THE ORGANIZATION OF ACTION IN THE FETUS: Prenatal development of orofacial movements in marmoset monkeys

Abstract

In primates, a number of vocal behaviors are present at birth. These behaviors are often dubbed as ‘innate’ but how they develop remains mysterious. As opposed to simply appearing de novo at birth, we hypothesize that vocalizations begin to self-organize prenatally through the interactions between spontaneous neural activity, fetal biomechanics and the physical constraints of the uterine environment. We investigated how fetal movements relate to the postnatal mouth movements required for vocal production by performing ultrasound imaging on awake, pregnant marmoset monkeys (Callithrix jacchus). Our expectations were two-fold (1) body parts linked to different behaviors become increasingly differentiated; and (2) body parts used for the same behavior become increasingly coordinated. We found that orofacial and head movements occur together early in gestation but gradually decouple and move independently by the end of gestation. Critically, we also observed that signature features of marmoset infant calls emerge prenatally as distinct patterns of orofacial movements: Late in gestation, the duration and syllable number of the phee call and twitter call — calls produced by marmoset monkeys on the first postnatal day — are evident in the orofacial movements of fetal marmosets. Our study shows that aspects of vocal behaviors in marmosets have a period of prenatal development.