The acoustic effect of vocal tract adjustments in zebra finches

Vocal production in songbirds requires the control of the respiratory system, the syrinx as sound source and the vocal tract as acoustic filter. Vocal tract movements consist of beak, tongue and hyoid movements, which change the volume of the oropharyngeal–esophageal cavity (OEC), glottal movements and tracheal length changes. The respective contributions of each movement to filter properties are not completely understood, but the effects of this filtering are thought to be very important for acoustic communication in birds. One of the most striking movements of the upper vocal tract during vocal behavior in songbirds involves the OEC. This study measured the acoustic effect of OEC adjustments in zebra finches by comparing resonance acoustics between an utterance with OEC expansion (calls) and a similar utterance without OEC expansion (respiratory sounds induced by a bilateral syringeal denervation). X-ray cineradiography confirmed the presence of an OEC motor pattern during song and call production, and a custom-built Hall-effect collar system confirmed that OEC expansion movements were not present during respiratory sounds. The spectral emphasis during zebra finch call production ranging between 2.5 and 5 kHz was not present during respiratory sounds, indicating strongly that it can be attributed to the OEC expansion.     

Beak gape dynamics during song in the zebra finch

Bird song is a complex communication behavior that requires the coordination of several motor systems. Sound is produced in the syrinx and then modified by the upper vocal tract, but the specific nature and dynamics of this modification are not well understood. To determine the contribution of beak movements to sound modification, we studied the beak gape patterns in zebra finches (Taeniopygia guttata). Subsyringeal air sac pressure and song were recorded together with changes in beak gape, which were monitored with a magneto-sensitive transducer. Beak gape was positively correlated with fundamental frequency, peak frequency, and subsyringeal air sac pressure in all but one bird. For harmonic stacks, peak frequency increased with increasing beak gape, and the relationship between fundamental frequency and beak gape was no longer significant. Experimentally holding the beak open or closed had acoustic consequences consistent with the model in which beak movements change upper vocal tract length and, thus, the filter properties. Beak gape was positively correlated with sound amplitude in all but two birds. The relationship between beak aperture and amplitude may, however, be indirect because air sac pressure is correlated with amplitude and beak gape. The beak is opened quickly and to its widest aperture immediately prior to the onset of sound and at rapid transitions in sound, suggesting that beak movements may affect vibratory behavior of the labia.     

Peripheral control and lateralization of birdsong

Recent studies on several species of oscine songbirds show that they achieve their varied vocal performances through coordinated activity of respiratory, syringeal, and other vocal tract muscles in ways that take maximum advantage of the acoustic flexibility made possible by the presence of two independently controlled sound sources in their bipartite syrinx (vocal organ). During song, special motor programs to respiratory muscles alter the pattern of ventilation to maintain the supply of respiratory air and oxygen to permit songs of long duration, high syllable repetition rates, or maximum spectral complexity. Each side of the syrinx receives its own motor program that, together with that sent to respiratory muscles, determines the acoustic properties of the ipsilaterally produced sound. The acoustic expression of these bilaterally distinct, phonetic motor patterns depends on the action of dorsal syringeal adductor muscles that, by opening or closing the ipsilateral side of the syrinx to airflow, determine the amount each side contributes to song. The syringeally generated sound is further modified by muscles that control the shape of the vocal tract. Different species have adopted different motor strategies that use the left and right sides of the syrinx in patterns of unilateral, bilateral, alternating, or sequential phonation to achieve the differing temporal and spectral characteristics of their songs. As a result, the degree of song lateralization probably varies between species to form a continuum from unilateral dominance to bilateral equality. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 632–652, 1997     

Superfast vocal muscles control song production in songbirds

Birdsong is a widely used model for vocal learning and human speech, which exhibits high temporal and acoustic diversity. Rapid acoustic modulations are thought to arise from the vocal organ, the syrinx, by passive interactions between the two independent sound generators or intrinsic nonlinear dynamics of sound generating structures. Additionally, direct neuromuscular control could produce such rapid and precisely timed acoustic features if syringeal muscles exhibit rare superfast muscle contractile kinetics. However, no direct evidence exists that avian vocal muscles can produce modulations at such high rates. Here, we show that 1) syringeal muscles are active in phase with sound modulations during song over 200 Hz, 2) direct stimulation of the muscles in situ produces sound modulations at the frequency observed during singing, and that 3) syringeal muscles produce mechanical work at the required frequencies and up to 250 Hz in vitro. The twitch kinematics of these so-called superfast muscles are the fastest measured in any vertebrate muscle. Superfast vocal muscles enable birds to directly control the generation of many observed rapid acoustic changes and to actuate the millisecond precision of neural activity into precise temporal vocal control. Furthermore, birds now join the list of vertebrate classes in which superfast muscle kinetics evolved independently for acoustic communication.     

The neuromuscular control of birdsong.

Birdsong requires complex learned motor skills involving the coordination of respiratory, vocal organ and craniomandibular muscle groups. Recent studies have added to our understanding of how these vocal subsystems function and interact during song production. The respiratory rhythm determines the temporal pattern of song. Sound is produced during expiration and each syllable is typically followed by a small inspiration, except at the highest syllable repetition rates when a pattern of pulsatile expiration is used. Both expiration and inspiration are active processes. The oscine vocal organ, the syrinx, contains two separate sound sources at the cranial end of each bronchus, each with independent motor control. Dorsal syringeal muscles regulate the timing of phonation by adducting the sound-generating labia into the air stream. Ventral syringeal muscles have an important role in determining the fundamental frequency of the sound. Different species use the two sides of their vocal organ in different ways to achieve the particular acoustic properties of their song. Reversible paralysis of the vocal organ during song learning in young birds reveals that motor practice is particularly important in late plastic song around the time of song crystallization in order for normal adult song to develop. Even in adult crystallized song, expiratory muscles use sensory feedback to make compensatory adjustments to perturbations of respiratory pressure. The stereotyped beak movements that accompany song appear to have a role in suppressing harmonics, particularly at low frequencies.     

Sensitive period for sensorimotor integration during vocal motor learning

Sensory experience during sensitive periods in development may direct the organization of neural substrates, thereby permanently influencing subsequent adult behavior. We report a sensitive period during the imitative motor learning phase of sensorimotor integration in birdsong development. By temporarily and reversibly blocking efference to the vocal muscles, we disrupted vocal motor practice during selected stages of song development. Motor disruption during prolonged periods early in development, which allows recovery of vocal control prior to the onset of adult song, has no effect on adult song production. However, song disruption late in development, during the emergence of adult song, results in permanent motor defects in adult song production. These results reveal a decreased ability to compensate for interference with motor function when disturbances occur during the terminal stage of vocal motor development. Temporary disruption of syringeal motor control in adults does not produce permanent changes in song production. Permanent vocal aberrations in juveniles are evident exclusively in learned song elements rather than nonlearned calls, suggesting that the sensitive period is associated with motor learning.     

Airflow and pressure during canary song: direct evidence for mini-breaths

Summary Male canaries (Serinus canaria) produce songs of long duration compared to the normal respiratory cycle. Each phrase in a song contains repetitions of a particular song syllable, with repetition rates for different syllables ranging from 3 to 35 notes/s. We measured tracheal airflow and air sac pressure in order to investigate respiratory dynamics during song.Song syllables (11–280 ms) are always accompanied by expiratory tracheal airflow. The silent intervals (15–90 ms) between successive syllables are accompanied by inspiration, except for a few phrases where airflow ceases instead of reversing. Thus, the mini-breath respiratory pattern is used most often by the five birds studied and pulsatile expiration is used only occasionally.Songs and phrases accompanied by minibreaths were of longer duration than those accompanied by pulsatile expiration, presumably because the animal's finite vital capacity is not a limiting factor when the volume of air expired for one note is replaced by inspiration prior to the next. Pulsatile expiration was used for only a few syllable types from one bird that were produced at higher repetition rates than syllables accompanied by mini-breaths. We suggest that male canaries switch to pulsatile expiration only when the syllable repetition rate is too high (greater than about 30 Hz) for them to achieve mini-breaths.Changes in syringeal configuration that may accompany song are discussed, based on the assumption that changes in the ratio of subsyringeal (air sac) pressure to tracheal flow rate reflect changes in syringeal resistance.     

Partial muting leads to age-dependent modification of motor patterns underlying crystallized zebra finch song

The crystallized structure of adult zebra finch (Taeniopygia guttata) song is modifiable if sensory feedback is altered during sound production. Such song plasticity has been studied by examining acoustic modifications to the motif; however, the underlying changes to the vocal motor patterns of these acoustic modifications have not been addressed. Adult birds in two age categories (young=90-120 days or middle aged 150-250 days) that sang crystallized song were used in the experiment. Vocal motor patterns were monitored by recording respiratory air sac pressure before, during, and after song plasticity was induced by partial or complete reduction of phonation (i.e., "partial muting"). Birds were recorded until changes in air sac pressure patterns underlying the song structure were observed (up to 160 days). Young adult birds were more likely to insert shorter duration (<125 ms) expiratory pulses (EPs) into the motif than middle-aged adults. These shorter duration EPs were produced with a unique pressure pattern relative to the intact song, and therefore appeared to be generated by novel motor gestures. Stuttering (atypical repetition of an EP) was observed when these novel EPs were inserted into the motif, regardless of age. The EP of the distance call, which is also a learned vocalization in zebra finches, showed a similar reduction in duration if EPs were also shortened in the song. The emergence of shorter duration EPs was not related to sound production, or nonspecific effects of the surgical procedure, which suggests an age-dependent neural process for song plasticity.     

Bilaterally symmetrical respiratory activity during lateralized birdsong

We investigated whether activity of expiratory muscles reflects lateralized activity of the vocal organ during production of birdsong. Respiration and syringeal motor activity were assessed in brown thrashers by monitoring bilateral airflow and subsyringeal air sac pressure, together with the electromyographic activity of expiratory abdominal muscles and vocal output. Activity of expiratory muscles was always present on both sides, regardless of whether song was produced bilaterally or on only one side of the syrinx. The average amplitude of expiratory EMG of one side does not change significantly, even if that side is silent during phonation. The temporal pattern of the electromyogram (EMG) was similar on both sides. Bilateral bursts of EMG activity on both sides accompanied changes in the rate of syringeal airflow, even when these flow fluctuations were generated only by one side of the syrinx. Motor commands to the respiratory muscles therefore appear to be bilaterally distributed, in contrast to the lateralized motor control of the syrinx.     

Partial muting leads to age‐dependent modification of motor patterns underlying crystallized zebra finch song

The crystallized structure of adult zebra finch (Taeniopygia guttata) song is modifiable if sensory feedback is altered during sound production. Such song plasticity has been studied by examining acoustic modifications to the motif; however, the underlying changes to the vocal motor patterns of these acoustic modifications have not been addressed. Adult birds in two age categories (young = 90–120 days or middle aged 150–250 days) that sang crystallized song were used in the experiment. Vocal motor patterns were monitored by recording respiratory air sac pressure before, during, and after song plasticity was induced by partial or complete reduction of phonation (i.e., “partial muting”). Birds were recorded until changes in air sac pressure patterns underlying the song structure were observed (up to 160 days). Young adult birds were more likely to insert shorter duration (<125 ms) expiratory pulses (EPs) into the motif than middle‐aged adults. These shorter duration EPs were produced with a unique pressure pattern relative to the intact song, and therefore appeared to be generated by novel motor gestures. Stuttering (atypical repetition of an EP) was observed when these novel EPs were inserted into the motif, regardless of age. The EP of the distance call, which is also a learned vocalization in zebra finches, showed a similar reduction in duration if EPs were also shortened in the song. The emergence of shorter duration EPs was not related to sound production, or nonspecific effects of the surgical procedure, which suggests an age‐dependent neural process for song plasticity. © 2004 Wiley Periodicals, Inc. J Neurobiol, 2004     

Respiratory units of motor production and song imitation in the zebra finch

Juvenile male zebra finches (Taeniopygia guttata) learn a stereotyped song by imitating sounds from adult male tutors. Their song is composed of a series of syllables, which are separated by silent periods. How acoustic units of song are translated into respiratory and syringeal motor gestures during the song learning process is not well understood. To learn about the respiratory contribution to the imitation process, we recorded air sac pressure in 38 male zebra finches and compared the acoustic structures and air sac pressure patterns of similar syllables qualitatively and quantitatively. Acoustic syllables correspond to expiratory pressure pulses and most often (74%) entire syllables are copied using similar air sac pressure patterns. Even notes placed within different syllables are generated with similar air sac pressure patterns when only segments of syllables are copied (9%). A few of the similar syllables (17%) are generated with a modified pressure pattern, typically involving addition or deletion of an inspiration. The high similarity of pressure patterns for like syllables indicates that generation of particular sounds is constrained to a narrow range of air sac pressure conditions. Following presentation of stroboscope flashes, song was typically interrupted at the end of an expiratory pressure pulse, confirming that expirations and, therefore, syllables are the smallest unit of motor production of song. Silent periods, which separate syllables acoustically, are generated by switching from expiration to inspiration. Switching between respiratory phases, therefore, appears to play a dominant role in organizing the stereotyped motor program for song production.     

Mechanisms of song production in the Australian magpie

Australian magpies (Gymnorhina tibicen) are notable for their vocal prowess. We investigated the syringeal and respiratory dynamics of vocalization by two 6-month-old males, whose songs had a number of adult features. There was no strong lateral syringeal dominance and unilateral phonation was most often achieved by closing the syringeal valve on the contralateral side of the syrinx. Unlike other songbirds studied, magpies sometimes used an alternative syringeal motor pattern during unilateral phonation in which both sides of the syrinx are partially adducted and open to airflow. Also, in contrast to most other songbirds, the higher fundamental frequency during two-voice syllables was usually generated on the left side of the syrinx. Amplitude modulation, a prominent feature of magpie song, was produced by linear or nonlinear interactions between different frequencies which may originate either on opposite sides of the syrinx or on the same side. Pulse tones, similar to vocal fry in human speech, were present in some calls. Unlike small songbirds, the fundamental of the modal frequency can be as low as that of the pulse tone, suggesting that large birds may have evolved pulse tones to increase acoustic diversity, rather than decrease the fundamental frequency.     

Contributions of syringeal muscles to respiration and vocalization in the zebra finch

Acute and chronic electromyographic (EMG) recordings from individual syringeal muscles were used to study syringeal participation in respiration and vocalization. In anesthetized birds, all syringeal muscles recorded were active to some degree during the expiratory phase of respiration, following activity in the abdominal musculature and preceding the emergence of breath from the nostril. In awake birds, the ventralis (V) muscle fired a strong, consistent burst, but the dorsalis (D) was variable both in strength and timing. Denervation of V is sufficient to produce the wheezing respiration originally seen in birds with complete bilateral section of the tracheosyringeal nerve. Complete syringeal denervation also removed almost all the acoustic features that distinguish individual song syllables, but had a minor effect on the temporal structure of song. When activity in V and D was recorded in awake, vocalizing birds, D was active before and during sound production, and V showed a small burst before sound onset and a vigorous burst timed to the termination of sound. During song, V was consistently active at sound offset, but also participated during sound for narrow bandwidth syllables. For some syllables (simple harmonic stacks), neither muscle was active. These data suggest that V contributes to syllable termination during vocalization and may silence the syrinx during normal respiration. D contributes to the acoustic structure of most syllables, and V may contribute to a special subset of syllables. In summary, the syringeal muscles show different activity patterns during respiration and vocalization and can be independently activated during vocalization, depending on the syllable produced.     

Sexual dimorphism and bilateral asymmetry of syrinx and vocal tract in the European starling (Sturnus vulgaris)

Sexually dimorphic vocal behavior in zebra finches (Taeniopygia guttata) is associated with a 100% larger syrinx in males and other morphological adaptations of the sound source. The songbird syrinx consists of two independent sound sources, whose specialization for different spectral ranges may be reflected in morphological properties, but the morphology of labia and syringeal skeleton have not been investigated for lateralized specializations. Similarly, little is known whether the morphology of the songbird vocal tract reflects differences in vocal behavior. Here, we tested the hypothesis that different vocal behavior and specialization is reflected in the morphology. We investigated syringeal and upper vocal tract morphology of male and female European starlings (Sturnus vulgaris). Female starlings exhibit smaller vocal repertoires and sing at lower rates than males. In males, the left syrinx produces mostly low frequencies, while the right one is used for higher notes. Macroscopic and histological techniques were used to record nineteen measurements from the syrinx and the vocal tract which were tested for sexual differences in syrinx and vocal tract and for lateral asymmetry within the syrinx. Sexually dimorphic vocal behavior is reflected in the morphology of the starling syrinx. Males have a larger syrinx with the size difference attributable to increased muscle mass and three enlarged elements of the syringeal skeleton. The upper vocal tract, however, does not differ between males and females. Distinct lateralization was found in two elements of the syringeal skeleton of females, and the labia in the left syrinx are larger than those on the right in both sexes. The sexual dimorphism of the syringeal size is smaller in starlings (35%) than in zebra finches (100%), which is consistent with the different vocal behavior of females in both species. The morphological differences between the two sound sources are discussed in relation to their vocal performance. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

鸣禽发声器官在鸣啭过程中的功能

鸣禽的鸣啭是一种习得行为,与人类的学习过程较为相似.因此鸣禽作为一种动物模型在研究人类学习记忆方面得到广泛的应用.鸣管和鸣肌是鸣禽鸣啭的主要器官,对鸣啭过程起着复杂的调节作用.此外,不同的鸣禽在鸣啭时,其发声器官具有不同的侧别优势.对近年在鸣禽发声器官功能方面的研究进行综述.     

Song Feature Specific Analysis of Isolate Song Reveals Interspecific Variation in Learned Components

Studies of avian vocal development without exposure to conspecific song have been conducted in many passerine species, and the resultant isolate song is often interpreted to represent an expression of the genetic code for conspecific song. There is wide recognition that vocal learning exists in oscine songbirds, but vocal learning has only been thoroughly investigated in a few model species, resulting in a narrow view of birdsong learning. By extracting acoustic signals from published spectrograms, we have reexamined the findings of isolate studies with a universally applicable semi‐automated quantitative analysis regimen. When song features were analyzed in light of three different production aspects (respiratory, syringeal, and central programming of sequence), all three show marked interspecific variability in how close isolate song features are to normal. This implies that song learning mechanisms are more variable than is commonly recognized. Our results suggest that the interspecific variation shows no readily observable pattern reflecting phylogeny, which has implications for understanding the mechanisms behind the evolution of avian vocal communication. We emphasize that song learning in passerines provides an excellent opportunity to investigate the evolution of a complex, plastic trait from a phylogenetic perspective.     

The acoustic role of tracheal chambers and nasal cavities in the production of sonar pulses by the horseshoe bat, Rhinolophus hildebrandti

Summary The acoustic role of the enlarged, bony, nasal cavities and rigid tracheal chambers in the horseshoe bat,Rhinolophus hildebrandti (Fig. 2) was investigated by determining the effect of their selective filling on the nasally emitted sonar pulse and on the sound traveling backwards down the trachea.Normal sonar signals of this bat contain a long constant frequency component with most energy in the second harmonic at about 48 kHz. The fundamental is typically suppressed 20 to 30 dB below the level of the second harmonic (Fig. 1).None of the experimental manipulations described affected the frequency of the sonar signal fundamental.Filling the dorsal and both lateral tracheal chambers had little effect on the emitted vocalization, but caused the level of the fundamental component in the trachea to increase 15 to 19 dB in most bats (Table 2). When only the dorsal chamber or only the two lateral chambers were filled, the effect was less striking and more variable (Tables 3 and 4), suggesting that the tracheal fundamental is normally suppressed by acoustic interaction between these three cavities.Filling the enlarged dorsal nasal cavities had no effect on the tracheal sound. The effect of this treatment on the nasally emitted sonar pulse was inconsistent. Sometimes the fundamental increased 10 to 12 dB, other times the intensity of all harmonics decreased; in still other cases the second, third or fourth harmonic increased, but the fundamental remained unchanged (Tables 5, 6, and 7).When bats were forced to vocalize through the mouth, by sealing the nostrils, there was a prominent increase in the level of the emitted fundamental (10 to 21 dB) and in the fourth harmonic (6 to 17 dB). In one instance there was also a significant increase in the level of the third harmonic (Tables 8 and 9). The supraglottal tract thus filters the fundamental from the nasally emitted sonar signal, although the role of the inflated nasal cavities in this process is unclear.We conclude that a high glottal impedance acoustically isolates the subglottal from the supraglottal vocal tract. The tracheal chambers do not affect the emitted sonar signal, but may attenuate the fundamental in the trachea and prevent it from being reflected from the lungs back towards the cochlea. It may be important to prevent the reflected fundamental from stimulating the cochlea, via tissue conduction, along multiple indirect pathways which would temporally smear cochlear stimulation.Tracheal and nasal chambers, by suppressing the internally reflected and externally radiated components, respectively, of the laryngeal fundamental, may enable horseshoe bats to rely on the tissue-conducted fundamental as a reference or marker of its own laryngeally generated sound which could be useful in processing sonar information.     

Lateralization and motor stereotype of song production in the brown-headed cowbird

Song production in adult brown-headed cowbirds(Molothrus ater ater) is lateralized, with a slight right syringeal dominance. The left size of the syrinx produces low-frequency (200–2000 Hz) notes within the introductory note clusters, while the right side produces the higher-frequency (1500–6000 Hz) introductory notes, the interphrase unit (10–12 kHz), and the final high-frequency whistle (5–13 kHz). Cross-correlation analyses reveal that individual cowbirds produce each of their four to seven song types with a distinct stereotyped motor pattern–as judged by the patterns of syringeal airflow and subsyringeal pressure. The acoustic differences across song types are reflected in the differences in the bronchial airflow and air sac pressure patterns associated with song production. These motor differences are particularly striking within the second and third introductory note clusters where there is a rapid switching back and forth between the two sides of the syrinx in the production of notes. These motor skills may be especially important in producing behaviorally effective song. 1994 John Wiley & Sons, Inc.     

The effects of tracheal coiling on the vocalizations of cranes (Aves; Gruidae)

Summary It is generally supposed that the elongated, often coiled tracheae of many species of birds are adaptations for the production of loud, penetrating calls. A corollary supposition is that the acoustic effects are produced by the resonant properties of the elongated tube, with the birds being analogized to a wind instrument. We have experimented with several species of cranes possessing different degrees of tracheal coiling. Regardless of the degree of coiling, all cranes can utter extremely loud calls using remarkably low driving pressures. Neither surgical modifications of the trachea nor changing the respiratory gases to helium-oxygen produced consistent changes of voice that could be unambiguously attributed to changes of tubal resonances. However, shortening the trachea markedly reduced vocal intensity, the degree of reduction being roughly proportional to the degree of shortening. Although some of that reduction may derive from an increased impedance mismatch at the external aperture of the tube, and some from a decreased radiation directly from the hard walls of the trachea, these explanations scarcely account for the dramatic effects we observed. We, therefore, hypothesize a more unusual mechanism: The tracheal coils that are embedded in the sternum serve a function analogous to the bridge of a stringed instrument, transmitting the vibrations of a tiny sound source to a large radiating surface, the sternum. The sternum then vibrates against the large internal air reservoir of the avian airsac system. As it has a complex shape, the sternum will have many resonances and will respond to many frequencies; as a solid oscillator, its resonances will not be greatly affected by low density gases. Hence, we suggest that cranes and other birds with enlarged windpipes are more properly analogized with a violin than a trombone.     

Hormonal acceleration of song development illuminates motor control mechanism in canaries

In songbirds, the ontogeny of singing behavior shows strong parallels with human speech learning. As in humans, development of learned vocal behavior requires exposure to an acoustic model of species‐typical vocalizations, and, subsequently, a sensorimotor practice period after which the vocalization is produced in a stereotyped manner. This requires mastering motor instructions driving the vocal organ and the respiratory system. Recently, it was shown that, in the case of canaries (Serinus canaria), the diverse syllables, constituting the song, are generated with air sac pressure patterns with characteristic shapes, remarkably, those belonging to a very specific mathematical family. Here, we treated juvenile canaries with testosterone at the onset of the sensorimotor practice period. This hormone exposure accelerated the development of song into stereotyped adultlike song. After 20 days of testosterone treatment, subsyringeal air sac pressure patterns of song resembled those produced by adults, while those of untreated control birds of the same age did not. Detailed temporal structure and modulation patterns emerged rapidly with testosterone treatment, and all previously identified categories of adult song were observed. This research shows that the known effect of testosterone on the neural circuits gives rise to the stereotyped categories of respiratory motor gestures. Extensive practice of these motor patterns during the sensorimotor phase is not required for their expression. © 2010 Wiley Periodicals, Inc. Develop Neurobiol 70: 943–960, 2010