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.     

Effects of unilateral lesions of HVC on song patterns of male domesticated canaries

Bird song is a model for studying neural control and lateralization of a learned behavior. Adult male canary develops large and varied song repertoires. Particular features of the male are well known to stimulate the reproductive activities of the female. We report here on the effect of lesions of either the left or right HVC, a key nucleus of the descending vocal control network of songbirds, on different song parameters of common domesticated male canaries of an European outbred strain. These canaries are useful to evaluate the question of central versus peripheral lateralization because they do not show syringeal dominance for syllable production compared to the previously studied canary strains. Right-sided lesions reduced the highest frequency and the widest frequency band. Left-sided lesion increased the lowest frequency. The size of the left-sided lesions correlated with the reduction of the repertoire of simple syllables, of the total repertoire and of the highest repetition rate, and with the increase of the lowest frequency. These results suggest a lateralized specialization of both left and right vocal pathways for particular features of the song, especially those that are known to elicit a great number of copulation solicitation displays (CSD). Lesions of both left and right pathways affected, however, sound amplitude of all syllables. Because this effect was more sever following left-sided lesions, and because the syrinx morphology of canaries has a left-right asymmetry, we suggest a peripheral mechanism for the observed lateralized specializations.     

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     

Right-side dominance for song control in the zebra finch.

Adult male zebra finches underwent unilateral denervation of the syrinx or unilateral lesion of the forebrain nucleus HVC known to be important for song control. Disruptive effects on song were greater after right-side than after left-side operations. After denervation of the right half of the syrinx, the fundamental frequencies of all syllables within a song converged on a value near 500 Hz, and nearly all syllables were altered in type. In contrast, the syllables produced after denervation of the left side of the syrinx largely maintained their preoperative frequencies, and fewer syllables changed in type. Unlike nerve sections, HVC lesions did not result in strikingly lateralized effects on syllable phonology; however, HVC lesions did affect the temporal patterning of a bird's song, whereas nerve sections did not, and changes in temporal patterning were more marked after right than after left HVC lesions. Right-side dominance for zebra finch song control is the reverse of that described in other songbird species with lateral asymmetry for vocal communication. We suggest that the need for a dominant side is more important than the side of dominance.     

Right-side dominance for song control in the zebra finch

Adult male zebra finches underwent unilateral denervation of the syrinx or unilateral lesion of the forebrain nucleus HVC known to be important for song control. Disruptive effects of song were greater after right-side than after left-side operations. After denervation of the right half of the syrinx, the fundamental frequencies of all syllables within a song converged on a value near 500 Hz, and nearly all syllables were altered in type. In contrast, the syllables produced after denervation of the left side of the syrinx largely maintained their preoperative frequencies, and fewer syllables changed in type. Unlike nerve sections, HVC lesions did not result in strikingly lateralized effects on syllable phonology; however, HVC lesions did affect the temporal patterning of a bird's song, whereas nerve sections did not, and changes in temporal patterning were more marked after right than after left HVC lesions. Right-side dominance for zebra finch song control is the reverse of that described in other songbird species with lateral asymmetry for vocal communication. We suggest that the need for a dominant side is more important than the side of dominance. © 1992 John Wiley & Sons, Inc.     

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.     

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.     

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.     

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.     

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.     

Reversal of hypoglossal dominance in canaries following unilateral syringeal denervation

Summary The song of intact male canaries develops under the almost exclusive control of the left hypoglossus and left syringeal half. Section of the left hypoglossus or of its tracheosyringealis branch induces the right hypoglossus to assume a dominant control over vocal behavior. When this operation is done during the first two weeks after hatching the ensuing song is under sole right hypoglossal control; if done during the third and fourth week after hatching song develops under shared right-left hypoglossal control. In either case the quality of song is close to that of intact birds of comparable age. If the left hypoglossal innervation to the syrinx is cut when song development is already well under way (plastic song) or after stable adult song has been acquired, then the quality of song developed is markedly poorer than that of controls. From these observations we may conclude that: 1) Left or right hypoglossal dominance are not necessary for the production of normal canary song. 2) Soon after hatching either hypoglossus has the potential to assume a dominant role in song development. 3) The ability of the right hypoglossus to develop normal song decreases as birds master song under dominant left hypoglossal control. It is suggested that hypoglossal dominance and dominance reversal may provide convenient material to study neuronal changes related to the learning of new motor tasks.Abbreviations e.l. external labium - i.t.m. internal tympaniform membrane - ts tracheosyringealis Steven Green, Myron C. Baker and Timothy DeVoogd provided invaluable help on statistical analysis. Steven Green also read the text and made useful suggestions.     

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.     

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.     

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.     

Unilateral nervous control of the syrinx in java sparrows (Padda oryzivora)

Summary The syrinx of song birds contains two sound sources, the internal tympaniform membranes located one in each bronchus, that are controlled by the syringeal musculature. These muscles are innervated by the cervicalis descendens superior (CDS) branch of the hypoglossal nerve. Unilateral sections of the left CDS nerve in Java sparrows markedly disrupted tonal quality of the songs, although temporal parameters were unaltered. Bilateral CDS nerve sections caused greater disruption in frequency characteristics and temporal parameters were altered. Most birds died due to asphyxia soon after the operation. Right CDS nerve sections had much less effect, except on long whistles where extra low frequency sounds appeared, probably from the denervated right bronchus. Intact song pattern was restored within four months without re-innervation of the right syringeal musculature. This unilateral dominance in the control of the syrinx agrees with previous work and adds to the support for the two voice theory of sound production in birds (Greenewalt, 1968; Stein, 1968).Abbreviation CDS Nervus cervicalis descendens superior     

Effect of tracheosyringeal denervation on call in greenfinch (Carduelis sinica)

After sections of left or right tracheosyringeal nerve (NXIIts), greenfinches may repeat everyday calls, with no effect on temporal properties. It is suggested that either side of syrinx may produce sound alone and ipsilateral innerration of NXIIts for the syringeal muscles. After section of left NXIIts, the bird produces the vocal pattern of partial tone increase, and effects on the sound intensity and sentence length average 1.4 and 2.8 times those after section of right NXIIts, suggesting that the innervation of NXIIts has left side dominance. After bilateral section of NXIIts, the call rhythm in company with expiratory motions is 98–146 times/min, on an average, and lose all sentence types and syllable structure of normal call. But the call spectra produced by tympaniform membrane vibrations without innervation still reserve frequency components similar to the tonic frequency and harmonics of normal calls.     

Relationship between song characters and morphology in New World pigeons

We studied the pattern of variation in song characters among 16 New World pigeon species belonging to different taxonomic groups defined by morphological characters. Structural, temporal and frequency characters of the song were analysed. Principal components analyses showed that species belonging to the same taxonomic group were also grouped together by their song characters. In addition, individuals were correctly assigned into taxonomic groups by discriminant function analyses in more than 87.8% of cases. These analyses also showed that more than 87.5% of the individuals could be correctly classified by species when all song characters were included. Correct classification of individuals by species and taxonomic groups dropped when character types were analysed separately, thus showing that structural, as well as temporal and frequency characters are fundamental to define species- and group-specific identities of New World pigeon's songs. Correspondence between patterns of vocal and morphological variation found in this study can be a consequence of evolutionary changes in morphology affecting song production, as for example body size changes that constrain the syrinx to produce certain acoustic frequencies.     

The effect of syringeal deafferentation on the stimulated vocalization in the domestic chick (Gallus gallus)

The r?le of syringeal feedback on the electrically elicited vocalization in chickens (Gallus gallus) was studied. The vocalization patterns elicited by stimulating the low-threshold "calling areas" in the midbrain, was examined before and after syringeal deafferentation obtained by cutting the X-XII anastomosis on either the left and right side. The results show that section of the X-XII anastomosis on the left side produces consistently a clear-cut lowering of the threshold for vocalization and an increase of the amplitude of the individual calls with no change in the repetition rate of the call sequences. All these effects are enhanced when the contralateral anastomosis is also severed. These results show that the bilateral syringeal deafferentation does not change the overall song pattern performance, that remains stereotyped both in duration and complexity, consistent with the hypothesis that, in adult birds, stable song patterns are not dependent on peripheral sources of feedback, but are ruled by a learned central control program. However the modification of vocalization threshold and amplitude suggests the hypothesis that the syringeal feedback plays an inhibitory r?le on vocalization by modulating the excitability of the central structures involved in the vocalization activity.     

Song Learning in the Anna Hummingbird (Calypte anna)

Songs of wild male Anna hummingbirds (Calypte anna) consist of syllables grouped into phrases. Nearest neighbors tend to share similar syllable types, rhythms and syntax. Songs from different localities contain different syllable types, syntax and repetition indices. A male raised by hand in isolation produced a song consisting of highly variable syllable types of a wide frequency range. The song was simple in structure, and syllables were not grouped into phrases. Three males raised by hand as a group sang songs containing two stereotyped syllable types sung in alternating sequence and without phrase structure. These three males shared syllable types and syntax. The data from our study indicate that despite its relatively simple syrinx the Anna hummingbird learns syllable types, frequency, rhythm and syntax (as do oscines with their more complex syringes) during the song development process.