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The cockatiel syrinx is situated at the distal end of the trachea cranial to the bronchi. (A) Schematic external ventral view of the cockatiel syrinx depicting the syringeal muscles and the inserted angioscope. Note the slightly asymmetric m. sternotrachealis (ST). (B) Schematic left-side view illustrating the extent of the paired protrusions (PP). (C) Schematic horizontal section through the cockatiel syrinx with the approximate position and field of view of the angioscope (yellow light) in Figs 6a–f and 7. SP, m. syringealis profundus; SS, m. syringealis superficialis; BC, bronchial cartilage; T, trachea; TL, m. tracheolateralis; TY, tympanum (consisting of four closely apposed or fused tracheosyringeal cartilages); LTM, lateral tympaniform membrane.
Source publication
The role of syringeal muscles in controlling the aperture of the avian vocal organ, the syrinx, was evaluated directly for the first time by observing and filming through an endoscope while electrically stimulating different muscle groups of anaesthetised birds.
In songbirds (brown thrashers, Toxostoma rufum, and cardinals, Cardinalis cardinalis),...
Contexts in source publication
Context 1
... frequency of the sound generated and closely parallels frequency modulation (Goller and Suthers, 1996a). Investigations of the parrot syrinx have suggested that the intrinsic muscles, m. syringealis superficialis and m. syringealis profundus, are arranged as antagonists, whose action narrows and widens the syringeal lumen, respectively (see Fig. ...
Context 2
... (the antagonists m. sternotrachealis and m. tracheolateralis). Electrode placement paralleled recording electrode sites in Goller and Suthers (1996a). In cockatiels, the m. syringealis superficialis was stimulated close to its caudal insertion on the bronchus to avoid simultaneous activation of the closely apposed m. syringealis profundus (see Fig. 5). Stimulation of syringeal muscles took place during quiet respiration. In two individual songbirds, the tracheosyringeal branch of the left hypoglossal nerve was resected to eliminate spontaneous respiratory activity, which tended to obscure the muscle-stimulation- induced labial movements on that ...
Context 3
... from published descriptions of the syrinx in other Psittaciformes, we include a section on morphology following the nomenclature of King (1989). In the cockatiel syrinx, we observed and stimulated three pairs of muscles: the extrinsic m. sternotrachealis (ST) and the intrinsic m. syringealis superficialis (SS) and m. syringealis profundus (SP) (Fig. 5). M. tracheolateralis (TL) is a very thin muscle, and its caudal insertion point could not be determined accurately (as in some other parrots) ( Gaunt and Gaunt, 1985a;King, ...
Context 4
... intrinsic muscles, SS and SP, are closely apposed (Fig. 5A,C). The SS attaches cranially to the dorso-lateral sides of the tympanum (King, 1989), formed by fusion of 4-5 ossified tracheosyringeal cartilages. From here, the SS arches latero-caudally to insert on tracheosyringeal cartilages ...
Context 5
... 1989). Endoscopic views of the syrinx through the trachea further suggest that the LTMs are folded into the tracheal lumen along their dorso-ventral axis ( Figs 5C, 6), which is the result of the close proximity of the cartilages on which they insert. The cranial edge of each LTM is defined by a paired ossified half-ring structure that protrudes dorsally and ventrally from the tube-like trachea to form a dorsal and a ventral protrusion (PP in Figs 5 and 6g-i). ...
Context 6
... Figs 5 and 6g-i). Each of these structures is cranially hinged to the ossified tympanum by a highly flexible ligament. The deep syringeal muscle, SP, is partly hidden underneath the SS. The SP attaches cranially to the lateral side of the caudal part of the tympanum while, caudally, it inserts along most of the length of the ipsilateral PP (see Fig. 5B,C). This arrangement gives the SP the shape of an isosceles triangle with the obtuse angle at the tympanum and the acute angles at the dorsal and ventral ...
Context 7
... was difficult to place the stimulating electrodes in the SS such that only this muscle was activated. When electrodes were placed near the syringeal insertion point on the tympanum (see Fig. 5C), both the SS and the SP contracted. The result was an initial adductive movement of the ipsilateral LTM, which was immediately overridden by abduction. When the electrodes were placed in the SS near its bronchial insertion (i.e. farthest from the SP), stimulation caused contraction of the SS without also activating the SP. ...
Context 8
... line outlines the medial edges of the median tympaniform membrane). B, bronchial cartilage; vS, m. syringealis ventralis; vTB, m. tracheobronchialis ventralis. Direct observation of syrinx muscles intensities only the dorsal part moved into the lumen. This observation is in agreement with the insertion of the SS on the dorsal side of the bronchus (Fig. 5A,B). The dorso-ventrally asymmetrical configuration makes it likely that even relatively weak contraction of the SS will mainly influence the dorsal side of the slit as it folds the LTMs into the tracheal ...
Context 9
... of the SP always produced a clear and vigorous abduction of the ipsilateral LTM (Fig. 6d-f). In contrast to adduction, no dorso-ventral asymmetry of LTM movements along the slot was observed. This is not surprising since there is no dorso-ventral asymmetry in origin and insertion of the SP (see Fig. 5B). Contraction of the SP moves the protruding ossified half-ring in a craniolateral direction, but does not generate a significant rotation of the cartilage. This is illustrated by the striking lateral displacement of the left ventral PP (Fig. ...
Context 10
... visible mechanical arrangement of cartilages present a less complicated biomechanical system than that of the songbird syrinx. The attachment of the SS on the bronchi suggests that adduction is achieved by shortening the rostro-caudal distance between the two cartilages on which the LTMs insert, thus folding the LTMs into the syringeal lumen (see Fig. 5C) (Nottebohm, 1976;Gaunt and Gaunt, 1985a). As suggested by the present observations, this action is dorsally biased and, in addition, may also be refined by ST activity, similar to the effect of the ST in the simpler syrinx of the pigeon (Goller and Larsen, ...
Context 11
... characteristic shape of the paired ossified half-ring structures (PP) (Fig. 5) with the well-defined insertion areas of the SP suggested that abduction is achieved by pulling the cartilage laterally (Nottebohm, 1976;Gaunt and Gaunt, 1985a). The extent of the rostro-lateral movement of the ventral (see Fig. 6g-i) protrusions of the cartilage illustrates the swinging motion and confirms earlier ...
Citations
... Indeed, enhanced tongue control during vocalization may be essential to the complex acoustics of parrot vocalizations [94], since parrots, like humans, have just a single sound source, in contrast to songbirds who have two sources. This is because the parrot syrinx, like the human larynx, has vibrating membranes above the splitting of the bronchi from the trachea, whereas songbirds have separate syringeal membranes below this split, within each of their two bronchi [95]. ...
Dancing to music is ancient and widespread in human cultures. While dance shows great cultural diversity, it often involves nonvocal rhythmic movements synchronized to musical beats in a predictive and tempo-flexible manner. To date, the only nonhuman animals known to spontaneously move to music in this way are parrots. This paper proposes that human-parrot similarities in movement to music and in the neurobiology of advanced vocal learning hold clues to the evolutionary foundations of human dance. The proposal draws on recent research on the neurobiology of parrot vocal learning by Jarvis and colleagues and on a recent cortical model for speech motor control by Hickock and colleagues. These two lines of work are synthesized to suggest that gene regulation changes associated with the evolution of a dorsal laryngeal pitch control pathway in ancestral humans fortuitously strengthened auditory-parietal cortical connections that support beat-based rhythmic processing. More generally, the proposal aims to explain how and why the evolution of strong forebrain auditory-motor integration in the service of learned vocal control led to a capacity and proclivity to synchronize nonvocal movements to the beat. The proposal specifies cortical brain pathways implicated in the origins of human beat-based dancing and leads to testable predictions and suggestions for future research.
... Additionally, the behavioral training task used in the present study, because it was based on the overall acoustic structure of the syllable and not on a single acoustic parameter, can be considered as probably more complex or difficult for the birds than the pitch-shifting behavioral task. The fundamental frequency may only be controlled by one set of muscles surrounding the syrinx (Larsen and Goller, 2002;Goller and Riede, 2013). To maintain all the acoustic parameters of a given syllable, it is likely that a greater number of muscles need to be controlled. ...
Human language learning and maintenance depend primarily on auditory feedback but are also shaped by other sensory modalities. Individuals who become deaf after learning to speak (post-lingual deafness) experience a gradual decline in their language abilities. A similar process occurs in songbirds, where deafness leads to progressive song deterioration. However, songbirds can modify their songs using non-auditory cues, challenging the prevailing assumption that auditory feedback is essential for vocal control. In this study, we investigated whether deafened birds could use visual cues to prevent or limit song deterioration. We developed a new metric for assessing syllable deterioration called the spectrogram divergence score. We then trained deafened birds in a behavioral task where the spectrogram divergence score of a target syllable was computed in real-time, triggering a contingent visual stimulus based on the score. Birds exposed to the contingent visual stimulus - a brief light extinction - showed more stable song syllables than birds that received either no light extinction or randomly triggered light extinction. Notably, this effect was specific to the targeted syllable and did not influence other syllables. This study demonstrates that deafness-induced song deterioration in birds can be partially mitigated with visual cues.
... In contrast, parrots do not have this independent control over the syrinx' muscles and thus lack this biphonation ability (22)(23)(24). Moreover, songbirds and parrots also differ in the neurological structures underlying vocal production learning (25). ...
... In contrast, parrots lack the independent control of these labia at both sides of the syrinx. Therefore, parrots lack the biphonation ability that starlings have (22)(23)(24). Differences in perception or cognitive abilities can therefore be excluded as explanation for the observed differences in imitation accuracy since starlings did not differ in how accurate they imitated monophonic sounds from parrots. ...
Vocal production learning is a widespread and remarkable phenomenon. However, the underlying mechanisms of allospecific vocal imitation are poorly understood. Parrots and corvids are well known for their imitation abilities, but imitation accuracy has not yet been studied across species in a comparative context. We compared imitation accuracy between nine parrot species and
European starlings based on imitation of monophonic and multiphonic sounds, produced by the Star Wars droid R2-D2. Our results show that starlings were better at imitating multiphonic sounds than parrots. However, no difference in imitation accuracy was found between parrots and starlings
when imitating monophonic sounds. The differences in imitating accuracy are likely based on a physiological difference in syrinx anatomy, rather than on perceptual or cognitive differences between starlings and parrots. Between our nine tested parrot species, we found that parrots with larger brains (e.g., African greys and amazon parrots) were less accurate at imitating monophonic
sounds than smaller brained budgerigars and cockatiels. The use of citizen science in our study shows the great potential this has to expand data collection beyond traditional studies. These findings contribute to a deeper understanding of the evolution of communication complexity in vocal learners.
... Unlike songbirds, that produce their vocalization using two relatively independent syringeal sound sources, parrots have only one sound source and modulate their vocalizations using trachea, tongue and beak. This is very similar to how humans produce the sounds that make up words [63][64][65][66][67][68][69][70]. This modulation or filtering by the vocal tract allows for many more individual-specific features to arise and make a voice-print more recognizable. ...
In humans, identity is partly encoded in a voice-print that is carried across multiple vocalizations. Other species also signal vocal identity in calls, such as shown in the contact call of parrots. However, it remains unclear to what extent other call types in parrots are individually distinct, and whether there is an analogous voice-print across calls. Here we test if an individual signature is present in other call types, how stable this signature is, and if parrots exhibit voice-prints across call types. We recorded 5599 vocalizations from 229 individually marked monk parakeets (Myiopsitta monachus) over a 2-year period in Barcelona, Spain. We examined five distinct call types, finding evidence for an individual signature in three. We further show that in the contact call, while birds are individually distinct, the calls are more variable than previously assumed, changing over short time scales (seconds to minutes). Finally, we provide evidence for voice-prints across multiple call types, with a discriminant function being able to predict caller identity across call types. This suggests that monk parakeets may be able to use vocal cues to recognize conspecifics, even across vocalization types and without necessarily needing active vocal signatures of identity.
... In order to sing, the bird activates syringeal muscles that rotate the third cartilage in such a way as to be carried inward. In this way, the lateral labia are positioned in the bronchial lumen in a 'pre-phonatory' position (Goller and Larsen, 1997;Suthers et al., 1999;Larsen and Goller, 2002;Fig. 1D). ...
Vocal behavior plays a crucial evolutionary role. In the case of birds, song is critically important in courtship, male-male competition and other key behaviors linked to reproduction. However, under natural conditions, a variety of avian species live in close proximity and share an 'acoustic landscape'. Therefore, they need to be able to differentiate their calls or songs from those of other species and also from those of other individuals of the same species. To do this efficiently, birds display a remarkable diversity of sounds. For example, in the case of vocal learners, such as oscine passerines (i.e. songbirds), complex sequences and subtle acoustic effects are produced through the generation of complex neuromuscular instructions driving the vocal organ, which is remarkably conserved across approximately 4000 oscine species. By contrast, the majority of the sister clade of oscines, the suboscine passerines, are thought not to be vocal learners. Despite this, different suboscine species can generate a rich variety of songs and quite subtle acoustic effects. In the last few years, different suboscine species have been shown to possess morphological adaptations that allow them to produce a diversity of acoustic characteristics. Here, we briefly review the mechanisms of sound production in birds, before considering three suboscine species in more detail. The examples discussed in this Review, integrating biological experiments and biomechanical modeling using non-linear dynamical systems, illustrate how a morphological adaptation can produce complex acoustic properties without the need for complex neuromuscular control.
... In birds, however, the larynx is not directly associated with sound production [2]. The syrinx, a vibrating organ specific to birds [3][4][5][6][7][8][9][10][11], produces a primary sound, subsequently filtered by the rest of the vocal tract. Because the syrinx is located near the base of the trachea, several structures, potentially involved in sound filtering [12], need to be crossed before the final sound exits: the trachea, the larynx, through its opening (i.e. the glottis), the beak, with a possible effect of tongue's position. ...
Despite the complex geometry of songbird's vocal system, it was typically modelled as a tube or with simple mathematical parameters to investigate sound filtering. Here, we developed an adjustable computational acoustic model of a sparrow's upper vocal tract ( Passer domesticus ), derived from micro-CT scans. We discovered that a 20% tracheal shortening or a 20° beak gape increase caused the vocal tract harmonic resonance to shift toward higher pitch (11.7% or 8.8%, respectively), predominantly in the mid-range frequencies (3–6 kHz). The oropharyngeal-oesophageal cavity (OEC), known for its role in sound filtering, was modelled as an adjustable three-dimensional cylinder. For a constant OEC volume, an elongated cylinder induced a higher frequency shift than a wide cylinder (70% versus 37%). We found that the OEC volume adjustments can modify the OEC first harmonic resonance at low frequencies (1.5–3 kHz) and the OEC third harmonic resonance at higher frequencies (6–8 kHz). This work demonstrates the need to consider the realistic geometry of the vocal system to accurately quantify its effect on sound filtering and show that sparrows can tune the entire range of produced sound frequencies to their vocal system resonances, by controlling the vocal tract shape, especially through complex OEC volume adjustments.
... The infrahyoid muscles are external laryngeal and tracheal muscles, 22 which are particularly well developed in singing birds. 23 In the AS chimeras, both QH1-positive and -negative iASCs existed in the infrahyoid muscles ( Figure 1O-R). ...
Background
The somatopleure serves as the primordium of the amnion, an extraembryonic membrane surrounding the embryo. Recently, we have reported that amniogenic somatopleural cells (ASCs) not only form the amnion but also migrate into the embryo and differentiate into cardiomyocytes and vascular endothelial cells. However, detailed differentiation processes and final distributions of these intra‐embryonic ASCs (hereafter referred to as iASCs) remain largely unknown.
Results
By quail‐chick chimera analysis, we here show that iASCs differentiate into various cell types including cardiomyocytes, smooth muscle cells, cardiac interstitial cells, and vascular endothelial cells. In the pharyngeal region, they distribute selectively into the thyroid gland and differentiate into vascular endothelial cells to form intra‐thyroid vasculature. Explant culture experiments indicated sequential requirement of fibroblast growth factor (FGF) and vascular endothelial growth factor (VEGF) signaling for endothelial differentiation of iASCs. Single‐cell transcriptome analysis further revealed heterogeneity and the presence of hemangioblast‐like cell population within ASCs, with a switch from FGF to VEGF receptor gene expression.
Conclusion
The present study demonstrates novel roles of ASCss especially in heart and thyroid development. It will provide a novel clue for understanding the cardiovascular development of amniotes from embryological and evolutionary perspectives.
... Whereas most song is under active neural control, there has been a growing interest in a different class of nonlinear vocalizations consisting of frequency jumps, sub-harmonics, bi-phonation and deterministic chaos that are also present in the vocal repertoires of many vertebrates and birds. Several sets of tracheobronchial and syringeal muscles are involved in the phonation/vocalization processes of the birds [9]. These are the tracheobronchialis ventralis muscle and tracheolateralis muscle associated with active abduction, tracheolateralis dorsalis muscle and syringealis dorsalis muscle regulating airflow through the syrinx and consistently activated during ipsilateral closing of the syrinx or increasing syringeal resistance, suggesting that their main role is adduction. ...
... Sternotrachealis muscle is most prominent during rapid changes in the rate of airflow or when switching between expiratory and inspiratory flow, suggesting a role in stabilizing the syringeal framework. Syringealis ventralis which does not appear to contribute directly to gating of airflow and its activity is not consistently correlated with active changes in syringeal resistance [9]. The contraction of the dorsal muscles, syringealis dorsalis muscle and tracheobronchialis dorsalis muscle, constricts the syringeal lumen and thus reduces airflow by adducting connective tissue masses; the medial and lateral labia [9]. ...
... Syringealis ventralis which does not appear to contribute directly to gating of airflow and its activity is not consistently correlated with active changes in syringeal resistance [9]. The contraction of the dorsal muscles, syringealis dorsalis muscle and tracheobronchialis dorsalis muscle, constricts the syringeal lumen and thus reduces airflow by adducting connective tissue masses; the medial and lateral labia [9]. ...
The anatomical structure of phonation in the domestic chicken Gallus gallus (red jungle fowl, forma domestica) of both sexes was studied to determine sex variations in structures. Ten (10) birds, involving 5 males and 5 females were obtained from a local market for student demonstrations and used for this study. Tracheal rings were observed to be made of circular cartilages numbering thirty and above with the distal most (1/5) tracheal rings narrowed, calcified and fused as the tympanum making part of the Syrinx. The rings become calcified and somewhat collapsed through the bronchial bifurcations. When squeezed, the trachea collapsed completely between fingers but could at releasing the fingers be raised up due to elastic components separating the rings from one another. Other structures involved in vocalization includes straps of muscles. Male structures involved in respiration and vocalization were well formed compared to those of the female. Both tracheobronchialis lateralis and ventralis muscles were thicker than those of the female. Male tracheobronchialis ventralis and dorsalis muscles were well formed and spindle shaped. However, the female tracheobronchialis muscles were seen to be wider compared to the male. The vocal organs (voice box) were seen to be arbitrarily triangular in structure at the bifurcation of the trachea in both sexes. The male Syringeal walls were thinner and were seen to have marked inter Pessula space. The Pessulus mark an abrupt change from the circular trachea to strongly elliptical entrances to the bronchi. It was concluded that the differences in the thinness of syringeal walls coupled with differences between the males and females in other tracheal muscles might be responsible for the stronger vocalization in the male.
... Indian ringneck parrots are 37-42 cm long including the tail length of 15-18 cm (refs 5, 6) and weighs around 120-140 g. Syrinx of parrots, the sound-initiating organ, consists of a pair of vibrating membranes; it is simple compared to the syrinx of other birds 9 . Parrots can modulate their tongue, enabling them to produce a variety of sound signals of varying spectral content 10,11 . ...
Speech signal is a natural means of communication. It uses small units of sound to convey feelings and messages. Birds also use sound signals to express their emotions. Some birds, like parrots and crows, are capable of imitating the speech of other animals. The aim of this study is to compare the imitating capabilities of these birds with those of human beings. The software COMSOL Multiphysics has been used for investigating the effect of dimensional modifications of the vocal tract on the system output. The analysis of the results shows that the acoustic spaces used by human beings, parrots and crows are not overlapping, but similar in shape. Further, maximum formant scattering is observed in human beings and minimum for parrots. The results may be important for understanding the vocal tract modulation, for example, to generate artificial food calls to assemble the birds for feeding medicines to avoid spread of diseases, specifically by parrots and crows as they try to settle down near human civilizations.
... The present results revealed that the syrinx of budgerigar is formed by the tympanum (cranial) part and bronchosyringeal (caudal) part, in addition to the lateral tympaniform membranes. As recorded in our investigation in budgerigars, the intermediate syringeal part is not recognized grossly and histologically (Nottebohm, 1976;Larsen & Goller, 2002;Gaban-lima & Höfling, 2006) in the syrinx of the Psittacidae. ...
... Additionally, the last (sixth) tracheal ring in the syrinx of budgerigar is divided into a pair of semi-rings called tympanic plates, each tympanic plate has two protrusions dorsally and ventrally extended out of its caudal edge known as tympanum processes. A similar observation was also recorded by Gaunt & Gaunt (1985a, 1985b, Larsen & Goller (2002), as well as Gaban-lima & Höfling (2006) in the syrinx of the Psittacidae, which indicated that the syrinx has general characters within this group. ...
The syrinx is the main source for phonation in birds, its function is analogous to the mammalian larynx. Birds have both a larynx and a syrinx, but they use only the latter to vocalize. The objective of this work to give a detailed description of the anatomical, histological, and ultrastructural of syrinx in male budgerigars as a model of a passerine bird. The syrinx in the current study was to be found as a tracheobronchial type, it consists of cranial (tympanum) part and caudal (bronchosyringeal) part and, additionally, there are lateral vibrating membranes. The tympanum is formed of the last six tracheal rings, histologically its lamina epithelialis is a pseudostratified ciliated columnar epithelium with goblet cells and interrupted by intraepithelial glands. The secretory acini appear oval and lined by pyramidal secretory cells. The lamina propria–submucosa contain numerous blood capillaries, immune cells, and telocytes (TCs). The electron microscopic examination revealed numerous blood capillaries surrounded by fibroblasts and numerous immune cells, including mast cells and wandering leukocytes, within the tympanum mucosa. Hence, this study provides a detailed knowledge about the syrinx in male budgerigars.
