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Open Access Highly Accessed Research article

The songbird syrinx morphome: a three-dimensional, high-resolution, interactive morphological map of the zebra finch vocal organ

Daniel N Düring1, Alexander Ziegler2, Christopher K Thompson13, Andreas Ziegler4, Cornelius Faber5, Johannes Müller6, Constance Scharff1 and Coen PH Elemans7*

Author affiliations

1 Verhaltensbiologie, Freie Universität Berlin, Takustrasse 6, 14195 Berlin, Germany

2 Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA

3 Current address: Department of Cell Biology, The Scripps Research Institute, 10550 North Torrey Pine Road, La Jolla, CA 92037, USA

4 Institut für Immungenetik, Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Thielallee 73, 14195 Berlin, Germany

5 Institut für Klinische Radiologie, Universitätsklinikum Münster, Albert-Schweitzer-Campus 1, 48149 Münster, Germany

6 Museum für Naturkunde, Leibniz-Institut für Evolutions und Biodiversitätsforschung, Humboldt-Universität zu Berlin, Invalidenstraße 43, 10115 Berlin, Germany

7 Institute of Biology, University of Southern Denmark, Campusvej 55, 5230 Odense, Denmark

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Citation and License

BMC Biology 2013, 11:1  doi:10.1186/1741-7007-11-1

Published: 8 January 2013

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.