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.

The habitat-induced degradation of the full song of the blackbird (Turdus merula) was quantified by measuring excess attenuation, reduction of the signal-to-noise ratio, and blur ratio, the latter measure representing the degree of blurring of amplitude and frequency patterns over time. All three measures were calculated from changes of the amplitude functions (i.e., envelopes) of the degraded songs using a new technique which allowed a compensation for the contribution of the background noise to the amplitude values. Representative songs were broadcast in a deciduous forest without leaves and rerecorded. Speakers and microphones were placed at typical blackbird emitter and receiver positions. Analyses showed that the three degradation measures were mutually correlated, and that they varied with log distance. Their variation suggests that the broadcast song could be detected across more than four, and discriminated across more than two territories. The song’s high-pitched twitter sounds were degraded more rapidly than its low-pitched motif sounds. Motif sounds with a constant frequency projected best. The effect of microphone height was pronounced, especially on motif sounds, whereas the effect of speaker height was negligible. Degradation was inversely proportional to microphone height. Changing the reception site from a low to a high position reduced the degradation by the same amount as by approaching the sound source across one-half or one-whole territory. This suggests that the main reason for a male to sing from a high perch is to improve the singer’s ability to hear responses to its songs, rather than to maximize the transmission distance. The difference in degradation between low and high microphone heights may explain why females, which tend to perch on low brush, disregard certain degradable components of the song.

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...

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The effects of bird song imply a transfer of information between conspecifics. This communication channel is constrained by habitat-induced degradation. Many studies suggest that birds can utilize features of degraded song to assess relative distance to the signaller (ranging). The degradation of transmitted song in the wren Troglodytes troglodytes is quantified to assess the opportunities offered in received song for both information transfer and ranging. This quantification incorporates three measurable aspects of degradation: signal-to-noise ratio; excess attenuation; blur ratio. Each aspect varies more-or-less predictably with transmission distance, i.e., a criterion for ranging. Significant effects of speaker and microphone elevation indicate a potential for birds to optimize both the opportunity for information transfer and ranging by considering perch location. Song elements are the smallest units of a song being defined as a continuous trace on a sonagram. Main and second-order effects of element type indicate element-specific patterns of degradation which could be a crucial factor in communication in this species. The element variation within a full song offers the potential for effective information transfer over a range of relevant distances and a variety of transmission pathways. It similarly offers highly flexible ranging opportunities.

Directional sound receivers are useful for locating sound sources, and they can also partly compensate for the signal degradations caused by noise and reverberations. Ears may become inherently directional if sound can reach both surfaces of the eardrum. Attempts to understand the physics of such pressure difference receiving ears have been hampered by lack of suitable experimental methods. In this review, we review the methods for collecting reliable data on the binaural directional cues at the eardrums, on how the eardrum vibrations depend on the direction of sound incidence, and on how sound waves behave in the air spaces leading to the interior surfaces of eardrums. A linear mathematical model with well-defined inputs is used for exploring how the directionality varies with the binaural directional cues and the amplitude and phase gain of the sound pathway to the inner surface of the eardrum. The mere existence of sound transmission to the inner surface does not ensure a useful directional hearing, since a proper amplitude and phase relationship must exist between the sounds acting on the two surfaces of the eardrum. The gain of the sound pathway must match the amplitude and phase of the sounds at the outer surfaces of the eardrums, which are determined by diffraction and by the arrival time of the sound, that is by the size and shape of the animal and by the frequency of sound. Many users of hearing aids do not obtain a satisfactory improvement of their ability to localize sound sources. We suggest that some of the mechanisms of directional hearing evolved in Nature may serve as inspiration for technical improvements.

In many birds, the middle ears are connected through an air-filled interaural pathway. Sound transmission through this pathway may improve directional hearing. However, attempts to demonstrate such a mechanism have produced conflicting results. One reason is that some species of birds develop a lower static air pressure in the middle ears when anaesthetized, which reduces eardrum vibrations. In anaesthetized budgerigars with vented interaural air spaces and presumed normal eardrum vibrations, we find that sound propagating through the interaural pathway considerably improves cues to the directional hearing. The directional cues in the received sound combined with amplitude gain and time delay of sound propagating through the interaural pathway quantitatively account for the observed dependence of eardrum vibration on direction of sound incidence. Interaural sound propagation is responsible for most of the frontal gradient of eardrum vibration (i.e. when a sound source is moved from a small contralateral angle to the same ipsilateral angle). Our study confirms that at low frequencies the interaural sound propagation may cause vibrations of the eardrum to differ much in time, thus providing a possible cue for directional hearing. The acoustically effective size of the head of our birds (diameter 28 mm) is much larger than expected from the dimensions of the skull, so apparently the feathers on the head have a considerable acoustical effect.

The sound-generating mechanism in the bird syrinx has been the subject of debate. Recent endoscopic imaging of the syrinx during phonation provided evidence for vibrations of membranes and labia, but could not provide quantitative analysis of the vibrations. We have now recorded vibrations in the intact syrinx directly with an optic vibration detector together with the emitted sound during brain stimulationinduced phonation in anaesthetized pigeons, cockatiels, and a hill myna. The phonating syrinx was also ¢lmed through an endoscope inserted into the trachea. In these species vibrations were always present during phonation, and their frequency and amplitude characteristics were highly similar to those of the emitted sound, including nonlinear acoustic phenomena. This was also true for tonal vocalizations, suggesting that a vibratory mechanism can account for all vocalizations presented in the study. In some vocalizations we found di¡erences in the shape of the waveform between vibrations and the emitted sound, probably re£ecting variations in oscillatory behaviour of syringeal structures. This study therefore provides the ¢rst direct evidence for a vibratory sound-generating mechanism (i.e. lateral tympaniform membranes or labia acting as pneumatic valves) and does not support pure aerodynamic models. Furthermore, the data emphasize a potentially high degree of acoustic complexity.