Like human infants, songbirds learn their species-specific vocalizations through imitation learning. The birdsong system has emerged as a widely used experimental animal model for understanding the underlying neural mechanisms responsible for vocal production learning. However, how neural impulses are translated into the precise motor behavior of the complex vocal organ (syrinx) to create song is poorly understood. First and foremost, we lack a detailed understanding of syringeal morphology. To fill this gap we combined non-invasive (high-field magnetic resonance imaging and micro-computed tomography) and invasive techniques (histology and micro-dissection) to construct the annotated high-resolution three-dimensional dataset, or morphome, of the zebra finch (Taeniopygia guttata) syrinx. We identified and annotated syringeal cartilage, bone and musculature in situ in unprecedented detail. We provide interactive three-dimensional models that greatly improve the communication of complex morphological data and our understanding of syringeal function in general. Our results show that the syringeal skeleton is optimized for low weight driven by physiological constraints on song production. The present refinement of muscle organization and identity elucidates how apposed muscles actuate different syringeal elements. Our dataset allows for more precise predictions about muscle co-activation and synergies and has important implications for muscle activity and stimulation experiments. We also demonstrate how the syrinx can be stabilized during song to reduce mechanical noise and, as such, enhance repetitive execution of stereotypic motor patterns. In addition, we identify a cartilaginous structure suited to play a crucial role in the uncoupling of sound frequency and amplitude control, which permits a novel explanation of the evolutionary success of songbirds.

The songbird syrinx morphome: a three-dimensional, high-resolution, interactive morphological map of the zebra finch vocal organ

As animals vocalize, their vocal organ transforms motor commands into vocalizations for social communication. In birds, the physical mechanisms by which vocalizations are produced and controlled remain unresolved because of the extreme difficulty in obtaining in vivo measurements. Here, we introduce an ex vivo preparation of the avian vocal organ that allows simultaneous high-speed imaging, muscle stimulation and kinematic and acoustic analyses to reveal the mechanisms of vocal production in birds across a wide range of taxa. Remarkably, we show that all species tested employ the myoelastic-aerodynamic (MEAD) mechanism, the same mechanism used to produce human speech. Furthermore, we show substantial redundancy in the control of key vocal parameters ex vivo, suggesting that in vivo vocalizations may also not be specified by unique motor commands. We propose that such motor redundancy can aid vocal learning and is common to MEAD sound production across birds and mammals, including humans.

/pdf/universal-mechanisms-of-sound-production-and-control-in-3rpt54es9n.pdf

Universal mechanisms of sound production and control in birds and mammals

One major feature of the remarkable vocal repertoires of birds is the range of fundamental frequencies across species, but also within individual species. This review discusses four variables that determine the oscillation frequency of the vibrating structures within a bird’s syrinx. These are (1) viscoelastic properties of the oscillating tissue, (2) air sac pressure, (3) neuromuscular control of movements and (4) source-filter interactions. Our current understanding of morphology, biomechanics and neural control suggests that a complex interplay of these parameters can lead to multiple combinations for generating a particular fundamental frequency. An increase in the complexity of syringeal morphology from non-passeriform birds to oscines also led to a different interplay for regulating oscillation frequency by enabling control of tension that is partially independent of regulation of airflow. In addition to reviewing the available data for all different contributing variables, we point out open questions and possible approaches.

Integrative physiology of fundamental frequency control in birds.

Acoustic properties of vocalizations arise through the interplay of neural control with the morphology and biomechanics of the sound generating organ, but in songbirds it is assumed that the main driver of acoustic diversity is variation in telencephalic motor control. Here we show, however, that variation in the composition of the vibrating tissues, the labia, underlies diversity in one acoustic parameter, fundamental frequency (F0) range. Lateral asymmetry and arrangement of fibrous proteins in the labia into distinct layers is correlated with expanded F0 range of species. The composition of the vibrating tissues thus represents an important morphological foundation for the generation of a broad F0 range, indicating that morphological specialization lays the foundation for the evolution of complex acoustic repertoires.

https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2013.2306

Morphological basis for the evolution of acoustic diversity in oscine songbirds

The performance of courtship signals provides information about the behavioural state and quality of the signaller, and females can use such information for social decision-making (eg mate choice) However, relatively little is known about the degree to which the perception of and preference for differences in motor performance are shaped by developmental experiences Furthermore, the neural substrates that development could act upon to influence the processing of performance features remains largely unknown In songbirds, females use song to identify males and select mates Moreover, female songbirds are often sensitive to variation in male song performance Consequently, we investigated how developmental exposure to adult male song affected behavioural and neural responses to song in a small, gregarious songbird, the zebra finch Zebra finch males modulate their song performance when courting females, and previous work has shown that females prefer the high-performance, female-directed courtship song However, unlike females allowed to hear and interact with an adult male during development, females reared without developmental song exposure did not demonstrate behavioural preferences for high-performance courtship songs Additionally, auditory responses to courtship and non-courtship song were altered in adult females raised without developmental song exposure These data highlight the critical role of developmental auditory experience in shaping the perception and processing of song performance

https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2017.0054

Courtship song preferences in female zebra finches are shaped by developmental auditory experience

Background Singing in songbirds is a complex, learned behavior which shares many parallels with human speech. The avian vocal organ (syrinx) has two potential sound sources, and each sound generator is under unilateral, ipsilateral neural control. Different songbird species vary in their use of bilateral or unilateral phonation (lateralized sound production) and rapid switching between left and right sound generation (interhemispheric switching of motor control). Bengalese finches (Lonchura striata domestica) have received considerable attention, because they rapidly modify their song in response to manipulations of auditory feedback. However, how the left and right sides of the syrinx contribute to acoustic control of song has not been studied. Methodology Three manipulations of lateralized syringeal control of sound production were conducted. First, unilateral syringeal muscular control was eliminated by resection of the left or right tracheosyringeal portion of the hypoglossal nerve, which provides neuromuscular innervation of the syrinx. Spectral and temporal features of song were compared before and after lateralized nerve injury. In a second experiment, either the left or right sound source was devoiced to confirm the role of each sound generator in the control of acoustic phonology. Third, air pressure was recorded before and after unilateral denervation to enable quantification of acoustic change within individual syllables following lateralized nerve resection. Significance These experiments demonstrate that the left sound source produces louder, higher frequency, lower entropy sounds, and the right sound generator produces lower amplitude, lower frequency, higher entropy sounds. The bilateral division of labor is complex and the frequency specialization is the opposite pattern observed in most songbirds. Further, there is evidence for rapid interhemispheric switching during song production. Lateralized control of song production in Bengalese finches may enhance acoustic complexity of song and facilitate the rapid modification of sound production following manipulations of auditory feedback.

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Kristen R. Secora

Papers

Syringeal Specialization of Frequency Control during Song Production in the Bengalese Finch (Lonchura striata domestica)