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Journal ArticleDOI

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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Citations
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Journal ArticleDOI
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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Journal ArticleDOI
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

Journal ArticleDOI
07 Mar 2013-Nature
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

Journal ArticleDOI
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

Journal ArticleDOI
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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Journal ArticleDOI
TL;DR: Examining the role of auditory feedback in song development and preliminary comments on neural control in suboscine flycatchers concludes that the apparent absence of brain sections of phoebes containing no obvious cell clusters like the forebrain song nuclei of songbirds is consistent with its ability to develop normal song without auditory feedback.

251 citations

Journal ArticleDOI
01 Jan 1984-The Auk
TL;DR: No microgeographic variation of wild songs, no evidence of learning from a tutor tape, nor any similarity of song characters among kin are found, and the vocal development of these suboscine flycatchers is strikingly different from that of typical oscines, where vocal learning is the rule.
Abstract: -I studied the song development of five Willow Flycatchers (Empidonax traillii) and four Alder Flycatchers (Empidonax alnorum) taken from nests at 7-10 days of age. Three Willow Flycatchers and four Alder Flycatchers were tutored with songs of the other species, and two Willow Flycatchers served as controls, hearing only conspecific songs. All nine subjects, both females (when administered exogenous testosterone) and males, and both experimentals and controls, produced remarkably normal songs; slight differences between songs of wild and experimental subjects could be attributed to motivational states rather than to the effects of acoustic isolation in the laboratory. I found no microgeographic variation of wild songs, no evidence of learning from a tutor tape, nor any similarity of song characters among kin. The vocal development of these suboscine flycatchers is strikingly different from that of typical oscines, where vocal learning is the rule. Received 17 January 1983, accepted 1

236 citations

Journal ArticleDOI
10 Aug 2000-Nature
TL;DR: It is shown, using behaviourally driven gene expression in freely ranging tropical animals, that the forebrain of hummingbirds contains seven discrete structures that are active during singing, providing the first anatomical and functional demonstration of vocal nuclei in hummingbirds.
Abstract: Hummingbirds have developed a wealth of intriguing features, such as backwards flight, ultraviolet vision, extremely high metabolic rates, nocturnal hibernation, high brain-to-body size ratio and a remarkable species–specific diversity of vocalizations1,2,3,4. Like humans, they have also developed the rare trait of vocal learning, this being the ability to acquire vocalizations through imitation rather than instinct5,6. Here we show, using behaviourally driven gene expression in freely ranging tropical animals, that the forebrain of hummingbirds contains seven discrete structures that are active during singing, providing the first anatomical and functional demonstration of vocal nuclei in hummingbirds. These structures are strikingly similar to seven forebrain regions that are involved in vocal learning and production in songbirds and parrots7,8,9,10,11,12,13—the only other avian orders known to be vocal learners5. This similarity is surprising, as songbirds, parrots and hummingbirds are thought to have evolved vocal learning and associated brain structures independently5,14, and it indicates that strong constraints may influence the evolution of forebrain vocal nuclei.

235 citations

Journal ArticleDOI
TL;DR: Left hypoglossal dominance occurs in canaries with small or large song repertoires, in chronically deafened canaries that never had access to their own auditory feedback, and in birds that had the right or left cochlea removed at an early age.
Abstract: 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.

226 citations

Journal ArticleDOI
TL;DR: It is suggested that the observed results were probably due to the effects of muting and epaulet-colouration upon advertising song and song-spread and bill-up displays, and a three-level territorial defence system is proposed for this species.

218 citations