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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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The sternotracheal muscle stabilizes the syrinx during song. (A) Lateral view of a μCT-based volume rendering showing the position of the syrinx in the skeletal framework of the upper thorax. A spine (orange dashed line) projects ventro-caudally from the second thoracic vertebra, thereby providing an anchor point for the lungs (green) and a pivot point (white circle) for the syrinx. On its ventral side, the syrinx fits into a dorsally oriented protrusion of the sternum, the external spine (EXS, *). The force (Fst) exerted by contraction of the ST (blue) rotates the syrinx ventrally (arrow) into the external spine. (B) Lateral view of a dissected syrinx with the ST muscles (left ST, black arrowheads) and their attachments intact. The external spine is continuous with a collagenous band (CB) that connects to the CASM (dotted white line). Also visible are the arteria syringealis, which supplies blood to the syrinx (white arrow), and the left syringeal nerve (black arrows). (C) Caudal view of a μCT-based volume rendering looking up from the sternum showing the position of the syrinx (yellow circle) and the attachment sites of the ST muscles (blue lines) in the intact skeletal framework. The ST attaches to tracheal ring T1 and on two lateral protrusions of the sternum. Contraction of the ST muscles pulls the syrinx onto the EXS. (D) Virtual slice through a 3D MRI dataset showing the syrinx (yellow dotted line) and EXS. Abbreviations as listed in Table 1.
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Figure 12: The sternotracheal muscle stabilizes the syrinx during song. (A) Lateral view of a μCT-based volume rendering showing the position of the syrinx in the skeletal framework of the upper thorax. A spine (orange dashed line) projects ventro-caudally from the second thoracic vertebra, thereby providing an anchor point for the lungs (green) and a pivot point (white circle) for the syrinx. On its ventral side, the syrinx fits into a dorsally oriented protrusion of the sternum, the external spine (EXS, *). The force (Fst) exerted by contraction of the ST (blue) rotates the syrinx ventrally (arrow) into the external spine. (B) Lateral view of a dissected syrinx with the ST muscles (left ST, black arrowheads) and their attachments intact. The external spine is continuous with a collagenous band (CB) that connects to the CASM (dotted white line). Also visible are the arteria syringealis, which supplies blood to the syrinx (white arrow), and the left syringeal nerve (black arrows). (C) Caudal view of a μCT-based volume rendering looking up from the sternum showing the position of the syrinx (yellow circle) and the attachment sites of the ST muscles (blue lines) in the intact skeletal framework. The ST attaches to tracheal ring T1 and on two lateral protrusions of the sternum. Contraction of the ST muscles pulls the syrinx onto the EXS. (D) Virtual slice through a 3D MRI dataset showing the syrinx (yellow dotted line) and EXS. Abbreviations as listed in Table 1.

Mentions: Our data support the hypothesis that shortening of the paired ST muscles can mechanically stabilize the syrinx during song [19,22,74]. Caudally to the syrinx, the primary bronchi are firmly anchored to the lungs, which are held in place against the vertebral column by a spiny intrusion of the second thoracic vertebra (Figure 12A). Micro-dissection shows that the syrinx is attached to this spine on the dorsal side by collagenous tissue. Furthermore, a thin, inflexible membrane, the interbronchial ligament (IBL), or bronchidesmus (Figures 8A and 9A), connects bronchial half-rings B4 and B5, thereby constraining rostral and lateral movement of the primary bronchi. These structures provide the caudal side of the syrinx with a rigid frame of reference relative to the spine (Figure 12A). In addition, on its dorsal side, the syrinx attaches to the esophagus and the vertebrae by collagenous sheets. We observed that ventral to the syrinx, the sternum protrudes into a Y-shape structure, the external spine (Figure 12). The ventral shape of the syrinx corresponds to the external spine (Figure 12B). Based on the orientation and attachment sites of the ST in situ (Figure 12C,D), our data suggest that co-activating the paired ST, leading to ST shortening, will pull the syrinx against the dorsal surface of the external spine, structurally stabilizing the syrinx relative to the skeleton.


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)

The sternotracheal muscle stabilizes the syrinx during song. (A) Lateral view of a μCT-based volume rendering showing the position of the syrinx in the skeletal framework of the upper thorax. A spine (orange dashed line) projects ventro-caudally from the second thoracic vertebra, thereby providing an anchor point for the lungs (green) and a pivot point (white circle) for the syrinx. On its ventral side, the syrinx fits into a dorsally oriented protrusion of the sternum, the external spine (EXS, *). The force (Fst) exerted by contraction of the ST (blue) rotates the syrinx ventrally (arrow) into the external spine. (B) Lateral view of a dissected syrinx with the ST muscles (left ST, black arrowheads) and their attachments intact. The external spine is continuous with a collagenous band (CB) that connects to the CASM (dotted white line). Also visible are the arteria syringealis, which supplies blood to the syrinx (white arrow), and the left syringeal nerve (black arrows). (C) Caudal view of a μCT-based volume rendering looking up from the sternum showing the position of the syrinx (yellow circle) and the attachment sites of the ST muscles (blue lines) in the intact skeletal framework. The ST attaches to tracheal ring T1 and on two lateral protrusions of the sternum. Contraction of the ST muscles pulls the syrinx onto the EXS. (D) Virtual slice through a 3D MRI dataset showing the syrinx (yellow dotted line) and EXS. 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 12: The sternotracheal muscle stabilizes the syrinx during song. (A) Lateral view of a μCT-based volume rendering showing the position of the syrinx in the skeletal framework of the upper thorax. A spine (orange dashed line) projects ventro-caudally from the second thoracic vertebra, thereby providing an anchor point for the lungs (green) and a pivot point (white circle) for the syrinx. On its ventral side, the syrinx fits into a dorsally oriented protrusion of the sternum, the external spine (EXS, *). The force (Fst) exerted by contraction of the ST (blue) rotates the syrinx ventrally (arrow) into the external spine. (B) Lateral view of a dissected syrinx with the ST muscles (left ST, black arrowheads) and their attachments intact. The external spine is continuous with a collagenous band (CB) that connects to the CASM (dotted white line). Also visible are the arteria syringealis, which supplies blood to the syrinx (white arrow), and the left syringeal nerve (black arrows). (C) Caudal view of a μCT-based volume rendering looking up from the sternum showing the position of the syrinx (yellow circle) and the attachment sites of the ST muscles (blue lines) in the intact skeletal framework. The ST attaches to tracheal ring T1 and on two lateral protrusions of the sternum. Contraction of the ST muscles pulls the syrinx onto the EXS. (D) Virtual slice through a 3D MRI dataset showing the syrinx (yellow dotted line) and EXS. Abbreviations as listed in Table 1.
Mentions: Our data support the hypothesis that shortening of the paired ST muscles can mechanically stabilize the syrinx during song [19,22,74]. Caudally to the syrinx, the primary bronchi are firmly anchored to the lungs, which are held in place against the vertebral column by a spiny intrusion of the second thoracic vertebra (Figure 12A). Micro-dissection shows that the syrinx is attached to this spine on the dorsal side by collagenous tissue. Furthermore, a thin, inflexible membrane, the interbronchial ligament (IBL), or bronchidesmus (Figures 8A and 9A), connects bronchial half-rings B4 and B5, thereby constraining rostral and lateral movement of the primary bronchi. These structures provide the caudal side of the syrinx with a rigid frame of reference relative to the spine (Figure 12A). In addition, on its dorsal side, the syrinx attaches to the esophagus and the vertebrae by collagenous sheets. We observed that ventral to the syrinx, the sternum protrudes into a Y-shape structure, the external spine (Figure 12). The ventral shape of the syrinx corresponds to the external spine (Figure 12B). Based on the orientation and attachment sites of the ST in situ (Figure 12C,D), our data suggest that co-activating the paired ST, leading to ST shortening, will pull the syrinx against the dorsal surface of the external spine, structurally stabilizing the syrinx relative to the skeleton.

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