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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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Syringeal muscles of a freshly dissected male zebra finch syrinx. (A) Ventral view of the caudal part of the syrinx showing the ventral muscles VS and VTB, and the IBL. The IBL connects the primary bronchi and restricts their lateral movement. Dashed box is shown enlarged in B. (B) Detail of VTB attachment on bronchial half-ring B3. Syringeal muscles are organized in sheets of muscle fibers (arrowheads). (C) Close-up of the rostral attachment sites of the ventral muscles. The VS fibers end on the edge of the tympanum, while the SVTB fibers do not attach onto bone but end in the connective tissue of the CASM. Rostral to the CASM, the extrinsic TL attaches and runs along the trachea up to the larynx. (D) Lateral view of the right hemisyrinx showing the muscle attaching on B3. Some fibers of the STB attach directly on the ML that is located on the inside of B3. (E) Dorsal muscle attachment sites. (F) Lateral view of rostral attachment sites of SVTB and DTB clearly reveals the organization of syringeal muscles in sheets (arrowheads). Individual muscle fibers can be seen within the fiber bundle sheets. The edge of the CASM is indicated by the dashed black line. Abbreviations as listed in Table 1.
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Figure 9: Syringeal muscles of a freshly dissected male zebra finch syrinx. (A) Ventral view of the caudal part of the syrinx showing the ventral muscles VS and VTB, and the IBL. The IBL connects the primary bronchi and restricts their lateral movement. Dashed box is shown enlarged in B. (B) Detail of VTB attachment on bronchial half-ring B3. Syringeal muscles are organized in sheets of muscle fibers (arrowheads). (C) Close-up of the rostral attachment sites of the ventral muscles. The VS fibers end on the edge of the tympanum, while the SVTB fibers do not attach onto bone but end in the connective tissue of the CASM. Rostral to the CASM, the extrinsic TL attaches and runs along the trachea up to the larynx. (D) Lateral view of the right hemisyrinx showing the muscle attaching on B3. Some fibers of the STB attach directly on the ML that is located on the inside of B3. (E) Dorsal muscle attachment sites. (F) Lateral view of rostral attachment sites of SVTB and DTB clearly reveals the organization of syringeal muscles in sheets (arrowheads). Individual muscle fibers can be seen within the fiber bundle sheets. The edge of the CASM is indicated by the dashed black line. Abbreviations as listed in Table 1.

Mentions: We identified two muscles on the ventral side of the syrinx: musculus syringealis ventralis or ventral syringeal muscle (VS) and musculus tracheobronchialis ventralis or ventral tracheobronchial muscle (VTB), of which the latter consists of two parts: musculus tracheobronchialis ventralis profundus or deep ventral tracheobronchial muscle (DVTB) and musculus tracheobronchialis ventralis superficialis or superficial ventral tracheobronchial muscle (SVTB) (Figure 8A,B). The VS is the largest syringeal muscle and its caudal attachment site is located in the cup of bronchial half-ring B2 and on the MVC, continuous with the ventral end of B2 (Figures 8C,D and 9A). Rostrally, the attachment site, which can be clearly seen as an impression in Figure 2 and Additional file 1 starts on the mid part of the tympanum and extends to the top of the tympanum (Figure 8C,K). The VS is organized as a series of muscle sheets that run parallel to the central axis of the syrinx (Figure 9B). The VTB has previously been considered as a single muscle [73], but using our μCT data supported by micro-dissection, it became apparent that the VTB is made up of two parts with distinct rostral attachment sites. The caudal attachment site for SVTB fibers is located on the rostro-ventral tip of B3 (Figures 8C,D and 9B). The rostral attachment site is not on bone but instead on the clavicular air sac membrane (CASM) at tracheal rings T4 and T5 (Figures 8C,D and 9C). The caudal attachment site for the DVTB is located on B3 more proximal to the attachment site of the SVTB (Figures 8CD and 9B). Both the SVTB and the DVTB are externally apparent at this point, but, more rostrally, the DVTB twists underneath the SVTB and is no longer externally visible. The rostral attachment site of the DVTB is a very thin lateral strip on the tympanum, running parallel to the central axis of the syrinx (Figure 8D,K).


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)

Syringeal muscles of a freshly dissected male zebra finch syrinx. (A) Ventral view of the caudal part of the syrinx showing the ventral muscles VS and VTB, and the IBL. The IBL connects the primary bronchi and restricts their lateral movement. Dashed box is shown enlarged in B. (B) Detail of VTB attachment on bronchial half-ring B3. Syringeal muscles are organized in sheets of muscle fibers (arrowheads). (C) Close-up of the rostral attachment sites of the ventral muscles. The VS fibers end on the edge of the tympanum, while the SVTB fibers do not attach onto bone but end in the connective tissue of the CASM. Rostral to the CASM, the extrinsic TL attaches and runs along the trachea up to the larynx. (D) Lateral view of the right hemisyrinx showing the muscle attaching on B3. Some fibers of the STB attach directly on the ML that is located on the inside of B3. (E) Dorsal muscle attachment sites. (F) Lateral view of rostral attachment sites of SVTB and DTB clearly reveals the organization of syringeal muscles in sheets (arrowheads). Individual muscle fibers can be seen within the fiber bundle sheets. The edge of the CASM is indicated by the dashed black line. Abbreviations as listed in Table 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 9: Syringeal muscles of a freshly dissected male zebra finch syrinx. (A) Ventral view of the caudal part of the syrinx showing the ventral muscles VS and VTB, and the IBL. The IBL connects the primary bronchi and restricts their lateral movement. Dashed box is shown enlarged in B. (B) Detail of VTB attachment on bronchial half-ring B3. Syringeal muscles are organized in sheets of muscle fibers (arrowheads). (C) Close-up of the rostral attachment sites of the ventral muscles. The VS fibers end on the edge of the tympanum, while the SVTB fibers do not attach onto bone but end in the connective tissue of the CASM. Rostral to the CASM, the extrinsic TL attaches and runs along the trachea up to the larynx. (D) Lateral view of the right hemisyrinx showing the muscle attaching on B3. Some fibers of the STB attach directly on the ML that is located on the inside of B3. (E) Dorsal muscle attachment sites. (F) Lateral view of rostral attachment sites of SVTB and DTB clearly reveals the organization of syringeal muscles in sheets (arrowheads). Individual muscle fibers can be seen within the fiber bundle sheets. The edge of the CASM is indicated by the dashed black line. Abbreviations as listed in Table 1.
Mentions: We identified two muscles on the ventral side of the syrinx: musculus syringealis ventralis or ventral syringeal muscle (VS) and musculus tracheobronchialis ventralis or ventral tracheobronchial muscle (VTB), of which the latter consists of two parts: musculus tracheobronchialis ventralis profundus or deep ventral tracheobronchial muscle (DVTB) and musculus tracheobronchialis ventralis superficialis or superficial ventral tracheobronchial muscle (SVTB) (Figure 8A,B). The VS is the largest syringeal muscle and its caudal attachment site is located in the cup of bronchial half-ring B2 and on the MVC, continuous with the ventral end of B2 (Figures 8C,D and 9A). Rostrally, the attachment site, which can be clearly seen as an impression in Figure 2 and Additional file 1 starts on the mid part of the tympanum and extends to the top of the tympanum (Figure 8C,K). The VS is organized as a series of muscle sheets that run parallel to the central axis of the syrinx (Figure 9B). The VTB has previously been considered as a single muscle [73], but using our μCT data supported by micro-dissection, it became apparent that the VTB is made up of two parts with distinct rostral attachment sites. The caudal attachment site for SVTB fibers is located on the rostro-ventral tip of B3 (Figures 8C,D and 9B). The rostral attachment site is not on bone but instead on the clavicular air sac membrane (CASM) at tracheal rings T4 and T5 (Figures 8C,D and 9C). The caudal attachment site for the DVTB is located on B3 more proximal to the attachment site of the SVTB (Figures 8CD and 9B). Both the SVTB and the DVTB are externally apparent at this point, but, more rostrally, the DVTB twists underneath the SVTB and is no longer externally visible. The rostral attachment site of the DVTB is a very thin lateral strip on the tympanum, running parallel to the central axis of the syrinx (Figure 8D,K).

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