Universal mechanisms of sound production and control in birds and mammals.

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.

New perspectives on mechanisms of sound generation in songbirds.

The physical mechanisms of sound generation in the vocal organ, the syrinx, of songbirds have been investigated mostly with indirect methods. Recent direct endoscopic observation identified vibrations of the labia as the principal sound source. This model suggests sound generation in a pulse-tone mechanism similar to human phonation with the labia forming a pneumatic valve. The classical avian model proposed that vibrations of the thin medial tympaniform membranes are the primary sound generating mechanism. As a direct test of these two hypotheses we ablated the medial tympaniform membranes in two species (cardinal and zebra finch) and found that both were still able to phonate and sing without functional membranes. Small changes in song structure (harmonic emphasis, frequency control) occurred after medial tympaniform membrane ablation and suggest that the medial tympaniform membranes play a role in adjusting tension on the labia. Such a role is consistent with the fact that the medial tympaniform membranes are directly attached to the medial labia. There is no experimental support for a third hypothesis, proposing an aerodynamic model for generation of tonal sounds. Indirect tests (song in heliox atmosphere) as well as direct (labial vibration during tonal sound) measurements of syringeal vibrations support a vibration-based sound-generating mechanism even for tonal sounds.

Migrating songbirds tested in computer-controlled Emlen funnels use stellar cues for a time-independent compass.

This paper investigates how young pied flycatchers, Ficedula hypoleuca, and blackcaps, Sylvia atricapilla, interpret and use celestial cues. In order to record these data, we developed a computer-controlled version of the Emlen funnel, which enabled us to make detailed temporal analyses. First, we showed that the birds use a star compass. Then, we tested the birds under a stationary planetarium sky, which simulated the star pattern of the local sky at 02:35 h for 11 consecutive hours of the night, and compared the birds' directional choices as a function of time with the predictions from five alternative stellar orientation hypotheses. The results supported the hypothesis suggesting that birds use a time-independent star compass based on learned geometrical star configurations to pinpoint the rotational point of the starry sky (north). In contrast, neither hypotheses suggesting that birds use the stars for establishing their global position and then perform true star navigation nor those suggesting the use of a time-compensated star compass were supported.

Avian species differences in susceptibility to noise exposure.

Previous studies of hair cell regeneration and hearing recovery in birds after acoustic overstimulation have involved relatively few species. Studies of the effects of acoustic overexposure typically report high variability. Though it is impossible to tell, the data so far also suggest there may be considerable species differences in the degree of damage and the time course and extent of recovery. To examine this issue, we exposed four species of birds (quail, budgerigars, canaries, and zebra finches) to identical conditions of acoustic overstimulation and systematically analyzed changes in hearing sensitivity, basilar papilla morphology, and hair cell number. Quail and budgerigars showed the greatest susceptibility to threshold shift and hair cell loss after overstimulation with either pure tone or bandpass noise, while identical types of overstimulation in canaries and zebra finches resulted in much less of a threshold shift and a smaller, more diffuse hair cell loss. All four species showed some recovery of threshold sensitivity and hair cell number over time. Canary and zebra finch hearing and hair cell number recovered to within normal limits while quail and budgerigars continued to have an approximately 20 dB threshold shift and incomplete recovery of hair cell number. In a final experiment, birds were exposed to identical wide-band noise overstimulation under conditions of artificial middle ear ventilation. Hair cell loss was substantially increased in both budgerigars and canaries suggesting that middle ear air pressure regulation and correlated changes in middle ear transfer function are one factor influencing susceptibility to acoustic overstimulation in small birds.

In situ biomechanics of the syrinx and sound generation in pigeons.

The in situ biomechanics of the vocal organ, the syrinx, was studied in anesthetized pigeons using fiberoptic instruments. The role of syringeal muscles was determined by electrical stimulation, and phonation was induced by injecting gas into the subsyringeal air sacs. This study presents the first direct observations of the biomechanical processes that occur in an intact syrinx. Contraction of one of the syringeal muscles, the m. tracheolateralis (TL), withdraws the lateral tympaniform membranes (LTM) from the syringeal lumen, causing opening of the syringeal airways. Shortening of a second muscle, the sternotrachealis (ST), draws the syringeal cartilages closer to each other, causing the LTM to fold into the syringeal lumen. Maximal ST contraction does not lead to complete closure of the syrinx. As air-sac pressure is increased by the injection of gas, the LTM are drawn into the syringeal lumen and balloon in a rostral direction until they touch, thus forming a fold-like valve. Air-induced phonation is always associated with vibrations of the membrane folds, suggesting that pulsatile release of air into the trachea by vibratory motion of the LTM generates sound. During air-induced phonation, strong stimulation of the TL terminates sound generation by abducting the LTM, whereas weak stimulation changes the geometry of the membrane folds, which is accompanied by changes in the acoustic structure of the sound. Stimulation of the ST has little effect on air-induced sounds. The LTM appear to be the main sound generators, since disabling the medial tympaniform membranes (MTM) with tissue adhesive does not prevent phonation or change the frequency and amplitude structure of display coos in spontaneously vocalizing pigeons. Moreover, the activity of the syringeal muscles appears to have a mainly modulatory function, suggesting that the basic sound-generating mechanism is similar in both air-induced and natural phonation.

Mechanisms of vocal production in budgerigars (Melopsittacus undulatus).

Songbirds vocalizing in helium show a change in the spectral quality of their vocalizations. This effect is due to an increase in the speed of sound in helium that in turn alters the resonance properties of the vocal tract. Here, this approach is extended to a psittacine, the budgerigar (Melopsittacus undulatus), whose syringeal anatomy and innervation differ from that of a songbird. Contact calls from birds vocalizing in heliox (70/30 helium/oxygen environment) showed an overall increase in the amount of energy at frequencies above the fundamental, slight changes in the frequency of the fundamental and harmonics, and some change in the level of harmonics. Calls produced by a syringeally denervated bird showed more dramatic changes. Recordings from live birds were compared with sounds produced by various simple "artificial" tracheal and syringeal models. Results suggest that budgerigars produce contact calls using the syringeal membranes as a unitary sound source which produces acoustic energy in a narrow frequency band whose fundamental frequency is matched to the resonant frequency of the trachea. The syrinx is not normally coupled to the tracheal resonator, and resonances probably play only a minor role in shaping the spectrum of contact calls.

A new mechanism of sound generation in songbirds.

Our current understanding of the sound-generating 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.

Azimuthal sound localization in the European starling (Sturnus vulgaris): I. Physical binaural cues.

The physical measurements reported here test whether the European starling (Sturnus vulgaris) evaluates the azimuth direction of a sound source with a peripheral auditory system composed of two acoustically coupled pressure-difference receivers (1) or of two decoupled pressure receivers (2). A directional pattern of sound intensity in the free-field was measured at the entrance of the auditory meatus using a probe microphone, and at the tympanum using laser vibrometry. The maximum differences in the sound-pressure level measured with the microphone between various speaker positions and the frontal speaker position were 2.4 dB at 1 and 2 kHz, 7.3 dB at 4 kHz, 9.2 dB at 6 kHz, and 10.9 dB at 8 kHz. The directional amplitude pattern measured by laser vibrometry did not differ from that measured with the microphone. Neither did the directional pattern of travel times to the ear. Measurements of the amplitude and phase transfer function of the starling's interaural pathway using a closed sound system were in accord with the results of the free-field measurements. In conclusion, although some sound transmission via the interaural canal occurred, the present experiments support the hypothesis 2 above that the starling's peripheral auditory system is best described as consisting of two functionally decoupled pressure receivers.