As animals vocalize, their vocal organ transforms motor commands into vocalizations for social communication. In birds, the physical mechanisms by which vocalizations are produced and controlled remain unresolved because of the extreme difficulty in obtaining in vivo measurements. Here, we introduce an ex vivo preparation of the avian vocal organ that allows simultaneous high-speed imaging, muscle stimulation and kinematic and acoustic analyses to reveal the mechanisms of vocal production in birds across a wide range of taxa. Remarkably, we show that all species tested employ the myoelastic-aerodynamic (MEAD) mechanism, the same mechanism used to produce human speech. Furthermore, we show substantial redundancy in the control of key vocal parameters ex vivo, suggesting that in vivo vocalizations may also not be specified by unique motor commands. We propose that such motor redundancy can aid vocal learning and is common to MEAD sound production across birds and mammals, including humans.

Communication and Social Behaviour Group Max Planck Institute for Ornithology Seewiesen 82319 Germany

Coulter Department of Biomedical Engineering Georgia Institute of Technology Atlanta Georgia 30332 USA

Department of Biology Emory University Atlanta Georgia 30332 USA

Department of Biology University of Southern Denmark Campusvej 55 5230 Odense Denmark

Department of Orthopaedic Surgery and Traumatology Odense University Hospital University of Southern Denmark Odense 5230 Denmark

Faculty of Science Department of Biophysics Voice Research Lab Palacky University Olomouc 77146 Czech Republic

QuanTM program Emory University Atlanta Georgia 30322 USA

Université de Saint Etienne Lyon ENES CNPS CNRS UMR8195 Saint Etienne 42023 France

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King A. S. Functional anatomy of the syrinx in Form and Function in Birds (eds King A. S., McLelland J. 4, 105–192Academic Press (1989).

Brainard M. S. & Doupe A. J. Translating birdsong: songbirds as a model for basic and applied medical research. Annu. Rev. Neurosci. 36, 489–517 (2013). PubMed PMC

Fee M. S. & Scharff C. The songbird as a model for the generation and learning of complex sequential behaviors. ILAR J. 51, 362–377 (2010). PubMed

Elemans C. P. H. The singer and the song: The neuromechanics of avian sound production. Curr. Opin. Neurobiol. 28, 172–178 (2014). PubMed

Goller F. & Larsen O. N. A new mechanism of sound generation in songbirds. Proc. Natl Acad. Sci. USA 94, 14787–14791 (1997). PubMed PMC

Jensen K. K., Cooper B. G., Larsen O. N. & Goller F. Songbirds use pulse tone register in two voices to generate low-frequency sound. Proc. Biol. Sci. 274, 2703–2710 (2007). PubMed PMC

Elemans C. P. H., Zaccarelli R. & Herzel H. Biomechanics and control of vocalization in a non-songbird. J. R. Soc. Interface 5, 691–703 (2008). PubMed PMC

Zaccarelli R., Elemans C. P. H., Fitch W. T. & Herzel H. Modelling bird songs: voice onset, overtones and registers. Acta Acust. United Acust. 92, 741–748 (2006).

Mindlin G. B. & Laje R. The Physics of Birdsong Springer (2005).

Amador A. & Margoliash D. A mechanism for frequency modulation in songbirds shared with humans. J. Neurosci. 33, 11136–11144 (2013). PubMed PMC

Amador A., Perl Y. S., Mindlin G. B. & Margoliash D. Elemental gesture dynamics are encoded by song premotor cortical neurons. Nature 495, 59–64 (2013). PubMed PMC

van den Berg J. Myoelastic-aerodynamic theory of voice production. J. Speech Hear. Res. 1, 227–244 (1958). PubMed

Titze I. R. Principles of Voice Production National Center for Voice and Speech (2000).

Titze I. R. Comments on the myoelastic—aerodynamic theory of phonation. J. Speech Hear. Res. 23, 495–510 (1980). PubMed

Titze I. R. & Alipour F. The Myoelastic Aerodynamic Theory of Phonation National Center for Voice and Speech (2006).

Riede T. & Goller F. Peripheral mechanisms for vocal production in birds—differences and similarities to human speech and singing. Brain Lang. 115, 69–80 (2010). PubMed PMC

Fitch T. in Encyclopedia of language and linguistics 2nd ed., Vol. 10 (ed Brown, K) 115–121 (Oxford, Elsevier (2006).

Herbst C. T. et al. How low can you go? Physical production mechanism of elephant infrasonic vocalizations. Science 337, 595–599 (2012). PubMed

Titze I. R. & Strong W. J. Normal modes in vocal cord tissues. J. Acoust. Soc. Am. 57, 736–749 (1975). PubMed

Titze I. R. On the relation between subglottal pressure and fundamental frequency in phonation. J. Acoust. Soc. Am. 85, 901–906 (1989). PubMed

Svec J. G., Horácek J., Sram F. & Veselý J. Resonance properties of the vocal folds: in vivo laryngoscopic investigation of the externally excited laryngeal vibrations. J. Acoust. Soc. Am. 108, 1397–1407 (2000). PubMed

Berry D. A. Mechanisms of modal and nonmodal phonation. J. Phon. 29, 431–450 (2001).

Flanagan J. L. & Landgraf L. L. Self-oscillating source for vocal-tract synthesizers. IEEE Trans. Audio Electroacoust. AU16, 57 (1968).

Titze I. R. The physics of small-amplitude oscillation of the vocal folds. J. Acoust. Soc. Am. 83, 1536–1552 (1988). PubMed

Ishizaka K. & Flanagan J. L. Synthesis of voiced sounds from a two-mass model of the vocal cords. Bell Syst. Tech. J. 51, 1233–1268 (1972).

Scherer R. C., Torkaman S., Kucinschi B. R. & Afjeh A. A. Intraglottal pressures in a three-dimensional model with a non-rectangular glottal shape. J. Acoust. Soc. Am. 128, 828–838 (2010). PubMed PMC

Fulcher L. P. et al. Pressure distributions in a static physical model of the hemilarynx: measurements and computations. J. Voice 24, 2–20 (2010). PubMed PMC

Miller D. G. & Schutte H. K. Characteristic patterns of sub-and supraglottal pressure variations within the glottal cycle. in Transcr. XIIIth Symp. Care Prof. Voice (ed. Lawrence, V. 70–75 (The Voice Foundation, New York, NY, USA, 1985).

Schutte H. K. & Miller D. G. Resonanzspiele der Gesangsstimme in ihren Beziehungen zu supra- und subglottalen Druckverläufen: Konsequenzen für die Stimmbildungstheorie. Folia. Phoniatr. (Basel) 40, 65–73 (1988). PubMed

Herbst C. T. et al. Complex vibratory patterns in an elephant larynx. J. Exp. Biol. 216, 4054–4064 (2013). PubMed

Larsen O. N. & Goller F. Role of syringeal vibrations in bird vocalizations. Proc. R. Soc. Biol. Sci. 266, 1609–1615 (1999).

Fee M. S., Shraiman B., Pesaran B. & Mitra P. P. The role of nonlinear dynamics of the syrinx in the vocalizations of a songbird. Nature 395, 67–71 (1998). PubMed

Fee M. S. Measurement of the linear and nonlinear mechanical properties of the oscine syrinx: implications for function. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 188, 829–839 (2002). PubMed

Dürrwang R. Funktionelle Biologie, Anatomie und Physiologie der Vogelstimme PhD thesis, University of Basel (Aku-Fotodruck, Basel, (1974).

Paulsen K. Das Prinzip der Stimmbildung in der Wirbeltierrehe und beim Menschen Akademische Verlagsgesellschaft (1967).

Amador A. & Mindlin G. B. Beyond harmonic sounds in a simple model for birdsong production. Chaos 18, 043123 (2008). PubMed

Goller F. & Riede T. Integrative physiology of fundamental frequency control in birds. J. Physiol. Paris 107, 230–242 (2013). PubMed PMC

Suthers R. A. & Zollinger S. A. in Neuroscience of birdsong (eds Zeigler, H.P. & Marler P) 78–98 (Cambridge University Press, Cambridge, UK, (2008).

Bernstein N. The Co-ordination and Regulation of Movements Pergamon Press (1967).

Herbst C. T., Ternström S. & Švec J. G. Investigation of four distinct glottal configurations in classical singing—a pilot study. J. Acoust. Soc. Am. 125, EL104–EL109 (2009). PubMed

Riede T. & Goller F. Morphological basis for the evolution of acoustic diversity in oscine songbirds. Proc. Biol. Sci. 281, 20132306 (2014). PubMed PMC

Kusuyama T., Fukuda H., Shiotani A., Nakagawa H. & Kanzaki J. Analysis of vocal fold vibration by X-ray stroboscopy with multiple markers. Otolaryngol. Head Neck Surg. 124, 317–322 (2001). PubMed

Döllinger M., Tayama N. & Berry D. A. Empirical eigenfunctions and medial surface dynamics of a human vocal fold. Methods Inf. Med. 44, 384–391 (2005). PubMed

Boessenecker A., Berry D. A., Lohscheller J., Eysholdt U. & Doellinger M. Mucosal wave properties of a human vocal fold. Acta Acust. United Acust. 93, 815–823 (2007).

Kobler J. B., Chang E. W., Zeitels S. M. & Yun S.-H. Dynamic imaging of vocal fold oscillation with four-dimensional optical coherence tomography. Laryngoscope 120, 1354–1362 (2010). PubMed PMC

Döllinger M., Berry D. A. & Berke G. S. Medial surface dynamics of an in vivo canine vocal fold during phonation. J. Acoust. Soc. Am. 117, 3174–3183 (2005). PubMed

Titze I. R., Jiang J. J. & Hsiao T. Y. Measurement of mucosal wave propagation and vertical phase difference in vocal fold vibration. Ann. Otol. Rhinol. Laryngol. 102, 58–63 (1993). PubMed

Maina J. N. The Lung-Air Sac System of Birds Springer Science & Business Media (2006).

Maina J. N., Singh P. & Moss E. A. Inspiratory aerodynamic valving occurs in the ostrich, Struthio camelus lung: a computational fluid dynamics study under resting unsteady state inhalation. Respir. Physiol. Neurobiol. 169, 262–270 (2009). PubMed

Mackelprang R. & Goller F. Ventilation patterns of the songbird lung/air sac system during different behaviors. J. Exp. Biol. 216, 3611–3619 (2013). PubMed PMC

Brackenbury J. H. Lung-air-sac anatomy and respiratory pressures in the bird. J. Exp. Biol. 57, 543–550 (1972). PubMed

Gaunt A. S., Stein R. C. & Gaunt S. L. Pressure and air flow during distress calls of the starling, Sturnus vulgaris (Aves; Passeriformes). J. Exp. Zool. 183, 241–261 (1973).

Beckers G. J. L. Mechanisms of frequency and amplitude modulation in ring dove song. J. Exp. Biol. 206, 1833–1843 (2003). PubMed

Elemans C. P. H., Spierts I. L. Y., Müller U. K., van Leeuwen J. L. & Goller F. Bird song: superfast muscles control dove's trill. Nature 431, 146 (2004). PubMed

Elemans C. P. H., Mead A. F., Rome L. C. & Goller F. Superfast vocal muscles control song production in songbirds. PLoS ONE 3, e2581 (2008). PubMed PMC

Düring D. N. et al. The songbird syrinx morphome: a three-dimensional, high-resolution, interactive morphological map of the zebra finch vocal organ. BMC Biol. 11, 1 (2013). PubMed PMC

Sober S. J., Wohlgemuth M. J. & Brainard M. S. Central contributions to acoustic variation in birdsong. J. Neurosci. 28, 10370–10379 (2008). PubMed PMC

Scholz J. P. & Schoner G. The uncontrolled manifold concept: identifying control variables for a functional task. Exp. Brain Res. 126, 289–306 (1999). PubMed

Todorov E. & Jordan M. I. Optimal feedback control as a theory of motor coordination. Nat. Neurosci. 5, 1226–1235 (2002). PubMed

Latash M. L. The bliss (not the problem) of motor abundance (not redundancy). Exp. Brain Res. 217, 1–5 (2012). PubMed PMC

Chhetri D. K. et al. Effects of asymmetric superior laryngeal nerve stimulation on glottic posture, acoustics, vibration. Laryngoscope 123, 3110–3116 (2013). PubMed PMC

Chhetri D. K., Neubauer J. & Berry D. A. Neuromuscular control of fundamental frequency and glottal posture at phonation onset. J. Acoust. Soc. Am. 131, 1401–1412 (2012). PubMed PMC

Qiu Q. & Schutte H. K. Real-time kymographic imaging for visualizing human vocal-fold vibratory function. Rev. Sci. Instrum. 78, 024302 (2007). PubMed

Švec J. G. & Schutte H. K. Kymographic imaging of laryngeal vibrations. Curr. Opin. Otolaryngol. Head Neck Surg. 20, 458–465 (2012). PubMed

Baken R. J. Electroglottography. J. Voice 6, 98–110 (1992).

Dooling R. J., Lohr B. & Dent M. L. Comparative Hearing: Birds and Reptiles 13, 308–359Springer (2000).

Goller F. & Suthers R. A. Role of syringeal muscles in controlling the phonology of bird song. J. Neurophysiol. 76, 287–300 (1996). PubMed

Schuster S., Zollinger S. A., Lesku J. A. & Brumm H. On the evolution of noise-dependent vocal plasticity in birds. Biol. Lett. 8, 913–916 (2012). PubMed PMC

Elemans C. P. H., Laje R., Mindlin G. B. & Goller F. Smooth operator: avoidance of subharmonic bifurcations through mechanical mechanisms simplifies song motor control in adult zebra finches. J. Neurosci. 30, 13246–13253 (2010). PubMed PMC

Secora K. R. et al. Syringeal specialization of frequency control during song production in the Bengalese finch (Lonchura striata domestica). PLoS ONE 7, e34135 (2012). PubMed PMC

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