AUTONOMIC NERVOUS SYSTEM DYNAMICS AND PRIMATE VOCAL PRODUCTION

Abstract

In humans, vocal production is typically cast as a cognitively intensive process, requiring a big brain and complex cognitive mechanisms. Recent studies have demonstrated that the vocal behavior of marmoset monkeys, a diminutive New World primate, is strikingly human-like in its dynamics and development. Considering the evolutionary gap between species, any shared neural mechanisms should be quite old. We propose that the convergent evolution of vocal behavior between marmosets and humans is partly due to neural mechanisms scaffolding upon a pre-existing arousal-regulation mechanism. We directly tested our hypothesis by recording natural changes in the adult marmoset’s arousal state as it spontaneously vocalized. We demonstrate predictable changes in the animal’s arousal state across multiple indices: heart rate, respiration rate, and motor activity. Moreover, the timing of vocal production in adult marmosets is coupled with the phase of a 0.1 Hz autonomic nervous system rhythm, the Mayer wave. The results of this study suggest that arousal dynamics are critical in assembling the timing and prediction of spontaneous primate vocalizations.

We next sought to determine whether the dynamics of the autonomic nervous system can act as a scaffold for the development of behavior. We densely sampled indices of arousal, motor activity, and vocal behavior from seven infant marmosets from birth until two months of age. Consistent with the human literature, changes in motor activity are predictive of vocal development in marmoset monkeys. Further, the developmental trajectory of the autonomic nervous system is itself oscillatory and correlates to changes in both the infant’s vocal development and its motor development. We used statistical methods to extract causality between these processes. Changes in the development of the autonomic nervous system drives both the development of mature motor behavior and mature vocal production. Taken together, this dissertation argues that the autonomic nervous system is critical for the development and expression of spontaneous behavior in primates.