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

Düring DN, Ziegler A, Thompson CK, Ziegler A, Faber C, Müller J, Scharff C, Elemans CP - BMC Biol. (2013)

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Verhaltensbiologie, Freie Universität Berlin, Takustrasse 6, 14195 Berlin, Germany.

ABSTRACT

Background: 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.

Results: 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.

Conclusions: 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.

Show MeSH

Related in: MedlinePlus

Ossified structural elements of the male and female zebra finch syrinx. (A) Ventral and (C) dorsal view of male syringeal skeleton surface rendering based on μCT datasets with 5 μm isotropic voxel resolution. (B) Ventral and (D) dorsal view of the female syringeal skeleton. Muscle attachment sites leave impressions on the surface of the tympanum (black arrowheads in A) and on bronchial half-rings B1 and B2 (insets). Abbreviations as listed in Table 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3539882&req=5

Figure 2: Ossified structural elements of the male and female zebra finch syrinx. (A) Ventral and (C) dorsal view of male syringeal skeleton surface rendering based on μCT datasets with 5 μm isotropic voxel resolution. (B) Ventral and (D) dorsal view of the female syringeal skeleton. Muscle attachment sites leave impressions on the surface of the tympanum (black arrowheads in A) and on bronchial half-rings B1 and B2 (insets). Abbreviations as listed in Table 1.

Mentions: We visualized and compared the ossified elements of the male (N = 12) and female (N = 5) zebra finch syrinx μCT datasets. Without staining of soft tissues, only ossified tissue is clearly visible in μCT scans. Figure 2 shows the 2D projections of a male and female 3D syringeal skeleton. Because no apparent asymmetries were observed in the number of bones comprising the syringeal skeleton (N = 17), we consider the structure symmetrical in our description. The zebra finch syringeal skeleton is clearly sexually dimorphic, with the male syrinx being larger and more robust (Figures 2 and 3, and Additional file 1). We observed considerable larger variation in the shape of the ossified elements in the female skeleton compared with the male skeleton (Figure 3). However, we found no differences in number and orientation of ossified elements between sexes (Figure 3). Therefore, we assume the following description to be accurate for both sexes.


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

Düring DN, Ziegler A, Thompson CK, Ziegler A, Faber C, Müller J, Scharff C, Elemans CP - BMC Biol. (2013)

Ossified structural elements of the male and female zebra finch syrinx. (A) Ventral and (C) dorsal view of male syringeal skeleton surface rendering based on μCT datasets with 5 μm isotropic voxel resolution. (B) Ventral and (D) dorsal view of the female syringeal skeleton. Muscle attachment sites leave impressions on the surface of the tympanum (black arrowheads in A) and on bronchial half-rings B1 and B2 (insets). Abbreviations as listed in Table 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3539882&req=5

Figure 2: Ossified structural elements of the male and female zebra finch syrinx. (A) Ventral and (C) dorsal view of male syringeal skeleton surface rendering based on μCT datasets with 5 μm isotropic voxel resolution. (B) Ventral and (D) dorsal view of the female syringeal skeleton. Muscle attachment sites leave impressions on the surface of the tympanum (black arrowheads in A) and on bronchial half-rings B1 and B2 (insets). Abbreviations as listed in Table 1.
Mentions: We visualized and compared the ossified elements of the male (N = 12) and female (N = 5) zebra finch syrinx μCT datasets. Without staining of soft tissues, only ossified tissue is clearly visible in μCT scans. Figure 2 shows the 2D projections of a male and female 3D syringeal skeleton. Because no apparent asymmetries were observed in the number of bones comprising the syringeal skeleton (N = 17), we consider the structure symmetrical in our description. The zebra finch syringeal skeleton is clearly sexually dimorphic, with the male syrinx being larger and more robust (Figures 2 and 3, and Additional file 1). We observed considerable larger variation in the shape of the ossified elements in the female skeleton compared with the male skeleton (Figure 3). However, we found no differences in number and orientation of ossified elements between sexes (Figure 3). Therefore, we assume the following description to be accurate for both sexes.

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Verhaltensbiologie, Freie Universität Berlin, Takustrasse 6, 14195 Berlin, Germany.

ABSTRACT

Background: 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.

Results: 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.

Conclusions: 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.

Show MeSH
Related in: MedlinePlus