In situ vocal fold properties and pitch prediction by dynamic actuation of the songbird syrinx

Abstract

The biomechanics of sound production forms an integral part of the neuromechanical control loop of avian vocal motor control. However, we critically lack quantification of basic biomechanical parameters describing the vocal organ, the syrinx, such as material properties of syringeal elements, forces and torques exerted on, and motion of the syringeal skeleton during song. Here, we present a novel marker-based 3D stereoscopic imaging technique to reconstruct 3D motion of servo-controlled actuation of syringeal muscle insertions sites in vitro and focus on two muscles controlling sound pitch. We furthermore combine kinematic analysis with force measurements to quantify elastic properties of sound producing medial labia (ML). The elastic modulus of the zebra finch ML is 18 kPa at 5% strain, which is comparable to elastic moduli of mammalian vocal folds. Additionally ML lengthening due to musculus syringealis ventralis (VS) shortening is intrinsically constraint at maximally 12% strain. Using these values we predict sound pitch to range from 350–800 Hz by VS modulation, corresponding well to previous observations. The presented methodology allows for quantification of syringeal skeleton motion and forces, acoustic effects of muscle recruitment, and calibration of computational birdsong models, enabling experimental access to the entire neuromechanical control loop of vocal motor control.

Vocal tract anatomy of king penguins: morphological traits of two-voiced sound production

“…In general, the membranes' fundamental frequency is determined by the elastic properties, size and tension of the membranes [20,57]. Düring et al [18] showed that increasing the length of the medial labia in various directions through muscle activation results in higher fundamental frequencies. Given the absence of intrinsic syringeal musculature, the extent between the two voices (F0 1 -F0 2 ) in the king penguins' call could be determined through the different sizes of the vibratory tissues on each side of the syrinx.…”

“…The exact role of the extrinsic ST and TL muscle remains unclear, however, it seems possible that the activation of the TL leads to passive stretching of the vibratory tissues and thus also influences the twovoice frequencies [60]. Future ex vivo studies [9] or biomechanical models based on tissue properties [18,61] would be necessary, to reveal the precise mechanism and control possibilities of the two voices of king penguins. Another important aspect to consider is the vibration frequencies as a result of source-filter interaction, where non-vibratory structures in the vocal tract interact with the vibratory tissues leading to spectrally complex sounds [62].…”

“…In addition to musculature, cartilaginous structures and ossified syringeal elements can play an important role in the biomechanics of sound production, e.g. by impacting the position of the vibrating tissues [4,17,18].…”

Morphological facilitators for vocal learning explored through the syrinx anatomy of a basal hummingbird

“…Thus, the presence of intrinsic musculature has been hypothesized as a prerequisite and not 60 an adaptation for vocal learning (Gaunt, 1983;Mindlin and Laje, 2006), that is, all vocal 61 learners should have intrinsic muscles, but not all species that have intrinsic muscles are 62 vocal learners. Unlike extrinsic muscles, which move the syrinx as a unit (Gaunt, 1983; 63 Mindlin and Laje, 2006), intrinsic muscles dissociate the control of tension from the control 64 of amplitude, for example, which in turn affects pitch (Düring et al, 2017;Goller and Riede, 65 2013). 66…”

“…Recent studies indicate that musculature is just one of the variables that define the 67 multi-dimensional parameter space that translates motor commands into vocal output 68 (Amador and Mindlin, 2008;Düring et al, 2017;Düring and Elemans, 2016;Elemans et al, 69 2015). Many factors, such as syrinx's morphology, physical interaction with the surrounding 70 environment, and neuro-mechanic activity, contribute to the creation of a large acoustic space 71 that is highly redundant (Elemans et al, 2015).…”