Fig 5 - uploaded by Ole Næsbye Larsen
Content may be subject to copyright.
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
... 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 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.
... 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.
... Several previous studies have reported surgical procedures to devocalize birds, but they are either technically difficult (Cooper and Goller, 2004) or unsuitable for long-term devocalization (Pytte and Suthers, 1999). The current protocol describes a novel method for devocalizing female zebra finches using tubing inserted into the bronchi to prevent adduction of the lateral labia into the expiratory air stream that is responsible for phonation (Goller and Larsen, 1997;Larsen and Goller, 2002). This method enables us to devocalize birds almost permanently without great technical difficulties. ...
Songbirds, such as the zebra finch, are a popular animal model for studying the neural basis of vocal and complex skill learning. Adult male zebra finches produce courtship song toward females (referred to as 'directed song') and recording and analyzing sounds of directed song along with underlying neural activity is important for investigating behavioral and neural mechanisms of song production and learning. However, recording of directed song is easily contaminated by calls that are often as loud as directed songs and frequently produced by a female bird is presented in the same sound-recording chamber to elicit directed song. We developed a new surgical procedure to relatively easily and almost completely devocalize female zebra finches semi-permanently, without affecting other behaviors. This procedure enables researchers to record directed songs with almost no contamination by female calls. The procedure can also be used to devocalize male birds as well and, thus, has great potential for a variety of experimental purposes, such as long-term elimination of auditory feedback during singing in male birds.
... In songbirds, there are an additional six pairs of internal muscles. The additional muscles affect the tension of the membranes as well as their location and the aperture at the tracheobronchial junction (Larsen and Goller 2002). This arrangement allows fine control of the syrinx for the generation of a rich set of sounds that vary not only in fundamental frequency but also in pitch saliency and in the shape of the spectral envelope (Sitt et al. 2008). ...
Oscines learn to produce a complex vocalization, the song, which they copy from a conspecific as young birds. The song is an attractive and conspicuous acoustic signal with striking spectral and temporal complexity. The oscine song copying behavior is also remarkable because vocal imitation is a relatively rare ability in vertebrates and because none of the nonavian species can outperform the best oscine mimics. Studies of the neurobiology of song learning have unraveled many of the mechanisms involved in this impressive vocal behavior. Song, however, is only one of the many vocalizations that are produced by oscines. The vocal repertoire of oscines is impressive not only because of the number of vocalizations produced but also because of the flexible production and usage of these sounds. This chapter reviews the vocal behavior of oscines in the framework of animal communication and examines the mechanisms underlying the production and perception of all vocalization types. The chapter also reviews how the auditory system and vocal and social brain networks might be connected to generate appropriate responses to communication calls and song. As a whole, this chapter argues that studies of the mechanisms underlying song learning and also the mechanisms underlying call plasticity, production, and perception are critical for understanding the neuroethology of vocal communication in oscines. Embracing the complexity of the vocal communication system of oscines will enhance our understanding of the brain areas that, until now, have mostly been studied in the context of song imitation.
... Endoscopic observations combined with vibration detection suggest that the avian sound generating mechanism is a pulse-tone mechanism similar to that in the human larynx (Larsen et al., 2006). Recent studies (Larsen & Goller, 2002;Gaban-lima & Höfling, 2006;Larsen et al., 2006) reported that good models for phonation researches in mammals are lacking and the syrinx of domestic birds can be used as an ideal experimental model for phonation researches as it is easily available and inexpensive. ...
... The extrinsic muscles are sternotrachealis (ST) and tracheolateralis (TL). The intrinsic muscles are confined to singing birds, humming birds, and parrots (Koch, 1973;Seller, 1987;Konig & Liebich, 2001;Larsen & Goller, 2002). The membranes are activated by the syringeal muscles during phonation (Suthers, 2001;Frank et al., 2006). ...
Many studies have been carried out to investigate the morphological structure of the syrinx in many bird species. However, the cellular organization of the syrinx in the fowls and pigeons is still unclear. The current study revealed that in fowl and pigeon, the syrinx is formed of three main parts including tympanum (cranial) part, intermediate syringeal part, and bronchosyringeal (caudal) part, in addition to pessulus and tympaniform membranes. A great variation in the structural characteristics of syrinx of fowl and pigeon was recorded. In fowl, the tympaniform membranes showed a characteristic distribution of elastic and collagen fibers which increase the elasticity of tympaniform membranes. Moreover, the bony pessulus helps the medial tympaniform membranes to be stiffer, vibrate more strongly so that louder sound will be generated. In pigeon, the lateral tympaniform membrane is of greater thickness so that the oscillation of this membrane is reduced and the amplitude is lower. Moreover, the pessulus is smaller in size and is formed mainly of connective tissue core (devoid of cartilaginous or bony plates), resulting in the failure of stretching and vibrating of the medial tympaniform membranes, that leads to the generation of deeper sound. Electron microscopic examination of the syringes of fowls and pigeons revealed numerous immune cells including dendritic cells, plasma cells, mast cells, and lymphocytes distributed within syringeal mucosa and invading the syringeal epithelium. Telocytes were first recorded in the syrinx of fowls and pigeons in this study. They presented two long telopodes that made up frequent close contacts with other neighboring telocytes, immune cells, and blood capillaries.
... occupied (e.g., Fine, Malloy, King, Mitchell, & Cameron, 2001;Fitch, 2006;Ladich & Bass, 2003;Larsen & Goller, 2002). Conversely, most reptiles and amphibians lack vocal folds or a syrinx and are considered silent. ...
Numerous chameleon species possess an out‐pocketing of the trachea known as the gular pouch. After surveying more than 250 specimens, representing nine genera and 44 species, we describe two different morphs of the gular pouch. Species of the genera Bradypodion and Chamaeleo, as well as Trioceros goetzei, all possess a single gular pouch (morph one) formed from ventral expansion of soft tissue where the larynx and trachea meet. Furcifer oustaleti and F. verrucosus possess from one to four gular pouches (morph two) formed by the expansion of soft tissue between sequential hyaline cartilage rings of the trachea. In T. melleri, examples of both morphs of the gular pouch were observed. Morphometric data are presented for 100 animals representing eight species previously known to possess a gular pouch and two additional species, B. thamnobates and B. transvaalense. In the species with the absolutely and relatively largest gular pouch, C. calyptratus, a significant difference was found between sexes in its width and volume, but not its length. In C. calyptratus, we show that an inflated gular pouch is in contact with numerous hyoid muscles and the tongue. Coupled with the knowledge that C. calyptratus generates vibrations from the throat region, we posit that the tongue (M. accelerator linguae and M. hyoglossus) and supporting hyoid muscles (i.e., Mm. sternohyoideus profundus et superficialis and M. mandibulohyoideus) are involved in the production of vibrations to produce biotremors that are amplified by the inflated gular pouch and used in substrate‐borne communication.
... The location of lateral tympani form membrane in this investigation was the same with Myers [26] Bell and Freeman [43] as well as Meclelland [27] similar location also reported in ostriches [19] singing birds [32] and turkeys [15,17]. While different locations were reported in some birds such as; it was extended between the third and fourth tracheosyringeal rings as in pigeons [14,27,44] located between first and second bronchosyringeal half-rings as in sea gulls [2,33] and long legged buzzards [23]. The inward curve of that membrane which gave the syrinx its characteristic appearance was also recorded by King and Mclelland and Nickel et al. [3,34]. ...
Birds are considered a good model for studying the phonation process, the syrinx is a vocal organ in birds. The purpose
of this study is to investigate the topographical and morphological characteristics of syrinx of male domestic
fowl. In the current study we use the syringes of seven adult males. The study shows that the syrinx of investigated
birds is tracheobronchial in type. It consists of; tympanum, tracheosyringeal and bronchosyringeal groups. In addition,
there are interbronchial ligament (brachidesm), lateral and medial vibrating membranes as well as the pessulus
at the tracheal bifurcation. Tympanum part forms the first part of the syrinx; it is formed of four tracheal rings.
The tracheosyringeal part is located at the point of tracheal bifurcation just below the tympanum. It is formed of
four highly modified incomplete tracheal rings. The bronchosyringeal part is formed of first three pairs of bronchial
half-rings. The current study was presented the detailed morphological characteristics of syrinx in male domestic
