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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 vibratory soft tissues in the primary bronchi. (A) Lateral view onto the lateral labium (LL, orange) of the male right hemisyrinx. Cartilaginous tissue (blue) extends from bronchial half-rings B2 and B3. The MVC (blue), a large cartilaginous pad, extends from B2 and bends medially. (B) Same structure as in A, but turned 180° around the vertical axis, providing a medial to lateral view onto the LL. The LL is connected to the medial side of bronchial half-ring B3 and is thickened in two bands (asterisks). (C) Same medial view as in B onto right LL of freshly dissected male right hemisyrinx (MVM removed). (D) Caudal view onto left LL of left hemisyrinx with left primary bronchus removed. (E) Lateral view on the medial vibratory mass (MVM, pink), the tissue continuum comprising ML and medial tympaniform membrane (MTM). Bronchial half-ring B3 is removed for an unobscured view onto the MVM, which attaches to the pessulus (PES) and forms the medial wall of the primary bronchi. (F) Same structure as in E, but turned 180° giving a medial to lateral view. The MVC is embedded in the ventral part of the MVM, as well as two small other cartilaginous pads: the medial dorsal cartilage (MDC) and the lateral dorsal cartilage (LDC). (G) Same view as in F of a freshly dissected right hemisyrinx with the musculature left intact. (H) Surface renderings of the ventral and (I) dorsal half of the internal bone structure of the syrinx with sound-producing labia. Abbreviations as listed in Table 1.
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Figure 7: The vibratory soft tissues in the primary bronchi. (A) Lateral view onto the lateral labium (LL, orange) of the male right hemisyrinx. Cartilaginous tissue (blue) extends from bronchial half-rings B2 and B3. The MVC (blue), a large cartilaginous pad, extends from B2 and bends medially. (B) Same structure as in A, but turned 180° around the vertical axis, providing a medial to lateral view onto the LL. The LL is connected to the medial side of bronchial half-ring B3 and is thickened in two bands (asterisks). (C) Same medial view as in B onto right LL of freshly dissected male right hemisyrinx (MVM removed). (D) Caudal view onto left LL of left hemisyrinx with left primary bronchus removed. (E) Lateral view on the medial vibratory mass (MVM, pink), the tissue continuum comprising ML and medial tympaniform membrane (MTM). Bronchial half-ring B3 is removed for an unobscured view onto the MVM, which attaches to the pessulus (PES) and forms the medial wall of the primary bronchi. (F) Same structure as in E, but turned 180° giving a medial to lateral view. The MVC is embedded in the ventral part of the MVM, as well as two small other cartilaginous pads: the medial dorsal cartilage (MDC) and the lateral dorsal cartilage (LDC). (G) Same view as in F of a freshly dissected right hemisyrinx with the musculature left intact. (H) Surface renderings of the ventral and (I) dorsal half of the internal bone structure of the syrinx with sound-producing labia. Abbreviations as listed in Table 1.

Mentions: The bilateral sound-producing vibrating tissues in the songbird syrinx [24,26,30,32] are located in the primary bronchi (Figure 7). Additional file 2 contains the interactive 3D model in which all structures are switched on initially. Although both left and right sides can be interactively accessed in Additional file 2, we will here focus on the right side of the male syrinx because it is predominantly used during zebra finch vocalization [71]. The lateral labium is connected to the medial side of half-ring B3 from dorsal to ventral (Figure 7A,B and Additional file 2, view Lateral labium) and thickens in two rostro-caudal running bands (Figure 7B), as also observed in all our fresh tissue micro-dissections (Figure 7C,D). On its medial side, each bronchus is sealed airtight from the pessulus to the lungs by the medial vibratory mass (Figure 7E and Additional file 2, view Medial vibratory mass). This tissue continuum [32] is roughly triangular-shaped from a medio-lateral view and consists of a thicker rostral part, the medial labium that connects dorso-ventrally to the pessulus, and a thinner caudal part, the medial tympaniform membrane (Figure 7F). We found no evidence of a membrana semilunaris on top of the pessulus in the zebra finch syrinx.


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 vibratory soft tissues in the primary bronchi. (A) Lateral view onto the lateral labium (LL, orange) of the male right hemisyrinx. Cartilaginous tissue (blue) extends from bronchial half-rings B2 and B3. The MVC (blue), a large cartilaginous pad, extends from B2 and bends medially. (B) Same structure as in A, but turned 180° around the vertical axis, providing a medial to lateral view onto the LL. The LL is connected to the medial side of bronchial half-ring B3 and is thickened in two bands (asterisks). (C) Same medial view as in B onto right LL of freshly dissected male right hemisyrinx (MVM removed). (D) Caudal view onto left LL of left hemisyrinx with left primary bronchus removed. (E) Lateral view on the medial vibratory mass (MVM, pink), the tissue continuum comprising ML and medial tympaniform membrane (MTM). Bronchial half-ring B3 is removed for an unobscured view onto the MVM, which attaches to the pessulus (PES) and forms the medial wall of the primary bronchi. (F) Same structure as in E, but turned 180° giving a medial to lateral view. The MVC is embedded in the ventral part of the MVM, as well as two small other cartilaginous pads: the medial dorsal cartilage (MDC) and the lateral dorsal cartilage (LDC). (G) Same view as in F of a freshly dissected right hemisyrinx with the musculature left intact. (H) Surface renderings of the ventral and (I) dorsal half of the internal bone structure of the syrinx with sound-producing labia. Abbreviations as listed in Table 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
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Figure 7: The vibratory soft tissues in the primary bronchi. (A) Lateral view onto the lateral labium (LL, orange) of the male right hemisyrinx. Cartilaginous tissue (blue) extends from bronchial half-rings B2 and B3. The MVC (blue), a large cartilaginous pad, extends from B2 and bends medially. (B) Same structure as in A, but turned 180° around the vertical axis, providing a medial to lateral view onto the LL. The LL is connected to the medial side of bronchial half-ring B3 and is thickened in two bands (asterisks). (C) Same medial view as in B onto right LL of freshly dissected male right hemisyrinx (MVM removed). (D) Caudal view onto left LL of left hemisyrinx with left primary bronchus removed. (E) Lateral view on the medial vibratory mass (MVM, pink), the tissue continuum comprising ML and medial tympaniform membrane (MTM). Bronchial half-ring B3 is removed for an unobscured view onto the MVM, which attaches to the pessulus (PES) and forms the medial wall of the primary bronchi. (F) Same structure as in E, but turned 180° giving a medial to lateral view. The MVC is embedded in the ventral part of the MVM, as well as two small other cartilaginous pads: the medial dorsal cartilage (MDC) and the lateral dorsal cartilage (LDC). (G) Same view as in F of a freshly dissected right hemisyrinx with the musculature left intact. (H) Surface renderings of the ventral and (I) dorsal half of the internal bone structure of the syrinx with sound-producing labia. Abbreviations as listed in Table 1.
Mentions: The bilateral sound-producing vibrating tissues in the songbird syrinx [24,26,30,32] are located in the primary bronchi (Figure 7). Additional file 2 contains the interactive 3D model in which all structures are switched on initially. Although both left and right sides can be interactively accessed in Additional file 2, we will here focus on the right side of the male syrinx because it is predominantly used during zebra finch vocalization [71]. The lateral labium is connected to the medial side of half-ring B3 from dorsal to ventral (Figure 7A,B and Additional file 2, view Lateral labium) and thickens in two rostro-caudal running bands (Figure 7B), as also observed in all our fresh tissue micro-dissections (Figure 7C,D). On its medial side, each bronchus is sealed airtight from the pessulus to the lungs by the medial vibratory mass (Figure 7E and Additional file 2, view Medial vibratory mass). This tissue continuum [32] is roughly triangular-shaped from a medio-lateral view and consists of a thicker rostral part, the medial labium that connects dorso-ventrally to the pessulus, and a thinner caudal part, the medial tympaniform membrane (Figure 7F). We found no evidence of a membrana semilunaris on top of the pessulus in the zebra finch syrinx.

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