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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.

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Location of song system components in the male zebra finch. (A) μCT-based volume rendering of the zebra finch skeleton. Boxed section shown enlarged in C. (B) Virtual sagittal section through a 3D high-field MRI dataset of the male zebra finch head. Visible are three nuclei of the song system: HVC (used as a proper name) and the robust nucleus of the arcopallium (RA) that both belong to the descending motor pathway, and the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN), which belongs to the anterior forebrain pathway. Dotted lines indicate the virtual sections shown in E and F. (C) Virtual sagittal section through a 3D MRI dataset showing that the syrinx is located at the bifurcation of the trachea into the bilateral primary bronchi, close to the heart (red shaded outline) and lungs (green shaded outline). Note the dark seeds in the crop. The asterisks indicate intercostal muscles. (D) μCT-based volume rendering showing the hyoid bone (yellow) and larynx (blue), which are upper vocal tract modulators important in the filtering of sound properties [38,40]. (E,F) Virtual transversal sections through a 3D MRI dataset of the head as indicated in (B) showing the tongue, larynx, trachea (blue) and hyoid (yellow dotted line). Scale bars: 10 mm.
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Figure 1: Location of song system components in the male zebra finch. (A) μCT-based volume rendering of the zebra finch skeleton. Boxed section shown enlarged in C. (B) Virtual sagittal section through a 3D high-field MRI dataset of the male zebra finch head. Visible are three nuclei of the song system: HVC (used as a proper name) and the robust nucleus of the arcopallium (RA) that both belong to the descending motor pathway, and the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN), which belongs to the anterior forebrain pathway. Dotted lines indicate the virtual sections shown in E and F. (C) Virtual sagittal section through a 3D MRI dataset showing that the syrinx is located at the bifurcation of the trachea into the bilateral primary bronchi, close to the heart (red shaded outline) and lungs (green shaded outline). Note the dark seeds in the crop. The asterisks indicate intercostal muscles. (D) μCT-based volume rendering showing the hyoid bone (yellow) and larynx (blue), which are upper vocal tract modulators important in the filtering of sound properties [38,40]. (E,F) Virtual transversal sections through a 3D MRI dataset of the head as indicated in (B) showing the tongue, larynx, trachea (blue) and hyoid (yellow dotted line). Scale bars: 10 mm.

Mentions: The brain nuclei that comprise the song system in the zebra finch (Figure 1A,B) contain motoneurons that connect with three major muscle systems: the respiratory system, including air sacs, modulated by intercostal and abdominal muscles; the syringeal musculature; and the suprasyringeal vocal tract, including trachea, larynx, oropharyngeal space and beak, modulated mainly by laryngeal, hyoid and orofacial muscles (Figure 1C-F). The zebra finch syrinx is located at the bifurcation of the trachea into the two primary bronchi, just anterior to the lungs and heart (Figure 1C). We constructed a 3D dataset of the syrinx with a 5-μm isotropic voxel resolution based on high-resolution μCT scans. We created a morphome of the syrinx by annotating structures in this dataset based on the μCT scans with complementary guidance by high-field MRI, conventional histology and micro-dissection (see Methods). We will present this dataset starting with the ossified skeleton of the syrinx, subsequently adding on the other tissues, such as cartilage, sound-producing labia and finally muscles. We will then summarize our results, focusing on the motor actuation of syringeal elements and syringeal stability in situ. Table 1 provides an overview of the nomenclature and abbreviations used in text and figures. We include two interactive 3D models (Additional files 1 and 2) for which we have included several predefined views that correspond to our two-dimensional (2D) figures below.


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)

Location of song system components in the male zebra finch. (A) μCT-based volume rendering of the zebra finch skeleton. Boxed section shown enlarged in C. (B) Virtual sagittal section through a 3D high-field MRI dataset of the male zebra finch head. Visible are three nuclei of the song system: HVC (used as a proper name) and the robust nucleus of the arcopallium (RA) that both belong to the descending motor pathway, and the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN), which belongs to the anterior forebrain pathway. Dotted lines indicate the virtual sections shown in E and F. (C) Virtual sagittal section through a 3D MRI dataset showing that the syrinx is located at the bifurcation of the trachea into the bilateral primary bronchi, close to the heart (red shaded outline) and lungs (green shaded outline). Note the dark seeds in the crop. The asterisks indicate intercostal muscles. (D) μCT-based volume rendering showing the hyoid bone (yellow) and larynx (blue), which are upper vocal tract modulators important in the filtering of sound properties [38,40]. (E,F) Virtual transversal sections through a 3D MRI dataset of the head as indicated in (B) showing the tongue, larynx, trachea (blue) and hyoid (yellow dotted line). Scale bars: 10 mm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Location of song system components in the male zebra finch. (A) μCT-based volume rendering of the zebra finch skeleton. Boxed section shown enlarged in C. (B) Virtual sagittal section through a 3D high-field MRI dataset of the male zebra finch head. Visible are three nuclei of the song system: HVC (used as a proper name) and the robust nucleus of the arcopallium (RA) that both belong to the descending motor pathway, and the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN), which belongs to the anterior forebrain pathway. Dotted lines indicate the virtual sections shown in E and F. (C) Virtual sagittal section through a 3D MRI dataset showing that the syrinx is located at the bifurcation of the trachea into the bilateral primary bronchi, close to the heart (red shaded outline) and lungs (green shaded outline). Note the dark seeds in the crop. The asterisks indicate intercostal muscles. (D) μCT-based volume rendering showing the hyoid bone (yellow) and larynx (blue), which are upper vocal tract modulators important in the filtering of sound properties [38,40]. (E,F) Virtual transversal sections through a 3D MRI dataset of the head as indicated in (B) showing the tongue, larynx, trachea (blue) and hyoid (yellow dotted line). Scale bars: 10 mm.
Mentions: The brain nuclei that comprise the song system in the zebra finch (Figure 1A,B) contain motoneurons that connect with three major muscle systems: the respiratory system, including air sacs, modulated by intercostal and abdominal muscles; the syringeal musculature; and the suprasyringeal vocal tract, including trachea, larynx, oropharyngeal space and beak, modulated mainly by laryngeal, hyoid and orofacial muscles (Figure 1C-F). The zebra finch syrinx is located at the bifurcation of the trachea into the two primary bronchi, just anterior to the lungs and heart (Figure 1C). We constructed a 3D dataset of the syrinx with a 5-μm isotropic voxel resolution based on high-resolution μCT scans. We created a morphome of the syrinx by annotating structures in this dataset based on the μCT scans with complementary guidance by high-field MRI, conventional histology and micro-dissection (see Methods). We will present this dataset starting with the ossified skeleton of the syrinx, subsequently adding on the other tissues, such as cartilage, sound-producing labia and finally muscles. We will then summarize our results, focusing on the motor actuation of syringeal elements and syringeal stability in situ. Table 1 provides an overview of the nomenclature and abbreviations used in text and figures. We include two interactive 3D models (Additional files 1 and 2) for which we have included several predefined views that correspond to our two-dimensional (2D) figures below.

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