Vocal state change through laryngeal development

Abstract

Across vertebrates, progressive changes in vocal behavior during postnatal development are typically attributed solely to developing neural circuits. How the changing body influences vocal development remains unknown. Here we show that state changes in the contact vocalizations of infant marmoset monkeys, which transition from noisy, low frequency cries to tonal, higher pitched vocalizations in adults, are caused partially by laryngeal development. Combining analyses of natural vocalizations, motorized excised larynx experiments, tensile material tests and high-speed imaging, we show that vocal state transition occurs via a sound source switch from vocal folds to apical vocal membranes, producing louder vocalizations with higher efficiency. We show with an empirically based model of descending motor control how neural circuits could interact with changing laryngeal dynamics, leading to adaptive vocal development. Our results emphasize the importance of embodied approaches to vocal development, where exploiting biomechanical consequences of changing material properties can simplify motor control, reducing the computational load on the developing brain.

Rapid development of mature vocal patterns of ultrasonic calls in a fast-growing rodent, the yellow steppe lemming (Eolagurus luteus)

“…Consistently, in Scotinomys singing mice, the vocal traits of adult songs emerge in pups earlier than they complete their physical growth [49]. Potentially, the transit from infantile to mature vocal patterns in rodent USV calls is due to the developmental changes of the larynx, as was convincingly demonstrated for the audible contact calls of common marmosets Callitrix jaccus [111] and goitred gazelles Gazella subgutturosa [112].…”

High-fidelity continuum modeling predicts avian voiced sound production

“…During postnatal vocal development, gradual body changes, such as lung growth or VF stiffness in marmosets (46,47) or increased muscle speed in songbirds (48), can drive changes in vocal 180 behavior. Embodied human VF models have direct clinical relevance to pathological physical behaviors with abnormal vocal output (1) and patient specific model-assisted phonosurgery (49,50), because most laryngeal human voice disorders are caused by changes in VF geometry, structural integrity, or kinematics (4).…”

Syringeal vocal folds do not have a voice in zebra finch vocal development

“…Especially in species capable of vocal imitation learning, progressive changes in vocal output are attributed to changes in the underlying brain circuitry. However, the maturation of the vocal organ and tract have profound effect on voice during puberty in humans 5 , and can explain transitions from juvenile to adult calls in marmosets 6 . Thus, the postnatal development of the body can drive changes in vocal behavior, and therefore needs to be included when studying vocal development.…”

“…Vocal fold resonance properties in turn are determined by vocal fold length and ultrastructure, such as collagen and elastin fiber composition, the occurrence of tissue layering and layer orientation 24 . During vocal development in humans [25][26][27] , and marmosets 6 , changes in size, (ultra)structure and mechanical properties of the labia have been linked to dramatic changes in vocal output. However, it is unknown whether material properties or morphology of songbird labial change over vocal development and if so whether these changes contribute to the changing vocal output.…”

“…Thus, the MVM properties have matured already at 25 DPH. This latter feature makes the songbird system a wonderful model system to study vocal development compared to mammalian systems where larynx maturation strongly contributes to vocal output6,[25][26][27] .Third, MVM properties remain constant even though they are colliding billions of times over their lifetime and there must be a large variability in use between individuals and sexes. In human vocal folds, strong collisions can lead to several types of lesions that severely affect vocal output 72 .…”