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Timbre changes after bilateral tracheosyringeal nerve section. A: Sonograms of Bird Y4's song and four additional syllables from Bird Y45's song as produced before tracheosyringeal nerve section. B: Sonograms of the same song and syllables as sung after bilateral nerve section. (Correlation coefficients for the comparisons between patterns of harmonic suppression as delivered before and after nerve section are shown. The amplitude envelope of syllables in Bird Y4's song is shown by the continuous line in the upper part of the sonogram. Note that Syllables 5 and 9 are omitted in the postoperative song.) This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
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Zebra finch (Taeniopygia guttata) song syllables often include harmonically related frequency components. These harmonics may be suppressed, and this differential emphasis varies between the syllables in a song and between individual birds' songs. These patterns of harmonic suppression are timbre. Individual syllables' patterns of harmonic suppress...
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Citations
... Most well known are sex differences in spatial cognition linked to ecology-males in many mammalian species may have increased spatial learning or memory hypothesized to relate to larger home ranges (Jones et al. 2003;Perdue et al. 2011), while females of avian brood parasites may have better spatial learning abilities in some tasks that helps in the prospecting and tracking of potential nests (Guigueno and Sherry 2017;Lois-Milevicich et al. 2020). Zebra finches also display sex differences in cognitive abilities, with one meta-analysis finding that females consistently learned auditory discriminations quicker than males, hypothesized to relate to the importance of females' discriminating the songs of potential mates (Kriengwatana et al. 2016), though other studies have found the opposite result-males learning auditory discriminations quicker than females and suggest that male song-learning necessitates enhanced auditory discrimination (Williams et al. 1989;Cynx 1993;Guillette et al. 2013). However, no study has examined sex differences in physical cognition, or the potential link between nest building ecology and physical cognition, in general. ...
... Another possible conclusion from our study is that males and females do differ in physical cognition but we were not able to detect this difference due to the nature of our study. The relationship between sex and vocal discrimination learning in zebra finches has provided conflicting results; as mentioned in the discussion, multiple studies have found sex differences but in differing directions (Searcy and Brenowitz 1988;Williams et al. 1989;Cynx 1993;Guillette et al. 2013;Kriengwatana et al. 2016). Nonetheless, there is clear indication cognitive sex differences can exist in zebra finches. ...
Nest-building behaviour in birds may be particularly relevant to investigating the evolution of physical cognition, as nest building engages cognitive mechanisms for the use and manipulation of materials. We hypothesized that nest-building ecology may be related to physical cognitive abilities. To test our hypothesis, we used zebra finches, which have sex-differentiated roles in nest building. We tested 16 male and 16 female zebra finches on three discrimination tasks in the following order: length discrimination, flexibility discrimination, and color discrimination, using different types of string. We predicted that male zebra finches, which select and deposit the majority of nesting material and are the primary nest builders in this species, would learn to discriminate string length and flexibility-structural traits relevant to nest building-in fewer trials compared to females, but that the sexes would learn color discrimination (not structurally relevant to nest building) in a similar number of trials. Contrary to these predictions, male and female zebra finches did not differ in their speed to learn any of the three tasks. There was, however, consistent among-individual variation in performance: learning speed was positively correlated across the tasks. Our findings suggest that male and female zebra finches either (1) do not differ in their physical cognitive abilities, or (2) any cognitive sex differences in zebra finches are more specific to tasks more closely associated with nest building. Our experiment is the first to examine the potential evolutionary relationship between nest building and physical cognitive abilities.
... Taken together, these psychophysical experiments with synthetic harmonic complexes, natural calls and song syllables show that zebra finches are exquisitely sensitive to changes in temporal fine structure in their vocalizations, possibly at the expense of sensitivity to overall envelope cues, at least in their song motifs. Both behavioural and single-unit studies using forward and reversed song syllables or motifs (where duration and overall spectrum are the same) also suggest that fine structure cues in these harmonic vocalizations could be important (Braaten et al., 2006; Margoliash & Fortune, 1992; Theunissen & Doupe, 1998; Williams, Cynx, & Nottebohm, 1989). ...
Peter Marler's fascination with richness of birdsong included the notion that birds attended to some acoustic features of birdsong, likely in the time domain, which were inaccessible to human listeners. While a considerable amount is known about hearing and vocal communication in birds, how exactly birds perceive their auditory world still remains somewhat of a mystery. For sure, field and laboratory studies suggest that birds hear the spectral, gross temporal features (i.e. envelope) and perhaps syntax of birdsong much like we do. However, there is also ample anecdotal evidence that birds are consistently more sensitive than humans to at least some aspects of their song. Here we review several psychophysical studies supporting Marler's intuitions that birds have both an exquisite sensitivity to temporal fine structure and may be able to focus their auditory attention on critical acoustic details of their vocalizations. Zebra finches, Taeniopygia guttata, particularly, seem to be extremely sensitive to temporal fine structure in both synthetic stimuli and natural vocalizations. This finding, together with recent research highlighting the complexity of zebra finch vocalizations across contexts, raises interesting questions about what information zebra finches may be communicating in temporal fine structure. Together these findings show there is an acoustic richness in bird vocalizations that is available to birds but likely out of reach for human listeners. Depending on the universality of these findings, it raises questions about how we approach the study of birdsong and whether potentially significant information is routinely being encoded in the temporal fine structure of avian vocal signals.
... The fundamental frequency of sound and fast temporal dynamics of songs are predominantly controlled by the syrinx [28,34-37], and spectral composition is additionally affected by upper vocal tract filtering [38-40]. The fine-temporal structure of song is under the direct motor control of syringeal muscles [34,41-44]. The (sub)millisecond temporal precision present in telencephalic pre-motor areas [45-47] is actuated by superfast syringeal musculature [36], a rare muscle type found predominantly in association with sound production and modulation in vertebrates [48,49]. ...
Background
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.
Results
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.
Conclusions
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.
... The vocal tract acoustics of zebra finches is distinctive. In contrast to species with tonal songs, adjustment of upper vocal tract structures in the zebra finch are linked to regulation of harmonic emphasis, rather than tracking of the fundamental frequency of song syllables (Williams et al. 1990;Goller et al. 2004;Ohms et al. 2010). Because calls and most song syllables of zebra finches are characterized by low fundamental frequency and rich harmonic spectrum, the analysis of resonance characteristics is facilitated for at least two reasons. ...
Vocal production in songbirds requires the control of the respiratory system, the syrinx as sound source and the vocal tract as acoustic filter. Vocal tract movements consist of beak, tongue and hyoid movements, which change the volume of the oropharyngeal-esophageal cavity (OEC), glottal movements and tracheal length changes. The respective contributions of each movement to filter properties are not completely understood, but the effects of this filtering are thought to be very important for acoustic communication in birds. One of the most striking movements of the upper vocal tract during vocal behavior in songbirds involves the OEC. This study measured the acoustic effect of OEC adjustments in zebra finches by comparing resonance acoustics between an utterance with OEC expansion (calls) and a similar utterance without OEC expansion (respiratory sounds induced by a bilateral syringeal denervation). X-ray cineradiography confirmed the presence of an OEC motor pattern during song and call production, and a custom-built Hall-effect collar system confirmed that OEC expansion movements were not present during respiratory sounds. The spectral emphasis during zebra finch call production ranging between 2.5 and 5 kHz was not present during respiratory sounds, indicating strongly that it can be attributed to the OEC expansion.
... The broad frequency spectrum of the calls is also well suited to convey their formant structure. Since formant frequencies are determined by the vocal tract resonances, which in turn depend on the detailed shape and dimensions of the vocal tract, they are potentially well designed to convey acoustic cues for individual recognition (Williams et al. 1989;Suthers 1994;Fitch and Kelley 2000). Such cues might be used by a parent magpie to recognize its own young when juvenile song is still highly variable. ...
Australian magpies (Gymnorhina tibicen) are notable for their vocal prowess. We investigated the syringeal and respiratory dynamics of vocalization by two 6-month-old males, whose songs had a number of adult features. There was no strong lateral syringeal dominance and unilateral phonation was most often achieved by closing the syringeal valve on the contralateral side of the syrinx. Unlike other songbirds studied, magpies sometimes used an alternative syringeal motor pattern during unilateral phonation in which both sides of the syrinx are partially adducted and open to airflow. Also, in contrast to most other songbirds, the higher fundamental frequency during two-voice syllables was usually generated on the left side of the syrinx. Amplitude modulation, a prominent feature of magpie song, was produced by linear or nonlinear interactions between different frequencies which may originate either on opposite sides of the syrinx or on the same side. Pulse tones, similar to vocal fry in human speech, were present in some calls. Unlike small songbirds, the fundamental of the modal frequency can be as low as that of the pulse tone, suggesting that large birds may have evolved pulse tones to increase acoustic diversity, rather than decrease the fundamental frequency.
... Before neurotomy, the low frequency component of male distance calls and fundamental frequency in female distance calls is similar, while a high-frequency component can only be found in male distance calls [this study, 34,35]. After syringeal denervation fundamental frequency of calls is similar for males and females [29,30,31,34,36,37], thus indicating that labial size is not an explanation for the observed differences. Because it is not clear which portion of the LL is actually vibrating during phonation, this morphological difference may not play a major role in the biomechanical control of sound frequency, but may be relevant in other aspects of sound production. ...
... 3]. Frequency control of song syllables is also largely driven by muscular control of labial tension, as is illustrated by the large drop after denervation [29,30,31,34,36,37] . The occurrence of cy song components further supports specialization of the male syrinx for high frequencies, because only males sing in the zebra finch. ...
In many songbirds the larger vocal repertoire of males is associated with sexual dimorphism of the vocal control centers and muscles of the vocal organ, the syrinx. However, it is largely unknown how these differences are translated into different acoustic behavior.
Here we show that the sound generating structures of the syrinx, the labia and the associated cartilaginous framework, also display sexual dimorphism. One of the bronchial half rings that position and tense the labia is larger in males, and the size and shape of the labia differ between males and females. The functional consequences of these differences were explored by denervating syringeal muscles. After denervation, both sexes produced equally low fundamental frequencies, but the driving pressure generally increased and was higher in males. Denervation strongly affected the relationship between driving pressure and fundamental frequency.
The syringeal modifications in the male syrinx, in concert with dimorphisms in neural control and muscle mass, are most likely the foundation for the potential to generate an enhanced frequency range. Sexually dimorphic vocal behavior therefore arises from finely tuned modifications at every level of the motor cascade. This sexual dimorphism in frequency control illustrates a significant evolutionary step towards increased vocal complexity in birds.
... Songs with noisier elements are less attractive than those with a better defined harmonic spectrum (Tomaszycki and Adkins-Regan, 2005). Aspects of timbre resulting from reinforcing or filtering particular parts of the spectrum are learned (Goller and Cooper, 2004; Williams et al., 1989). Spectral characteristics have been shown to become more consistent with age up until 15 months of age, suggesting an effect of practice long after song crystallization which takes place when males are approximately 100 days old (Pytte et al., 2007). ...
Zebra finches are an important model for vocal learning and avian mate choice. The two are contingent on each other: males' learned songs are addressed at females with learned preferences. This review documents the recent changes away from a purely mechanism-orientated approach of song learning toward the question of how variation in male phenotypic quality is reflected by variation in male song. The substantial evidence for female song preference learning is reviewed and compared to what is known to about unlearned preference biases. From the complementary evidence, a picture emerges that shows how cultural transmission of the male mating signal is paralleled by sensory learning processes on the receiver's side. The question of how the trait and preference might react in concert to environmental change and how learned receiver biases affect the evolutionary dynamics of culturally transmitted song emerge as exciting future research prospects.
... speech, are known to require cerebellar input (Gordon, 2007). Songbirds possess an exceptional capacity to perform complex behaviors including song, a behavior that requires intricate and well-timed fine motor function as well as significant cognitive input (Williams et al., 1989;Clayton & Dickinson, 1998). The avian cerebellum shares much anatomical similarity with that of mammals so results from songbirds will probably generalize to other species (Paula-Barbosa & Sobrinho-Simões, 1976;Tohyama, 1976;Paula-Barbosa et al., 1980;Smith et al., 1993). ...
In addition to its key role in complex motor function, the cerebellum is increasingly recognized to have a role in cognition. Songbirds are particularly good models for the investigation of motor and cognitive processes but little is known about the role of the songbird cerebellum in these processes. To explore cerebellar function in a songbird, we lesioned the cerebellum of adult female zebra finches and examined the effects on a spatial working memory task and on motor function during this task. There is evidence for steroid synthesis in the songbird brain and neurosteroids may have an impact on some forms of neural plasticity in adult songbirds. We therefore hypothesized that neurosteroids would affect motor and cognitive function after a cerebellar injury. We found that cerebellar lesions produced deficits in motor and cognitive aspects of a spatial task. In line with our prediction, birds in which estrogen synthesis was blocked had impaired performance in our spatial task compared with those that had estrogen synthesis blocked but estrogen replaced. There was no clear effect of estrogen replacement on motor function. We also found that lesions induced expression of the estrogen synthetic enzyme aromatase in reactive astrocytes and Bergmann glia around a cerebellar lesion. These data suggest that the cerebellum of songbirds mediates both motor and cognitive function and that estrogens may improve the recovery of cognitive aspects of cerebellar function after injury.
... Syringeal motor neurons drive highly dynamic syringeal muscle activity during singing. When the XIIts nerve is cut, the spectral and fine temporal features of song are severely disrupted, while the global temporal features of song, which are determined by expiratory musculature, remain largely intact ( Williams et al., 1989Simpson and Vicario, 1990). The sparing of song temporal structure following XIIts nerve section indicates that central pathways controlling syringeal and respiratory activity are independent. ...
Songbirds are one of the few nonhuman animals that learn to vocalize. Juvenile songbirds first memorize a tutor song and then match this memorized model using auditory feedback. The close parallels between song learning in birds and speech learning in humans have piqued interest in the mechanisms of song learning. The neurobiological analysis of birdsong was revolutionized by the discovery of a specialized constellation of brain nuclei necessary to singing. Part of this ‘song system’ includes a basal ganglia pathway necessary to song plasticity, providing an important insight into neural mechanisms of song learning. Other important issues, such as where tutor song memories are stored and how and where auditory feedback registers in the brain of the singing bird, are now beginning to be addressed, with many of the most exciting results about to unfold. This chapter discusses song’s function as a communication signal, the role experience plays in song development, peripheral and central song mechanisms, and neural mechanisms of song learning.
... This rendered spectrographs with a resolution of 10 kHz with a temporal resolution of 1 ms. The computational determination of fundamental frequency of song elements is sometimes difficult in zebra finches because the harmonics (multiple frequencies of the fundamental frequency that are used in its automatic calculation) can be suppressed in the elements (Williams et al. 1989). We therefore used both the automatic pitch detection and manual fine tuning feature in Luscinia (Appendix A1). ...
Birdsong is a sexually selected and culturally transmitted multidimensional signal. Sexually selected traits are generally assumed to indicate condition. In oscine songbirds, song is learned early in life. The developmental stress hypothesis proposed that poor early developmental condition can adversely affect song learning. The quality and accuracy of learned song features could thus indicate male quality to conspecifics. Surprisingly, studies testing this hypothesis to date mostly compared adult males' song repertoires without looking at song imitation. The few that did reported inconsistent effects and analyzed a limited number of song features. Here, we examined the effects of early condition (by brood size manipulation) on learned song in zebra finches, Taeniopygia guttata, in comparing both the number of specific elements copied from an adult song tutor and a great number of previously neglected syntax-, complexity-, and performance-related song features. The treatment did not significantly affect average number of imitated elements, the standard measure of quality of song imitation in this species. However, developmental condition had 2 significant main effects on adult song: birds from large broods (i.e., of poor early condition) in comparison to birds from small broods copied syntactical dependencies of song elements from the song motif of their tutor less accurately and had less consistent sound duration between song motifs. These findings support the developmental stress hypothesis. We discuss how this sheds light on the potential role of such long-term signals of male developmental condition in female mate choice and potential constraints underlying condition-dependent expression of song features. Copyright 2008, Oxford University Press.
