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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.

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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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Two syringeal muscles exert direct motor control on the medial vibratory mass. (A) Ventral and (B) dorsal view of the right primary bronchus. The muscles VS and MDS insert directly on cartilaginous pads embedded in the MVM, hence controlling its tension. (C) Medial view of the MVM of the morphome and (D) of a fresh dissection. Contraction of the VS generates a force (FVS) that bends the MVC, thereby stretching (dotted lines) the ML towards the lateral dorsal cartilage (LDC). Energy stored within the MVC is released after VS contraction. This restores VS length back to resting length, and therefore also reduces the tension in the ML back to baseline. Contraction of the MDS generates a force (FMDS) that also increases tension in MVM, but with a different orientation. (E) The rostral view shows that the projected working lines (arrows) of the VS and MDS are aligned along the dorso-ventral axis. Contraction of these muscles therefore results in no or very little adduction of the ML into the bronchial lumen, and modulates tension only. Abbreviations as listed in Table 1. Colors as in previous figures.
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Figure 10: Two syringeal muscles exert direct motor control on the medial vibratory mass. (A) Ventral and (B) dorsal view of the right primary bronchus. The muscles VS and MDS insert directly on cartilaginous pads embedded in the MVM, hence controlling its tension. (C) Medial view of the MVM of the morphome and (D) of a fresh dissection. Contraction of the VS generates a force (FVS) that bends the MVC, thereby stretching (dotted lines) the ML towards the lateral dorsal cartilage (LDC). Energy stored within the MVC is released after VS contraction. This restores VS length back to resting length, and therefore also reduces the tension in the ML back to baseline. Contraction of the MDS generates a force (FMDS) that also increases tension in MVM, but with a different orientation. (E) The rostral view shows that the projected working lines (arrows) of the VS and MDS are aligned along the dorso-ventral axis. Contraction of these muscles therefore results in no or very little adduction of the ML into the bronchial lumen, and modulates tension only. Abbreviations as listed in Table 1. Colors as in previous figures.

Mentions: The two bilateral pairs of labia are the principal sound generators in songbirds [24,26,30,32]. Our data show that two intrinsic syringeal muscles attach directly to cartilages that are embedded in the ML (Figure 10). Ventrally, the VS attaches to the MVC (Figure 8A) and, dorsally, the MDS attaches to the medial dorsal cartilage (Figure 10B). Because these cartilages are firmly embedded in the ML, our data suggest that, based on the orientation and location of the VS and MDS, shortening by either muscle would stretch the ML predominantly in the dorso-ventral axis. This would increase ML tension without changing ML ab- or adduction into the bronchial lumen (Figure 10C-E), which is consistent with earlier endoscopic observations during muscle micro-stimulation [23].


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)

Two syringeal muscles exert direct motor control on the medial vibratory mass. (A) Ventral and (B) dorsal view of the right primary bronchus. The muscles VS and MDS insert directly on cartilaginous pads embedded in the MVM, hence controlling its tension. (C) Medial view of the MVM of the morphome and (D) of a fresh dissection. Contraction of the VS generates a force (FVS) that bends the MVC, thereby stretching (dotted lines) the ML towards the lateral dorsal cartilage (LDC). Energy stored within the MVC is released after VS contraction. This restores VS length back to resting length, and therefore also reduces the tension in the ML back to baseline. Contraction of the MDS generates a force (FMDS) that also increases tension in MVM, but with a different orientation. (E) The rostral view shows that the projected working lines (arrows) of the VS and MDS are aligned along the dorso-ventral axis. Contraction of these muscles therefore results in no or very little adduction of the ML into the bronchial lumen, and modulates tension only. 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 10: Two syringeal muscles exert direct motor control on the medial vibratory mass. (A) Ventral and (B) dorsal view of the right primary bronchus. The muscles VS and MDS insert directly on cartilaginous pads embedded in the MVM, hence controlling its tension. (C) Medial view of the MVM of the morphome and (D) of a fresh dissection. Contraction of the VS generates a force (FVS) that bends the MVC, thereby stretching (dotted lines) the ML towards the lateral dorsal cartilage (LDC). Energy stored within the MVC is released after VS contraction. This restores VS length back to resting length, and therefore also reduces the tension in the ML back to baseline. Contraction of the MDS generates a force (FMDS) that also increases tension in MVM, but with a different orientation. (E) The rostral view shows that the projected working lines (arrows) of the VS and MDS are aligned along the dorso-ventral axis. Contraction of these muscles therefore results in no or very little adduction of the ML into the bronchial lumen, and modulates tension only. Abbreviations as listed in Table 1. Colors as in previous figures.
Mentions: The two bilateral pairs of labia are the principal sound generators in songbirds [24,26,30,32]. Our data show that two intrinsic syringeal muscles attach directly to cartilages that are embedded in the ML (Figure 10). Ventrally, the VS attaches to the MVC (Figure 8A) and, dorsally, the MDS attaches to the medial dorsal cartilage (Figure 10B). Because these cartilages are firmly embedded in the ML, our data suggest that, based on the orientation and location of the VS and MDS, shortening by either muscle would stretch the ML predominantly in the dorso-ventral axis. This would increase ML tension without changing ML ab- or adduction into the bronchial lumen (Figure 10C-E), which is consistent with earlier endoscopic observations during muscle micro-stimulation [23].

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