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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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Overview of terminology describing ossified structural elements of the songbird syrinx. Alternative nomenclatures of previous authors [16,18,19,28,43,52,72,73,106,123-129]. The system that we adopt in this study is a combination of terminologies proposed by Häcker [129], Chamberlain and colleagues [125], and Warner [126]. Note in particular the approach proposed by Ames [19], which emphasizes the microstructure of individual syringeal bones that make up the tympanum. Abbreviations as listed in Table 1.
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Figure 4: Overview of terminology describing ossified structural elements of the songbird syrinx. Alternative nomenclatures of previous authors [16,18,19,28,43,52,72,73,106,123-129]. The system that we adopt in this study is a combination of terminologies proposed by Häcker [129], Chamberlain and colleagues [125], and Warner [126]. Note in particular the approach proposed by Ames [19], which emphasizes the microstructure of individual syringeal bones that make up the tympanum. Abbreviations as listed in Table 1.

Mentions: The zebra finch syringeal skeleton consists of modified tracheal rings and bronchial half-rings. It is therefore considered a syrinx of the tracheobronchial type [16]. Two bronchial half-rings and four to six tracheal rings are fused to form a rigid cylinder named the tympanum (Figure 2 and Additional file 1). At the tympanum's caudal end, two bronchial half-rings form a medial dorso-ventral bridge called the pessulus (Figure 2 and Caudal view in Additional file 1). The trachea consists of tracheal rings (T1, T2, and so on) rostral to the tympanum. Caudal to the tympanum are bronchial half-rings (B1, B2, and so on), of which the first three (B1 to B3) are highly modified (Figure 2). Despite the above-mentioned observation that the most caudal part of the tympanum consists of two bronchial half-rings, we decided not to rename them B1 to avoid excessive alterations to existing nomenclature. Figure 4 lists our nomenclature together with the alternative nomenclature of previous authors.


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)

Overview of terminology describing ossified structural elements of the songbird syrinx. Alternative nomenclatures of previous authors [16,18,19,28,43,52,72,73,106,123-129]. The system that we adopt in this study is a combination of terminologies proposed by Häcker [129], Chamberlain and colleagues [125], and Warner [126]. Note in particular the approach proposed by Ames [19], which emphasizes the microstructure of individual syringeal bones that make up the tympanum. 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 4: Overview of terminology describing ossified structural elements of the songbird syrinx. Alternative nomenclatures of previous authors [16,18,19,28,43,52,72,73,106,123-129]. The system that we adopt in this study is a combination of terminologies proposed by Häcker [129], Chamberlain and colleagues [125], and Warner [126]. Note in particular the approach proposed by Ames [19], which emphasizes the microstructure of individual syringeal bones that make up the tympanum. Abbreviations as listed in Table 1.
Mentions: The zebra finch syringeal skeleton consists of modified tracheal rings and bronchial half-rings. It is therefore considered a syrinx of the tracheobronchial type [16]. Two bronchial half-rings and four to six tracheal rings are fused to form a rigid cylinder named the tympanum (Figure 2 and Additional file 1). At the tympanum's caudal end, two bronchial half-rings form a medial dorso-ventral bridge called the pessulus (Figure 2 and Caudal view in Additional file 1). The trachea consists of tracheal rings (T1, T2, and so on) rostral to the tympanum. Caudal to the tympanum are bronchial half-rings (B1, B2, and so on), of which the first three (B1 to B3) are highly modified (Figure 2). Despite the above-mentioned observation that the most caudal part of the tympanum consists of two bronchial half-rings, we decided not to rename them B1 to avoid excessive alterations to existing nomenclature. Figure 4 lists our nomenclature together with the alternative nomenclature of previous authors.

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