gestures can be dynamically modulated in rhythm, form, and/or extent across different social contexts. The rhythmic alignment requires auditory feedback, is under the control of a premotor song nucleus, and gradually develops during the sensitive period of vocal learning. Females respond differently when songs and co-song gestures are misaligned, suggesting a social function. This dynamic modulation of co-song gestures provides a behavioral window into brain and cognitive states, making the zebra finch a promising model for understanding the mechanisms underlying rhythmic synchronization of multi-sensorimotor systems and the origin and evolution of co-speech gestures in humans.