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: Syringeal complexity may not be an adaptation for plastic vocal behavior, but it is permissive of and probably prerequisite for such behavior.
Abstract: -Neither the possession of large vocabularies or repertoires nor the ability to learn phonations can be precisely correlated with the structural complexity of a syrinx. Hence, some recent investigators have suggested that avian vocal plasticity arises solely from a neurological shift. A simple syrinx, i.e. one with only extrinsic musculature, is subject to certain constraints, however. Its configuration changes as a unit, and the factors responsible for modulating sounds cannot be independently varied. Thus, the temporal characteristics of sound patterns can be varied easily, but rapid juxtaposition of different modulatory patterns is difficult. Intrinsic musculature permits isolation and independent control of syringeal components and thereby simplifies control of modulations. Syringeal complexity may not be an adaptation (i.e. did not evolve under selection) for plastic vocal behavior, but it is permissive of and probably prerequisite for such behavior. Received 17 November 1982, ac-
78 citations
Book•
01 Jan 2005
TL;DR: In this paper, the authors focus on the physical mechanisms at play in the production of birds' singing and discuss some complex acoustic features present in the avian vocal organ, and how to control it in order to produce different sounds.
Abstract: Few sounds in nature show the beauty, diversity and structure that we find
in birdsong. The song produced by a bird that is frequently found in the
place where we grew up has an immense evocative power, hardly comparable
with any other natural phenomenon. These reasons would have been more
than enough to attract our interest to the point of working on an aspect
of this phenomenon. However, in recent years birdsong has also turned into
an extremely interesting problem for the scientific community. The reason is
that, out of the approximately 10 000 species of birds known to exist, some
4000 share with humans (and just a few other examples in the animal kingdom)
a remarkable feature: the acquisition of vocalization requires a certain
degree of exposure to a tutor. These vocal learners are the oscine songbirds,
together with the parrots and hummingbirds. For this reason, hundreds of
studies have focused on localizing, within the birds’ brains, the regions involved
in the learning and production of the song. The hope is to understand
through this example the mechanisms involved in the acquisition of a general
complex behavior through learning. The shared, unspoken dream is to
learn something about the way in which we humans learn speech. Studies
of the roles of hormones, genetics and experience in the configuration of the
neural architecture needed to execute the complex task of singing have kept
hundreds of scientists busy in recent years.
Between the complex neural architecture generating the basic instructions
and the beautiful phenomenon that we enjoy frequently at dawn stands
a delicate apparatus that the bird must control with incredible precision.
This book deals with the physical mechanisms at play in the production of
birdsong. It is organized around an analysis of the song “up” toward the
brain. We begin with a brief introduction to the physics of sound, discussing
how to describe it and how to generate it. With these elements, we discuss
the avian vocal organ of birds, and how to control it in order to produce
different sounds. Different species have anatomically different vocal organs;
we concentrate on the case of the songbirds for the reason mentioned above.
We briefly discuss some aspects of the neural architecture needed to control
the vocal organ, but our focus is on the physics involved in the generation
of the song. We discuss some complex acoustic features present in the song
that are generated when simple neural instructions drive the highly complex
vocal organ. This is a beautiful example of how the study of the brain and
physics complement each other: the study of neural instructions alone does
not prepare us for the complexity that arises when these instructions interact
with the avian vocal organ.
77 citations
"Frequency Modulation During Song in..." refers background in this paper
...Previous work on the physical mechanisms involved in song production explored linear approximations for the restitution force as a function of labial displacement (Mindlin and Laje 2005)....
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01 Oct 2004
TL;DR: The extensive knowledge the authors now have about vocal learning in birds may provide a useful guide on how best to approach the study of these mammalian vocal learners, though cetaceans will always be a challenge.
Abstract: Scientists have a come a long way in their studies of brains and birdsong. The discovery of new neurons in the adult brain has revolutionary implications for medical science. The molecular biology of vocal learning is helpful in understanding genetic mechanisms of behavior, and in resolving the great mystery of how vocal learning evolved. Some areas as yet unexplored include the study of vocal brain areas in the other mammalian vocal learners, cetaceans, and bats. The extensive knowledge we now have about vocal learning in birds may provide a useful guide on how best to approach the study of these mammalian vocal learners, though cetaceans will always be a challenge. New techniques may emerge for exploring brain connectivity and behaviorally-driven gene expression in human brains in an ethically responsible manner, though it is not yet clear how best to proceed.
76 citations
TL;DR: Air sac pressure variation as a mechanism for frequency modulation contrasts with the specialized syringeal musculature of songbirds and may explain why the fundamental frequency in non-songbird vocalizations is generally modulated within a limited frequency range.
Abstract: Birdsong assumes its complex and specific forms by the modulation of phonation in frequency and time domains. The organization of control mechanisms and intrinsic properties causing such modulation have been studied in songbirds but much less so in non-songbirds, the songs of which are often regarded as relatively simple. We examined mechanisms of frequency and amplitude modulation of phonation in ring doves Streptopelia risoria, which are non-songbirds. Spontaneous coo vocalizations were recorded together with concurrent pressure patterns in two different air sacs and air flow rate in the trachea. The results show that amplitude modulation is the result of the cyclic opening and closure of a valve instead of fluctuations in driving pressure, as is the current explanation. Frequency modulation is more complex than previously recognized and consists of gradual, continuous time-frequency patterns, punctuated by instantaneous frequency jumps. Gradual frequency modulation patterns correspond to pressure variation in the interclavicular air sac but not to pressure variation in the cranial thoracic air sac or air flow rate variation in the trachea. The cause of abrupt jumps in frequency has not been identified but can be explained on the basis of intrinsic properties of the vocal organ. Air sac pressure variation as a mechanism for frequency modulation contrasts with the specialized syringeal musculature of songbirds and may explain why the fundamental frequency in non-songbird vocalizations is generally modulated within a limited frequency range.
67 citations
TL;DR: The song system of oscine birds has become a versatile model system that is used to study diverse problems in neurobiology and it is suggested that the forebrains of birds and mammals are more alike than they first appeared.
Abstract: The song system of oscine birds has become a versatile model system that is used to study diverse problems in neurobiology. Because the song system is often studied with the intention of applying the results to mammalian systems, it is important to place song system brain nuclei in a broader context and to understand the relationships between these avian structures and regions of the mammalian brain. This task has been impeded by the distinctiveness of the song system and the vast apparent differences between the forebrains of birds and mammals. Fortunately, accumulating data on the development, histochemistry, and anatomical organization of avian and mammalian brains has begun to shed light on this issue. We now know that the forebrains of birds and mammals are more alike than they first appeared, even though many questions remain unanswered. Furthermore, the song system is not as singular as it seemed-it has much in common with other neural systems in birds and mammals. These data provide a firmer foundation for extrapolating knowledge of the song system to mammalian systems and suggest how the song system might have evolved.
55 citations