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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 internal bone structure of the male zebra finch demonstrates optimization by combining low weight with strength. (A) Ventral and (B) dorsal halves of a clipped bone surface rendering of non-contrasted μCT scan of the male syrinx, revealing the inside surface of the syrinx and cross-sectional views of the bronchial rings. The bronchial half-rings are hollow, laterally flattened, thin-walled bones fortified with trabeculae. The holes (asterisks) in the tympanum indicate lower X-ray attenuation values due to very thin walls or lower-density bone. The boxed inset shows a detailed view of bronchial half-rings B1 and B2 with trabeculae in bronchial half-ring B1. (C) Medial view of a semi-transparent volume rendering of the left hemisyrinx. Trabeculae can be seen as bright bars or dots, when seen on-axis, due to high density bone tissue (dashed circles). (D) Medial view of right hemisyrinx. Lateral flattening (ellipses) of bronchial half-rings increases their resistance to bending in the horizontal plane (dotted line and shaded plane) and therefore increases the maximal perpendicular force () that can be applied before mechanical failure occurs due to breaking [75,76]. The trabeculae prevent failure of the bones due to buckling [76]. Abbreviations as listed in Table 1.
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Figure 5: The internal bone structure of the male zebra finch demonstrates optimization by combining low weight with strength. (A) Ventral and (B) dorsal halves of a clipped bone surface rendering of non-contrasted μCT scan of the male syrinx, revealing the inside surface of the syrinx and cross-sectional views of the bronchial rings. The bronchial half-rings are hollow, laterally flattened, thin-walled bones fortified with trabeculae. The holes (asterisks) in the tympanum indicate lower X-ray attenuation values due to very thin walls or lower-density bone. The boxed inset shows a detailed view of bronchial half-rings B1 and B2 with trabeculae in bronchial half-ring B1. (C) Medial view of a semi-transparent volume rendering of the left hemisyrinx. Trabeculae can be seen as bright bars or dots, when seen on-axis, due to high density bone tissue (dashed circles). (D) Medial view of right hemisyrinx. Lateral flattening (ellipses) of bronchial half-rings increases their resistance to bending in the horizontal plane (dotted line and shaded plane) and therefore increases the maximal perpendicular force () that can be applied before mechanical failure occurs due to breaking [75,76]. The trabeculae prevent failure of the bones due to buckling [76]. Abbreviations as listed in Table 1.

Mentions: Bronchial half-ring B1 is the first of the three heavily modified bronchial half-rings, whose geometry can be best understood by rotating the 3D models in Additional file 1. Bronchial half-ring B1 is hollow and arc-shaped seen from a lateral view and flattened in transverse section (Figure 5A,B). It fits tightly to the tympanum and its internal walls form a smooth surface (Figure 5A). In addition, several trabeculae structurally connect the inner and outer walls of B1 (Figure 5). The dorsal end of B1 contains no trabeculae (Figure 5C,D), is rostro-caudally flattened, and has a concave muscle attachment site (Figure 2C and Additional file 1). The dorsal apex of B1 has a lateral protuberance of which the caudal side forms a smooth arc with the pessulus and B4 when seen from a dorsal viewpoint (Additional file 1, Cut dorsolateral view with labels). The second bronchial half-ring (B2) is also arc-shaped, hollow and slightly flattened. Both the ventral and dorsal side have cup-shaped muscle attachment sites (Figure 2). In contrast with B1, B2 has no internal trabeculae (Figure 5). The third bronchial half-ring (B3) is the least arced of the three half-rings but also hollow, laterally flattened and heavily reinforced with trabeculae. The dorsal end widens to about four times its medial width and is characterized by a domed surface on the rostral end, which forms a joint with the flattened dorsal cup of B2 (Additional file 1, Rostral view).


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 internal bone structure of the male zebra finch demonstrates optimization by combining low weight with strength. (A) Ventral and (B) dorsal halves of a clipped bone surface rendering of non-contrasted μCT scan of the male syrinx, revealing the inside surface of the syrinx and cross-sectional views of the bronchial rings. The bronchial half-rings are hollow, laterally flattened, thin-walled bones fortified with trabeculae. The holes (asterisks) in the tympanum indicate lower X-ray attenuation values due to very thin walls or lower-density bone. The boxed inset shows a detailed view of bronchial half-rings B1 and B2 with trabeculae in bronchial half-ring B1. (C) Medial view of a semi-transparent volume rendering of the left hemisyrinx. Trabeculae can be seen as bright bars or dots, when seen on-axis, due to high density bone tissue (dashed circles). (D) Medial view of right hemisyrinx. Lateral flattening (ellipses) of bronchial half-rings increases their resistance to bending in the horizontal plane (dotted line and shaded plane) and therefore increases the maximal perpendicular force () that can be applied before mechanical failure occurs due to breaking [75,76]. The trabeculae prevent failure of the bones due to buckling [76]. 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 5: The internal bone structure of the male zebra finch demonstrates optimization by combining low weight with strength. (A) Ventral and (B) dorsal halves of a clipped bone surface rendering of non-contrasted μCT scan of the male syrinx, revealing the inside surface of the syrinx and cross-sectional views of the bronchial rings. The bronchial half-rings are hollow, laterally flattened, thin-walled bones fortified with trabeculae. The holes (asterisks) in the tympanum indicate lower X-ray attenuation values due to very thin walls or lower-density bone. The boxed inset shows a detailed view of bronchial half-rings B1 and B2 with trabeculae in bronchial half-ring B1. (C) Medial view of a semi-transparent volume rendering of the left hemisyrinx. Trabeculae can be seen as bright bars or dots, when seen on-axis, due to high density bone tissue (dashed circles). (D) Medial view of right hemisyrinx. Lateral flattening (ellipses) of bronchial half-rings increases their resistance to bending in the horizontal plane (dotted line and shaded plane) and therefore increases the maximal perpendicular force () that can be applied before mechanical failure occurs due to breaking [75,76]. The trabeculae prevent failure of the bones due to buckling [76]. Abbreviations as listed in Table 1.
Mentions: Bronchial half-ring B1 is the first of the three heavily modified bronchial half-rings, whose geometry can be best understood by rotating the 3D models in Additional file 1. Bronchial half-ring B1 is hollow and arc-shaped seen from a lateral view and flattened in transverse section (Figure 5A,B). It fits tightly to the tympanum and its internal walls form a smooth surface (Figure 5A). In addition, several trabeculae structurally connect the inner and outer walls of B1 (Figure 5). The dorsal end of B1 contains no trabeculae (Figure 5C,D), is rostro-caudally flattened, and has a concave muscle attachment site (Figure 2C and Additional file 1). The dorsal apex of B1 has a lateral protuberance of which the caudal side forms a smooth arc with the pessulus and B4 when seen from a dorsal viewpoint (Additional file 1, Cut dorsolateral view with labels). The second bronchial half-ring (B2) is also arc-shaped, hollow and slightly flattened. Both the ventral and dorsal side have cup-shaped muscle attachment sites (Figure 2). In contrast with B1, B2 has no internal trabeculae (Figure 5). The third bronchial half-ring (B3) is the least arced of the three half-rings but also hollow, laterally flattened and heavily reinforced with trabeculae. The dorsal end widens to about four times its medial width and is characterized by a domed surface on the rostral end, which forms a joint with the flattened dorsal cup of B2 (Additional file 1, Rostral view).

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