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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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Muscle actuation of bronchial half-rings B1-B3. (A) Rostro-lateral and (B) dorso-lateral view of the right primary bronchus showing the muscles DDS and LDS that attach directly onto bronchial half-ring B1. (C,D) Same views as in A and B, but now showing the muscles DTB and STB that attach directly onto bronchial half-ring B2. The large VS muscle is omitted for clarity. (E,F) The muscles SVTB and DVTB attach directly onto bronchial half-ring B3. Abbreviations as listed in Table 1. Colors as in previous figures.
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Figure 11: Muscle actuation of bronchial half-rings B1-B3. (A) Rostro-lateral and (B) dorso-lateral view of the right primary bronchus showing the muscles DDS and LDS that attach directly onto bronchial half-ring B1. (C,D) Same views as in A and B, but now showing the muscles DTB and STB that attach directly onto bronchial half-ring B2. The large VS muscle is omitted for clarity. (E,F) The muscles SVTB and DVTB attach directly onto bronchial half-ring B3. Abbreviations as listed in Table 1. Colors as in previous figures.

Mentions: All other intrinsic syringeal muscles attach directly to bronchial half-rings B1 to B3 (Figure 11). Each half-ring has a parallel-running pair of muscles of which at least one muscle attaches to the tympanum and one more rostrally to the CASM. Two dorsal muscles actuate the bronchial half-ring B1: the LDS attaches to the tympanum and the DDS to the CASM (Figure 11A,B). Three muscles actuate the bronchial half-ring B2: on the dorsal side the parallel-running muscles DTB and STB (Figure 11C,D), of which the STB attaches to the tympanum and the DTB to the CASM. On the ventral side of the syrinx, some fibers of the VS attach to the ventral side of half-ring B2 (Figure 10A). Therefore both DTB and STB could act as functional antagonists to the VS, rotating half-ring B2 around a medial pivot (Figure 11C). Finally, two parts of the VTB actuate bronchial half-ring B3 of which the DVTB attaches to the tympanum and the SVTB to the CASM.


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)

Muscle actuation of bronchial half-rings B1-B3. (A) Rostro-lateral and (B) dorso-lateral view of the right primary bronchus showing the muscles DDS and LDS that attach directly onto bronchial half-ring B1. (C,D) Same views as in A and B, but now showing the muscles DTB and STB that attach directly onto bronchial half-ring B2. The large VS muscle is omitted for clarity. (E,F) The muscles SVTB and DVTB attach directly onto bronchial half-ring B3. Abbreviations as listed in Table 1. Colors as in previous figures.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 11: Muscle actuation of bronchial half-rings B1-B3. (A) Rostro-lateral and (B) dorso-lateral view of the right primary bronchus showing the muscles DDS and LDS that attach directly onto bronchial half-ring B1. (C,D) Same views as in A and B, but now showing the muscles DTB and STB that attach directly onto bronchial half-ring B2. The large VS muscle is omitted for clarity. (E,F) The muscles SVTB and DVTB attach directly onto bronchial half-ring B3. Abbreviations as listed in Table 1. Colors as in previous figures.
Mentions: All other intrinsic syringeal muscles attach directly to bronchial half-rings B1 to B3 (Figure 11). Each half-ring has a parallel-running pair of muscles of which at least one muscle attaches to the tympanum and one more rostrally to the CASM. Two dorsal muscles actuate the bronchial half-ring B1: the LDS attaches to the tympanum and the DDS to the CASM (Figure 11A,B). Three muscles actuate the bronchial half-ring B2: on the dorsal side the parallel-running muscles DTB and STB (Figure 11C,D), of which the STB attaches to the tympanum and the DTB to the CASM. On the ventral side of the syrinx, some fibers of the VS attach to the ventral side of half-ring B2 (Figure 10A). Therefore both DTB and STB could act as functional antagonists to the VS, rotating half-ring B2 around a medial pivot (Figure 11C). Finally, two parts of the VTB actuate bronchial half-ring B3 of which the DVTB attaches to the tympanum and the SVTB to the CASM.

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