Aerodynamics and motor control of ultrasonic vocalizations for social communication in mice and rats

Abstract

Background Rodent ultrasonic vocalizations (USVs) are crucial to their social communication and a widely used translational tool for linking gene mutations to behavior. To maximize the causal interpretation of experimental treatments, we need to understand how neural control affects USV production. However, both the aerodynamics of USV production and its neural control remain poorly understood. Results Here, we test three intralaryngeal whistle mechanisms—the wall and alar edge impingement, and shallow cavity tone—by combining in vitro larynx physiology and individual-based 3D airway reconstructions with fluid dynamics simulations. Our results show that in the mouse and rat larynx, USVs are produced by a glottal jet impinging on the thyroid inner wall. Furthermore, we implemented an empirically based motor control model that predicts motor gesture trajectories of USV call types. Conclusions Our results identify wall impingement as the aerodynamic mechanism of USV production in rats and mice. Furthermore, our empirically based motor control model shows that both neural and anatomical components contribute to USV production, which suggests that changes in strain specific USVs or USV changes in disease models can result from both altered motor programs and laryngeal geometry. Our work provides a quantitative neuromechanical framework to evaluate the contributions of brain and body in shaping USVs and a first step in linking descending motor control to USV production.

Bats expand their vocal range by recruiting different laryngeal structures for echolocation and social communication

“…We next mounted these larynges in an excised larynx setup ( Fig 2A , see Materials and methods ) [ 19 , 26 – 28 ]. After approximation of the ventricular folds with micromanipulators, increasing the bronchial pressure induced self-sustained vibration of the ventricular folds ( Fig 2B and 2C and S1 Movie ) in 3 out of 3 individuals.…”

“…The role of the peculiar ventricular apical membranes remains unclear. The ventricular and vocal membranes form a drumhead with a narrow slit over the ventricle of Morgagni [ 15 ], this configuration opens to the hypothesis that the ventricle of Morgagni acts as a cavity that generated a shallow cavity whistle [ 26 ] for echolocation calls. However, our data clearly shows that removing the ventricular folds and membranes—and thereby the ventricle—results in high-frequency sounds by vocal membrane oscillation.…”

Rates but not acoustic features of ultrasonic vocalizations are related to non-vocal behaviors in mouse pups

“…S5). Ultimately, the acoustic features of a given USV depend on respiratory rate, subglottal pressure and air flow, laryngeal muscle activation, and vocal tract configuration (Håkansson et al, 2022; Riede, 2011, 2013, 2018). Thus, our findings suggest patterns of activity in the premotor and motor neurons that control the vocal actuators are not highly constrained by pup non-vocal behavior.…”

Convergent and divergent neural circuit architectures that support acoustic communication

“…In most tetrapods, sounds are powered by expiration of air from the lungs driving vibrations of the vocal folds (Ghazanfar and Rendall, 2008 ; Fitch and Suthers, 2016 ) or—in birds—of the internal tympaniform membranes (Elemans, 2014 ). In mice, for example, ultrasonic vocalizations are produced by high velocity air jets that power vocal fold vibrations (Håkansson et al, 2022 ). CNS respiratory and vocal circuitry must thus be closely linked.…”