Motor dynamics of song production by mimic thrushes

In brown thrashers (Toxostoma rufum) and grey catbirds (Dumetella carolinensis) neither side of the syrinx has a consistently dominant role in song production. During song, the two sides operate independently, but in close cooperation with each other and with the respiratory muscles which are capable of adjusting expiratory effort to maintain a constant rate of syringeal airflow despite sudden changes in syringeal resistance. Phonation is frequently switched from one side of the syrinx to the other, both between syllables and within a syllable. When both sides of the syrinx produce sound simultaneously, their respective contributions are seldom harmonically related. The resulting “two-voice” syllables sometimes contain difference tones with prominent sinusoidal amplitude modulation (AM). Rarely, both sides simultaneously produce the same sound. In general, however, the frequency range of sound contributed by the right syrinx is higher than that of the left syrinx. The right syrinx is also primarily responsible for producing a rapid cyclical amplitude modulation which is a characteristic feature of some syllables. This kind of AM is generated by either repetitive brief bursts of sound from the right side that modulate the amplitude of a continuous sound arising on the left side or cyclically opening the right syrinx, allowing unmodulated expiratory air to bypass the phonating left side. 1994 John Wiley & Sons, Inc.     

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     

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.     

Syringeal specialization of frequency control during song production in the Bengalese finch (Lonchura striata domestica)

Background

Singing in songbirds is a complex, learned behavior which shares many parallels with human speech. The avian vocal organ (syrinx) has two potential sound sources, and each sound generator is under unilateral, ipsilateral neural control. Different songbird species vary in their use of bilateral or unilateral phonation (lateralized sound production) and rapid switching between left and right sound generation (interhemispheric switching of motor control). Bengalese finches (Lonchura striata domestica) have received considerable attention, because they rapidly modify their song in response to manipulations of auditory feedback. However, how the left and right sides of the syrinx contribute to acoustic control of song has not been studied.

Methodology

Three manipulations of lateralized syringeal control of sound production were conducted. First, unilateral syringeal muscular control was eliminated by resection of the left or right tracheosyringeal portion of the hypoglossal nerve, which provides neuromuscular innervation of the syrinx. Spectral and temporal features of song were compared before and after lateralized nerve injury. In a second experiment, either the left or right sound source was devoiced to confirm the role of each sound generator in the control of acoustic phonology. Third, air pressure was recorded before and after unilateral denervation to enable quantification of acoustic change within individual syllables following lateralized nerve resection.

Significance

These experiments demonstrate that the left sound source produces louder, higher frequency, lower entropy sounds, and the right sound generator produces lower amplitude, lower frequency, higher entropy sounds. The bilateral division of labor is complex and the frequency specialization is the opposite pattern observed in most songbirds. Further, there is evidence for rapid interhemispheric switching during song production. Lateralized control of song production in Bengalese finches may enhance acoustic complexity of song and facilitate the rapid modification of sound production following manipulations of auditory feedback.     

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.     

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.     

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.     

The songbird syrinx morphome: a three-dimensional, high-resolution, interactive morphological map of the zebra finch vocal organ

Background

Like human infants, songbirds learn their species-specific vocalizations through imitation learning. The birdsong system has emerged as a widely used experimental animal model for understanding the underlying neural mechanisms responsible for vocal production learning. However, how neural impulses are translated into the precise motor behavior of the complex vocal organ (syrinx) to create song is poorly understood. First and foremost, we lack a detailed understanding of syringeal morphology.

Results

To fill this gap we combined non-invasive (high-field magnetic resonance imaging and micro-computed tomography) and invasive techniques (histology and micro-dissection) to construct the annotated high-resolution three-dimensional dataset, or morphome, of the zebra finch (Taeniopygia guttata) syrinx. We identified and annotated syringeal cartilage, bone and musculature in situ in unprecedented detail. We provide interactive three-dimensional models that greatly improve the communication of complex morphological data and our understanding of syringeal function in general.

Conclusions

Our results show that the syringeal skeleton is optimized for low weight driven by physiological constraints on song production. The present refinement of muscle organization and identity elucidates how apposed muscles actuate different syringeal elements. Our dataset allows for more precise predictions about muscle co-activation and synergies and has important implications for muscle activity and stimulation experiments. We also demonstrate how the syrinx can be stabilized during song to reduce mechanical noise and, as such, enhance repetitive execution of stereotypic motor patterns. In addition, we identify a cartilaginous structure suited to play a crucial role in the uncoupling of sound frequency and amplitude control, which permits a novel explanation of the evolutionary success of songbirds.     

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.     

BIOACOUSTICS IN NEW ZEALAND AND JAPAN

Although it is highly recognisable, relatively little is known about the repertoire composition and singing behaviour of the Hermit Thrush (Catharus guttatus). To address this, we recorded spontaneously singing males in two eastern populations (Halifax, NS (n = 11) and Hancock County, ME (n = 7)) and analysed the recordings with respect to repertoire size, basic song type characteristics and song syntax. Males had song type repertoires of 7–12 song types, and no song type sharing between individuals was observed within or between populations. While frequency-related structural characteristics of the song types were the same between the populations, song type duration (especially that of the introductory note) differed significantly. The song types within each repertoire could be categorised into high and low song types based on introductory note frequency, and these song type categories also differed with respect to the amount and distribution of spectral energy. In both populations, males sang with immediate variety, never repeating the same song type consecutively, and preferentially used some song-type to song-type transitions more than others. In addition, we found correlational evidence of changes in singing behaviour (e.g., the relative use of low versus high song types) over the course of the breeding season. We discuss these findings in the context of other songbird research as well as their implications for future work examining how Hermit Thrush males utilise their songs in defending territories and attracting mates.     

Left hypoglossal dominance in the control of canary and white-crowned sparrow song

Summary The syrinx of songbirds includes two separate sound sources, the internal tympaniform membranes (ITM), which form the medial wall of each bronchus. The performance of each ITM is controlled by the muscles of that syringeal half. In the canarySerinus canarius, hypoglossal fibers reaching the syrinx via the tracheosyringealis branch of the hypoglossus are responsible for sound modulation. The muscles controlling the performance of the left syringeal half are innervated solely by the left tracheosyringealis; those controlling the right syringeal half are innervated only by the right tracheosyringealis. In the canary and white-crowned sparrow (Zonotrichia leucophrys) a great majority of song elements disappears after section of the left tracheosyringealis, yet remains intact after section of the right one. This phenomenon, earlier described in the chaffinch (Nottebohm, 1970, 1971, 1972) and confirmed in the white-throated sparrow (Lemon, 1973), has been called left hypoglossal dominance. Left hypoglossal dominance occurs in canaries with small or large song repertoires. It occurs in chronically deafened canaries that never had access to their own auditory feedback; it also occurs in birds that had the right or left cochlea removed at an early age. To this extent, left hypoglossal dominance seems to emerge in the individual as a motor phenomenon.We wish to thank Betsy Manning for all the time and effort she spent recording the song of our birds. We are also indebted to Professor Peter Marler, Rockefeller University, for letting us include in our study several birds which he reared in noise and which formed part of an earlier experiment (Marler et al., 1973). Our research was supported by NIH grant MH 18343.     

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.     

Bilateral song production in domestic canaries

We studied the mechanism of song production in the outbred common or domestic canary (Serinus canaria). The contribution that each side of the syrinx makes to song was investigated by observing the effect of unilaterally occluding the left or right primary bronchus, followed by section of the ipsilateral branch of the tracheosyringeal nerve. In other birds with a bilaterally intact vocal system we monitored airflow through each side of the syrinx, together with subsyringeal pressure, during spontaneous song. Song production by domestic canaries is not strongly lateralized as it is in the conspecific song-bred waterslager strain. Some syllables are produced entirely on the left or right side of the syrinx, whereas others contain sequential contributions from each side. Low fundamental frequencies are produced with the left syrinx and high frequencies by the right syrinx, increasing the frequency range of domestic canary song compared to that of the waterslager strain. Midrange frequencies can be generated by either side. Syllables at repetition rates below about 25 s(-1) were accompanied by minibreaths, which were usually bilateral. Unilateral minibreaths were typically on the left side. At higher syllable repetition rates, minibreaths were replaced by a respiratory pattern of pulsatile expiration. Our data show that strong unilateral dominance in song production, present in the waterslager strain, is not a trait of the species as a whole and that the pattern of song lateralization can be altered by selective breeding for particular song characteristics.     

Motor mechanisms of a vocal mimic: implications for birdsong production

The diverse vocal performances of oscine songbirds are produced by the independent but coordinated patterns of activity in muscles controlling separate sound generators on the left and right sides of their duplex vocal organ, the syrinx. Species with different song styles use the two sides of their syrinx in different ways to produce their species-typical songs. Understanding how a vocal mimic copies another species' song may provide an insight into whether there are alternative motor mechanisms for generating the model's song and what parts of his song are most difficult to produce. We show here that when a vocal mimic, the northern mockingbird, accurately copies the song of another species it also uses the vocal motor pattern employed by the model species. Deviations from the model's production mechanism result in predictable differences in the mockingbird's song. Species-specific acoustic features of the model seem most difficult to copy, suggesting that they have been exposed to the strongest selective pressure to maximize their performance.     

Atypical Song Reveals Spontaneously Developing Coordination between Multi-Modal Signals in Brown-Headed Cowbirds (Molothrus ater)

The courtship and dominance behavior of brown-headed cowbirds (Molothrus ater) consists of a multi-modal display, including song as well as postural and wing movements. The temporal sequences of the acoustic and the visual display are coordinated. In adult male cowbirds the largest wing movements of the display are synchronized with silent periods of song, but it is unknown how this coordination emerges during song development. Here we investigate how visual display features are coordinated with song by using atypical song sequence structure of isolation-reared male cowbirds. In birds with atypical song, all components of the visual display were highly similar to those of “normal” song displays, but their timing was slightly different. The number of maximal wing movement cycles of isolation-reared males was linked to the number of sound units in the song, and was therefore reduced during the abbreviated song types of isolates. These data indicate that young cowbirds do not need to be exposed to a model of the visual display during ontogeny and that there is synchronization with the temporal structure of song. A physiological link between respiratory and syringeal control of silent periods between sound units and wing movement cycles may be driving this synchronization.     

Motor stereotypy and diversity in songs of mimic thrushes

The relationship between the motor and acoustic similarity of song was examined in brown thrashers (Toxostoma rufum) and grey catbirds (Dumetella carolinensis) (family Mimidae), which have very large song repertoires and sometimes mimic other species. Motor similarity was assessed by cross correlation of syringeal airflows and air sac pressures that accompany sound production. Although most syllables were sung only once in the song analyzed, some were repeated, either immediately forming a couplet, or after a period of intervening song, as a distant repetition. Both couplets and distant repetitions are produced by distinctive, stereotyped motor patterns. Their motor similarity does not decrease as the time interval between repetitions increases, suggesting that repeated syllables are stored in memory as fixed motor programs. The acoustic similarity between nonrepeated syllables, as indicated by correlation of their spectrograms, has a significant positive correlation with their motor similarity. This correlation is weak, however, suggesting that there is no simple linear relationship between motor action and acoustic output and that similar sounds may sometimes be produced by different motor mechanisms. When compared without regard to the sequence in which they are sung, syllables paired for maximum spectral similarity form a continuum with repeated syllables in terms of their acoustic and motor similarity. The prominence of couplets in the “syntax” of normal song is enhanced by the dissimilarity of successive nonrepeated syllables that make up the remainder of the song. © 1996 John Wiley & Sons, Inc.     

Innate differences in singing behaviour of sparrows reared in isolation from adult conspecific song

Innate differences in the singing behaviour of male swamp (Melospiza georgiana) and song (M. melodia) sparrows were identified by rearing males from the egg in the laboratory under identical conditions, in complete isolation from adult conspecific song. Isolation-reared males of both species displayed several abnormal song features, including reduced numbers of notes per song, longer durations of notes and inter-note intervals, and fewer notes per syllable. Despite these and other abnormalities, many species differences emerged that matched differences in the natural singing behaviour of the two species. These included differences in song repertoire size, song duration and degrees of segmentation, numbers of notes per song, durations of notes and inter-note intervals, and several measures reflecting the organization of songs into note complexes, syllables and trills. Although learning can influence all levels of organization of the motor patterns of song in swamp and song sparrows, its contribution to the achievement of normal song behaviour appears to be most crucial at the level of the fine structure of the notes and syllables from which the songs are constructed.     

Lateralization of syringeal function during song production in the canary

The canary (Serinus canaria) vocal organ, the syrinx, has two separate sound sources, one in the cranial end of each bronchus. Previous investigations of whether song syllables are produced unilaterally or bilaterally have provided two contradictory results, as one researcher suggested that almost all syllables are produced by the left side of the syrinx alone, whereas another researcher suggested that both sides contribute similarly to all syllables. Our experiments, which involved unilateral bronchus plugging followed later by denervation of the ipsilateral syringeal muscles, attempted to resolve this disagreement. The males with right bronchus plugs, singing on the left side of the syrinx alone, produced nearly normal songs, whereas the birds with left bronchus plugs, singing on the right side, sang quite poorly. Interpretation of these data is difficult because it is not clear how syringeal function would be affected if the airflow rate through the intact side is increased above normal, nor is it known if the bird can compensate for bronchus occlusion. Nonetheless, we suggest that in male canaries most syllables are normally sung by the left side alone, with some syllables being produced by the right side alone and some being sung by both sides together. Right nerve section had little effect on the right-bronchus-plugged males' ability to sing, but the repertoires of the left-plugged males were altered after left nerve section, indicating the possibility that signals carried by the left nerve exert an influence on the contralateral side.     

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.     

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