Frequency Modulation During Song in a Suboscine Does Not Require Vocal Muscles
01 May 2008-Journal of Neurophysiology (American Physiological Society)-Vol. 99, Iss: 5, pp 2383-2389
TL;DR: This work investigates sound production and control of sound frequency in the Great Kiskadee by recording air sac pressure and vocalizations during spontaneously generated song and assumes a nonlinear restitution force for the oscillating membrane folds in a two mass model of sound production to reproduce the frequency modulations of the observed vocalizations.
Abstract: The physiology of sound production in suboscines is poorly investigated. Suboscines are thought to develop song innately unlike the closely related oscines. Comparing phonatory mechanisms might therefore provide interesting insight into the evolution of vocal learning. Here we investigate sound production and control of sound frequency in the Great Kiskadee (Pitangus sulfuratus) by recording air sac pressure and vocalizations during spontaneously generated song. In all the songs and calls recorded, the modulations of the fundamental frequency are highly correlated to air sac pressure. To test whether this relationship reflects frequency control by changing respiratory activity or indicates synchronized vocal control, we denervated the syringeal muscles by bilateral resection of the tracheosyringeal nerve. After denervation, the strong correlation between fundamental frequency and air sac pressure patterns remained unchanged. A single linear regression relates sound frequency to air sac pressure in the intact and denervated birds. This surprising lack of control by syringeal muscles of frequency in Kiskadees, in strong contrast to songbirds, poses the question of how air sac pressure regulates sound frequency. To explore this question theoretically, we assume a nonlinear restitution force for the oscillating membrane folds in a two mass model of sound production. This nonlinear restitution force is essential to reproduce the frequency modulations of the observed vocalizations.
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TL;DR: A growing number of studies ask whether and how bird songs vary between areas with low versus high levels of anthropogenic noise as discussed by the authors and find that birds are seen to sing at higher frequencies in urban versus rural populations, presumably because of selection for higher-pitched songs in the face of low-frequency urban noise.
196 citations
Cites background from "Frequency Modulation During Song in..."
...A strong correlation between subsyringeal pressure and vocalization frequencywas also found in a suboscine bird, the great kiskadee, Pitangus sulphuratus (Amador et al. 2008), providing further evidence that driving pressure and frequency are biomechanically linked....
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TL;DR: The results show that the syringeal skeleton is optimized for low weight driven by physiological constraints on song production, and 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.
Abstract: 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. 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. 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.
187 citations
TL;DR: The HVC precisely encodes vocal motor output through activity at the times of extreme points of movement trajectories, and it is proposed that the sequential activity of HVC neurons is used as a 'forward' model, representing the sequence of gestures in song to make predictions on expected behaviour and evaluate feedback.
Abstract: Quantitative biomechanical models can identify control parameters that are used during movements, and movement parameters that are encoded by premotor neurons. We fit a mathematical dynamical systems model including subsyringeal pressure, syringeal biomechanics and upper-vocal-tract filtering to the songs of zebra finches. This reduces the dimensionality of singing dynamics, described as trajectories (motor 'gestures') in a space of syringeal pressure and tension. Here we assess model performance by characterizing the auditory response 'replay' of song premotor HVC neurons to the presentation of song variants in sleeping birds, and by examining HVC activity in singing birds. HVC projection neurons were excited and interneurons were suppressed within a few milliseconds of the extreme time points of the gesture trajectories. Thus, the HVC precisely encodes vocal motor output through activity at the times of extreme points of movement trajectories. We propose that the sequential activity of HVC neurons is used as a 'forward' model, representing the sequence of gestures in song to make predictions on expected behaviour and evaluate feedback.
160 citations
TL;DR: Comparison of patterns of song adjustment to noise in oscines and suboscines in Brazil and Mexico City suggests that song learning and/or song plasticity allows adaptation to new habitats and that this selective advantage may be linked to the evolution ofsong learning and plasticity.
Abstract: Song learning has evolved within several avian groups. Although its evolutionary advantage is not clear, it has been proposed that song learning may be advantageous in allowing birds to adapt their songs to the local acoustic environment. To test this hypothesis, we analysed patterns of song adjustment to noisy environments and explored their possible link to song learning. Bird vocalizations can be masked by low-frequency noise, and birds respond to this by singing higher-pitched songs. Most reports of this strategy involve oscines, a group of birds with learning-based song variability, and it is doubtful whether species that lack song learning (e.g. suboscines) can adjust their songs to noisy environments. We address this question by comparing the degree of song adjustment to noise in a large sample of oscines (17 populations, 14 species) and suboscines (11 populations, 7 species), recorded in Brazil (Manaus, Brasilia and Curitiba) and Mexico City. We found a significantly stronger association between minimum song frequency and noise levels (effect size) in oscines than in suboscines, suggesting a tighter match in oscines between song transmission capacity and ambient acoustics. Suboscines may be more vulnerable to acoustic pollution than oscines and thus less capable of colonizing cities or acoustically novel habitats. Additionally, we found that species whose song frequency was more divergent between populations showed tighter noise-song frequency associations. Our results suggest that song learning and/or song plasticity allows adaptation to new habitats and that this selective advantage may be linked to the evolution of song learning and plasticity.
73 citations
TL;DR: It is suggested that adjustments in song frequency and amplitude are largely independent and, thus, can be complementary rather than alternative vocal adjustments to noise.
70 citations
References
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TL;DR: The incorporation of brainstem‐based respiratory‐vocal variables is likely to be a necessary next step in the construction of more sophisticated models of the control of vocalization.
Abstract: Reviews of the songbird vocal control system frequently begin by describing the forebrain nuclei and pathways that form anterior and posterior circuits involved in song learning and song production, respectively. They then describe extratelencephalic projections upon the brainstem respiratory-vocal system in a manner suggesting, quite erroneously, that this system is itself well understood. One aim of this chapter is to demonstrate how limited is our understanding of that system. I begin with an overview of the neural network for the motor control of song production, with a particular emphasis on brainstem structures, including the tracheosyringeal motor nucleus (XIIts), which innervates the syrinx, and nucleus retroambigualis (RAm), which projects upon XIIts and upon spinal motor neurons innervating expiratory muscles. I describe the sources of afferent projections to XIIts and RAm and discuss their probable role in coordinating the bilateral activity of respiratory and syringeal muscles during singing. I then consider the routes by which sensory feedback, which could arise from numerous structures involved in singing, might access the song system to guide song learning, maintain accurate song production, and inform the song system of the requirements for air. I describe possible routes of access of auditory feedback, which is known to be necessary for song learning and maintenance, and identify potential sites of interaction with somatosensory and visceral feedback that could arise from the syrinx, the lungs and air sacs, and the upper vocal tract, including the jaw. I conclude that the incorporation of brainstem-based respiratory-vocal variables is likely to be a necessary next step in the construction of more sophisticated models of the control of vocalization.
116 citations
TL;DR: The role of syringeal muscles in controlling the aperture of the avian vocal organ, the syrinx, was evaluated directly by observing and filming through an endoscope while electrically stimulating different muscle groups of anaesthetised birds.
Abstract: 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), direct observations of the biomechanical effects of contraction largely confirm the functions of the intrinsic syringeal muscles proposed from indirect studies. Contraction of the dorsal muscles, m. syringealis dorsalis (dS) and m. tracheobronchialis dorsalis, constricts the syringeal lumen and thus reduces airflow by adducting connective tissue masses, the medial (ML) and lateral (LL) labia. Activity of the medial portion of the dS appears to affect the position of the ML and, consequently, plays a previously undescribed role in aperture control. Under the experimental conditions used in this study, full constriction of the syringeal lumen could not be achieved by stimulating adductor muscles. Full closure may require simultaneous activation of extrinsic syringeal muscles or the supine positioning of the bird may have exerted excessive tension on the syrinx. Contraction of m. tracheobronchialis ventralis enlarges the syringeal lumen and thus increases airflow by abducting the LL but does not affect the ML. The largest syringeal muscle, m. syringealis ventralis, plays a minor role, if any, in direct aperture control and thus in gating airflow. In parrots (cockatiels, Nymphicus hollandicus), direct observations show that even during quiet respiration the lateral tympaniform membranes (LTMs) are partially adducted into the tracheal lumen to form a narrow slot. Contraction of the superficial intrinsic muscle, m. syringealis superficialis, adducts the LTMs further into the tracheal lumen but does not close the syringeal aperture fully. The intrinsic deep muscle, m. syringealis profundus, abducts the LTMs through cranio-laterad movement of a paired, protruding half-ring. The weakly developed extrinsic m. sternotrachealis seems to increase tension in the ipsilateral LTM but does not move it in or out of the syringeal lumen.
112 citations
"Frequency Modulation During Song in..." refers background in this paper
...…in this context that in parrots activity of intrinsic syringeal muscles does not show a clear correlation with fundamental frequency of sound (Gaunt and Gaunt 1985), and tension control therefore appears to be more indirect through the gating activity of these muscles (Larsen and Goller 2002)....
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...Frequency control in other bird groups is less well understood but may not involve such direct action by vocal muscles (e.g., Gaunt and Gaunt 1977, 1985; Gaunt et al. 1982; Larsen and Goller 2002; Suthers 2001; Youngren et al. 1974)....
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...How the positioning of the medial labium is controlled is less well understood, but, most likely, it involves the dorsal syringeal muscle (Larsen and Goller 2002)....
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TL;DR: The data suggest that V contributes to syllable termination during vocalization and may silence the syrinx during normal respiration, and D contributes to the acoustic structure of most syllables, and V may contribute to a special subset of syllables.
Abstract: Acute and chronic electromyographic (EMG) recordings from individual syringeal muscles were used to study syringeal participation in respiration and vocalization In anesthetized birds, all syringeal muscles recorded were active to some degree during the expiratory phase of respiration, following activity in the abdominal musculature and preceding the emergence of breath from the nostril In awake birds, the ventralis (V) muscle fired a strong, consistent burst, but the dorsalis (D) was variable both in strength and timing Denervation of V is sufficient to produce the wheezing respiration originally seen in birds with complete bilateral section of the tracheosyringeal nerve Complete syringeal denervation also removed almost all the acoustic features that distinguish individual song syllables, but had a minor effect on the temporal structure of song When activity in V and D was recorded in awake, vocalizing birds, D was active before and during sound production, and V showed a small burst before sound onset and a vigorous burst timed to the termination of sound During song, V was consistently active at sound offset, but also participated during sound for narrow bandwidth syllables For some syllables (simple harmonic stacks), neither muscle was active These data suggest that V contributes to syllable termination during vocalization and may silence the syrinx during normal respiration D contributes to the acoustic structure of most syllables, and V may contribute to a special subset of syllables In summary, the syringeal muscles show different activity patterns during respiration and vocalization and can be independently activated during vocalization, depending on the syllable produced
102 citations
TL;DR: A dynamical model of the processes involved in birdsong production is presented, relating qualitatively its parameters with biological ones and intended to unify the activity patterns of the muscles controlling the vocal organ with the resulting vocalization.
Abstract: We present a dynamical model of the processes involved in birdsong production, relating qualitatively its parameters with biological ones. In this way, we intend to unify the activity patterns of the muscles controlling the vocal organ with the resulting vocalization. With relatively simple paths in the parameter space of our model, we reproduce experimental recordings of the Chingolo sparrow (Zonotrichia capensis).
91 citations
TL;DR: It is suggested that the role of the vocal fold and the thin, paired vocal and ventricular membranes are the ultrasonic generators and that the cricothyroid muscle contracts just prior to each ultrasonic vocalization and relaxes during phonation.
Abstract: The echolocative pulses emitted at high repetition rates by bats pose a number of questions regarding the mechanism of their production. We have investigated some physiologic parameters of vocalization in the North American Vespertilionid bat Eptesicus fuscus , including pulse insertion within the respiratory cycle and subglottic pressure changes accompanying these intense sounds. Subglottic pressures are considerably higher than those characteristic of human speech and, therefore, require a substantial structure to act as a glottal stop. We suggest that this is the role of the vocal fold and that the thin, paired vocal and ventricular membranes are the ultrasonic generators. The cricothyroid muscle, which is thought to influence sound frequency by altering the tension on these membranes, contracts just prior to each ultrasonic vocalization and relaxes during phonation. Cricothyroid muscle relaxation may gradually decrease the tension on the membranes and create the downward frequency sweep characteristic of most pulses.
89 citations