A new mechanism of sound generation in songbirds

Abstract

Our current understanding of the soundgenerating mechanism in the songbird vocal organ, the syrinx, is based on indirect evidence and theoretical treatments. The classical avian model of sound production postulates that the medial tympaniform membranes (MTM) are the principal sound generators. We tested the role of the MTM in sound generation and studied the songbird syrinx more directly by filming it endoscopically. After we surgically incapacitated the MTM as a vibratory source, zebra finches and cardinals were not only able to vocalize, but sang nearly normal song. This result shows clearly that the MTM are not the principal sound source. The endoscopic images of the intact songbird syrinx during spontaneous and brain stimulation-induced vocalizations illustrate the dynamics of syringeal reconfiguration before phonation and suggest a different model for sound production. Phonation is initiated by rostrad movement and stretching of the syrinx. At the same time, the syrinx is closed through movement of two soft tissue masses, the medial and lateral labia, into the bronchial lumen. Sound production always is accompanied by vibratory motions of both labia, indicating that these vibrations may be the sound source. However, because of the low temporal resolution of the imaging system, the frequency and phase of labial vibrations could not be assessed in relation to that of the generated sound. Nevertheless, in contrast to the previous model, these observations show that both labia contribute to aperture control and strongly suggest that they play an important role as principal sound generators.The study of vocal communication in songbirds makes significant contributions to various biological disciplines (1, 2) and provides inspiration to related areas, such as linguistics (3, 4). However, unlike the case in human speech (5), the physical mechanism of phonation in birds is poorly understood (6 -7).Sound production in songbirds is commonly believed to involve a constriction of the bronchial lumen by the lateral labium (LL), which, when combined with high subsyringeal air sac pressure and increased air velocity, induces vibrations of the medial tympaniform membranes (MTM) by Bernoulli forces and pressure differences. Support for this interpretation was provided by direct observation of vibrations of the MTM in the excised syrinx during artificially induced sound production (8), indirect anatomical and physiological observations (8-17), acoustic analyses (10, 18), simple syringeal models (18), and theoretical accounts (19)(20)(21)(22)(23). Detailed analyses of the vocal mechanism in non-songbirds (24-29) also provided a framework for the development of this classical model of songbird phonation. However, unlike the case in nonsongbirds (25-27), the predictions of this model for songbirds never have been tested by manipulation of the presumed sound generators, the MTM.Here we report the results of experiments in which the MTM were surgically disabled. Furthermore, we studied the intact songbird syrinx in situ by...

The neuromuscular control of birdsong

“…The precise rotational movement of the third bronchial semi-ring, which is involved in controlling the position of the lateral labium is still not su¤ciently understood (e.g. Chamberlain et al 1968;Goller & Larsen 1997), and the biomechanical mechanisms responsible for moving the medial labium have not been described. The muscles involved in this process of controlling the syringeal aperture have, however, been identi¢ed.…”

“…Each bronchus contains a pair of sound-generating medial and lateral labia. These can be adducted into the bronchial lumen and function as valves to regulate syringeal air£ow by restricting or closing the lumen of the ipsilateral side of the syrinx (Goller & Larsen 1997). The syringeal aperture and other aspects of syringeal con¢guration are controlled by half a dozen pairs of muscles (four intrinsic and two extrinsic) that envelop the syrinx (King 1989)(¢gure 3).…”

Neuromuscular control: introduction and overview

“…During phonation, air is pushed through the primary bronchi towards the mouth, while bronchial and tracheal membranes are pushed inwards by pressure in the interclavicular air sac. Endoscopic observations have shown that during phonation in songbirds, the syrinx deforms so that the medial and lateral labia ( just distal to the medial membranes of the bronchi) are pushed inwards forming a`vocal slit' which is analogous to the laryngeal vocal slit in mammals (Goller & Larsen 1998). The £ow of air sets the labia into oscillation with a fundamental frequency corresponding to that of the recorded sound.…”

“…Recent studies have not, however, supported this type of mechanism (Goller & Larsen 1997, 1998Ballintijn & Ten Cate 1998) in pigeons (a`non-songbird') and songbirds. Alternatively, voiced sounds are produced by a £ow-induced vibration of membranes (in non-songbirds; Goller & Larsen 1997) or labia and membranes (in songbirds; Goller & Larsen 1998) in the syrinx (the principal vocal organ around the junction of trachea and primary bronchi). During phonation, air is pushed through the primary bronchi towards the mouth, while bronchial and tracheal membranes are pushed inwards by pressure in the interclavicular air sac.…”

Glycohistochemistry of the lateral tympanic membrane in the syrinx of the Denizli cock

“…It has been reported that the LTM is the main sound generator in pigeons (4). Furthermore, Goller and Larsen (11) suggested that the labia play an important role as principal sound generators in the songbirds. Riede and Goller (12) also reported that laterally positioned labia are passively set into vibration, thus interrupting a passing air stream.…”