Rapid encoding of an internal model for imitative learning

As in human infant speech development, vocal imitation in songbirds involves sensory acquisition and memorization of adult-produced vocal signals, followed by a protracted phase of vocal motor practice. The internal model of adult tutor song in the juvenile male brain, termed ‘the template’, is central to the vocal imitation process. However, even the most fundamental aspects of the template, such as when, where and how it is encoded in the brain, remain poorly understood. A major impediment to progress is that current studies of songbird vocal learning use protracted tutoring over days, weeks or months, complicating dissection of the template encoding process. Here, we take the key step of tightly constraining the timing of template acquisition. We show that, in the zebra finch, template encoding can be time locked to, on average, a 2 h period of juvenile life and based on just 75 s of cumulative tutor song exposure. Crucially, we find that vocal changes occurring on the day of training correlate with eventual imitative success. This paradigm will lead to insights on how the template is instantiated in the songbird brain, with general implications for deciphering how internal models are formed to guide learning of complex social behaviours.     

Comparisons of different methods to train a young zebra finch (Taeniopygia guttata) to learn a song

Like humans, oscine songbirds exhibit vocal learning. They learn their song by imitating conspecifics, mainly adults. Among them, the zebra finch (Taeniopygia guttata) has been widely used as a model species to study the behavioral, cellular and molecular substrates of vocal learning. Various methods using taped song playback have been used in the laboratory to train young male finches to learn a song. Since different protocols have been applied by different research groups, the efficiency of the studies cannot be directly compared. The purpose of our study was to address this problem. Young finches were raised by their mother alone from day post hatching (dph) 10 and singly isolated from dph 35. One week later, exposure to a song model began, either using a live tutor or taped playback (passive or self-elicited). At dph 100, the birds were transferred to a common aviary. We observed that one-to-one live tutoring is the best method to get a fairly complete imitation. Using self-elicited playback we observed high inter-individual variability; while some finches learned well (including good copying of the song model), others exhibited poor copying. Passive playback resulted in poor imitation of the model. We also observed that finches exhibited vocal changes after dph 100 and that the range of these changes was negatively related to their imitation of the song model. Taken together, these results suggest that social aspects are predominant in the success outcome of song learning in the zebra finch.     

Variable Food Begging Calls Are Harbingers of Vocal Learning

Vocal learning has evolved in only a few groups of mammals and birds. The developmental and evolutionary origins of vocal learning remain unclear. The imitation of a memorized sound is a clear example of vocal learning, but is that when vocal learning starts? Here we use an ontogenetic approach to examine how vocal learning emerges in a songbird, the chipping sparrow. The first vocalizations of songbirds, food begging calls, were thought to be innate, and vocal learning emerges later during subsong, a behavior reminiscent of infant babbling. Here we report that the food begging calls of male sparrows show several characteristics associated with learned song: male begging calls are highly variable between individuals and are altered by deafening; the production of food begging calls induces c-fos expression in a forebrain motor nucleus, RA, that is involved with the production of learned song. Electrolytic lesions of RA significantly reduce the variability of male calls. The male begging calls are subsequently incorporated into subsong, which in turn transitions into recognizable attempts at vocal imitation. Females do not sing and their begging calls are not affected by deafening or RA lesion. Our results suggest that, in chipping sparrows, intact hearing can influence the quality of male begging calls, auditory-sensitive vocal variability during food begging calls is the first step in a modification of vocal output that eventually culminates with vocal imitation.     

Call Learning in Black-capped Chickadees (Parus atricapillus): The Role of Experience in the Development of ‘Chick-A-Dee’ Calls

The role of learning in the development of bird vocalizations other than territorial song is not well studied. The well-known role of direct imitation in the development of territorial song potentially masks the effects of other processes in the development of vocal behaviour. The ‘chick-a-dee’ call of black-capped chickadees is a good system in which to investigate more subtle developmental processes because this call is composed of a small number of distinctive note types. These note types may be classified objectively based on a simple set of acoustic variables, allowing for a quantitative assessment of vocal learning. We raised four groups of black-capped chickadees under different degrees of social and acoustic isolation. We then used a multivariate analysis of the acoustic structure of the introductory call notes (‘A-’ ‘B-’ and ‘C-notes’) to determine how similar the notes produced by these hand-reared birds were to the notes of wild birds. Hand-reared chickadees with greater exposure to normal phonology produced notes of all three note types that were more similar to those of wild birds. Regardless of experience, however, all birds produced A-notes that fell within the normal range of those produced by wild birds. By contrast, the development of normal B- and C-notes appears to be more dependent upon experience. These data suggest that learning may play a different role in the development of different phonological units within one vocalization. Our results also illustrate the importance of considering processes other than simple imitation in the development of avian vocalizations.     

Age‐dependent song changes in a closed‐ended vocal learner: elevation of song performance after song crystallization

Birdsong is a sexual signal that serves as an indicator of male quality. There is already abundant evidence that song elaboration reflects early life‐history because early developmental stress affects neural development of song control systems, and leaves irreversible adverse effects on song phenotypes. Especially in closed‐ended vocal learners, song features crystallized early in life are less subject to changes in adulthood. This is why less attention has been paid to lifelong song changes in closed‐ended learners. However, in the eyes of female birds that gain benefits from choosing mates based on male songs, not only past but also current conditions encoded in songs would be meaningful, given that even crystallized songs in closed‐ended learners would not be identical in the long term. In this study, we examine within‐individual song changes in the Java sparrow Lonchura oryzivora, with the aim of shedding light on the relationship between song and long‐term life history. Specifically, we compared song length, tempo, and song complexity measures between the point just after song crystallization and around 1 yr later, and also compared those traits between fathers and sons to clarify the effect of vocal learning. While it is not surprising that song complexity did not differ depending on age or between fathers and sons, we found that song length and tempo increased with age. Follow‐up analyses have revealed that frequency bandwidth and peak frequency of song notes also elevated with age. Our results show that song performance related to motor skills can be improved even after song crystallization. We also suggest that song performance in closed‐ended vocal learners gives a reliable clue for mate choice by reflecting male quality with aging.     

澳大利亚Floreana岛达尔文小树雀喙型与其鸣唱的不相关性

鸟类鸣唱的功能通常是吸引配偶,对于建立繁殖隔离也是非常重要的。现有的研究认为鸟类鸣唱表演可能受到鸟类喙型变化的影响。达尔文鸣雀是一类用来验证喙型和鸣唱表演关系的模型物种,前人的研究认为较低的元音演奏与更大的喙相关。本文用在Floreana岛屿生活的达尔文小树雀(Camarhynchus parvulus)来验证喙型和元音演奏的关系。结果显示,喙型大小与元音演奏之间无相关性。这个发现与过去对小树雀中的研究结果相似,但却与达尔文鸣雀中更大体型的鸟类研究结果相反。讨论了研究结果在物种的生态分化和生态变异之间的前后关系。     

A procedure for an automated measurement of song similarity

Assessment of vocal imitation requires a widely accepted way of describing and measuring any similarities between the song of a tutor and that of its pupil. Quantifying the similarity between two songs, however, can be difficult and fraught with subjective bias. We present a fully automated procedure that measures parametrically the similarity between songs. We tested its performance on a large database of zebra finch, Taeniopygia guttata, songs. The procedure uses an analytical framework of modern spectral analysis to characterize the acoustic structure of a song. This analysis provides a superior sound spectrogram that is then reduced to a set of simple acoustic features. Based on these features, the procedure detects similar sections between songs automatically. In addition, the procedure can be used to examine: (1) imitation accuracy across acoustic features; (2) song development; (3) the effect of brain lesions on specific song features; and (4) variability across different renditions of a song or a call produced by the same individual, across individuals and across populations. By making the procedure available we hope to promote the adoption of a standard, automated method for measuring similarity between songs or calls. Copyright 2000 The Association for the Study of Animal Behaviour.     

Sensitive periods and circuits for learned birdsong

Experience influences the development of certain behaviors and their associated neural circuits during a discrete period after birth. Songbirds, with their highly quantifiable vocal output and well-delineated vocal control circuitry, provide an excellent context in which to examine the neural mechanisms regulating sensitive periods for learning. Recent discoveries indicate that auditory input to the vocal control circuitry in songbirds is dynamically modulated and show that neural circuitry previously thought to be used only in plastic juvenile song may also actively maintain stable adult song. These findings provide important clues to how sensitive periods for auditory feedback and vocal plasticity are regulated during song development.     

An Automated Procedure for Evaluating Song Imitation

Songbirds have emerged as an excellent model system to understand the neural basis of vocal and motor learning. Like humans, songbirds learn to imitate the vocalizations of their parents or other conspecific “tutors.” Young songbirds learn by comparing their own vocalizations to the memory of their tutor song, slowly improving until over the course of several weeks they can achieve an excellent imitation of the tutor. Because of the slow progression of vocal learning, and the large amounts of singing generated, automated algorithms for quantifying vocal imitation have become increasingly important for studying the mechanisms underlying this process. However, methodologies for quantifying song imitation are complicated by the highly variable songs of either juvenile birds or those that learn poorly because of experimental manipulations. Here we present a method for the evaluation of song imitation that incorporates two innovations: First, an automated procedure for selecting pupil song segments, and, second, a new algorithm, implemented in Matlab, for computing both song acoustic and sequence similarity. We tested our procedure using zebra finch song and determined a set of acoustic features for which the algorithm optimally differentiates between similar and non-similar songs.     

Social Guidance of Vocal Learning by Female Cowbirds: Validating its Functional Significance

Juvenile male M. a. ater cowbirds, who have never heard other male cowbirds sing, develop distinctively different repertoires when housed with M. a. ater females from their own area versus M. a. obscurus females from a distant population. Because female cowbirds do not sing, the differences in the males' songs do not arise through vocal imitation. Here we provide data demonstrating that the songs of female-housed males are functionally, as well as acoustically, distinctive. The songs of 8 groups of males were tested where the groups differed by age of singer, acoustic experience, and identity of social companion. The playback results demonstrate that non-singing female cowbirds not only stimulate the male to modify song content, but song potency. As such, they demonstrate the critical role female cowbirds may assume in the proximate and ultimate regulation of vocal development.     

A Tradeoff Between Performance and Accuracy in Bird Song Learning

Some of nature’s most complex behaviors, such as human speech and oscine bird song, are acquired through imitative learning. Accurate imitative learning tends to preserve patterns of behavior across generations, thus limiting the scope of cultural evolution. Less well studied are the routes by which cultural novelties arise during development, beyond simple copy error. In this study we assess, in a species of songbird, the relationship in song learning between two potentially conflicting learning goals: accuracy in copying and maximization of vocal performance. In our study species, the swamp sparrow (Melospiza georgiana), vocal performance can be defined for a given song type and frequency range by the rate of note repetition (‘trill rate’), with faster trills being more difficult to sing. We trained young swamp sparrows with song models with experimentally modified trill rates and characterized both the accuracy and performance levels of copies. Our main finding is that birds elevated the trill rates of low‐performance models, but at the expense of imitative accuracy. By contrast, birds reproduced normal and high‐performance models with typically high accuracy in structure and timing. Developmental mechanisms that enable songbirds to balance imitative accuracy and vocal performance are likely favored by sexual selection and may help explain some current patterns of variation in birdsong. Such mechanisms may also explain how behaviors that are learned by imitation can nevertheless respond to selection for high‐performance levels in their expression.     

Non‐Salient Geographic Variation in Birdsong in a Species That Learns by Improvisation

Geographic variation in birdsong and differential responses of territorial males to local and non‐local song variants have been documented in a number of songbird species in which males learn their songs through imitation. Here, we investigated geographic song variation and responses to local and non‐local song in the grasshopper sparrow (Ammodramus savannarum), a species in which males develop song by improvisation rather than imitation, as a first step toward understanding how the extent and salience of geographic song variation is related to the mode of song development. To describe the geographic variation in song, we compared songs from populations in eastern Maryland and central Ohio, USA, using multiple acoustic analysis techniques. We then conducted a playback experiment in Maryland using local and non‐local (Ohio) songs to test how territorial males responded to this geographic variation. We found acoustic differences between songs from the two sites. However, males responded similarly to playback of these songs, suggesting that this geographic variation is not behaviorally salient in a territorial context. Together with previous studies, our results suggest that across species, geographic song variation and the extent to which this variation functions in communication may be correlated with the accuracy with which song models are imitated during song development.     

Core and Shell Song Systems Unique to the Parrot Brain

The ability to imitate complex sounds is rare, and among birds has been found only in parrots, songbirds, and hummingbirds. Parrots exhibit the most advanced vocal mimicry among non-human animals. A few studies have noted differences in connectivity, brain position and shape in the vocal learning systems of parrots relative to songbirds and hummingbirds. However, only one parrot species, the budgerigar, has been examined and no differences in the presence of song system structures were found with other avian vocal learners. Motivated by questions of whether there are important differences in the vocal systems of parrots relative to other vocal learners, we used specialized constitutive gene expression, singing-driven gene expression, and neural connectivity tracing experiments to further characterize the song system of budgerigars and/or other parrots. We found that the parrot brain uniquely contains a song system within a song system. The parrot “core” song system is similar to the song systems of songbirds and hummingbirds, whereas the “shell” song system is unique to parrots. The core with only rudimentary shell regions were found in the New Zealand kea, representing one of the only living species at a basal divergence with all other parrots, implying that parrots evolved vocal learning systems at least 29 million years ago. Relative size differences in the core and shell regions occur among species, which we suggest could be related to species differences in vocal and cognitive abilities.     

Sensitive period for sensorimotor integration during vocal motor learning

Sensory experience during sensitive periods in development may direct the organization of neural substrates, thereby permanently influencing subsequent adult behavior. We report a sensitive period during the imitative motor learning phase of sensorimotor integration in birdsong development. By temporarily and reversibly blocking efference to the vocal muscles, we disrupted vocal motor practice during selected stages of song development. Motor disruption during prolonged periods early in development, which allows recovery of vocal control prior to the onset of adult song, has no effect on adult song production. However, song disruption late in development, during the emergence of adult song, results in permanent motor defects in adult song production. These results reveal a decreased ability to compensate for interference with motor function when disturbances occur during the terminal stage of vocal motor development. Temporary disruption of syringeal motor control in adults does not produce permanent changes in song production. Permanent vocal aberrations in juveniles are evident exclusively in learned song elements rather than nonlearned calls, suggesting that the sensitive period is associated with motor learning.     

Vocal performance influences female response to male bird song: an experimental test

Female songbirds are thought to assess males based on aspectsof song, such as repertoire size or amount of singing, thatcould potentially provide information about male quality. Arelatively unexplored aspect of song that also might serve asan assessment signal is a male's ability to perform physicallychallenging songs. Trilled songs, such as those produced byswamp sparrows (Melospiza georgiana), present males with a performancechallenge because trills require rapid and precise coordinationof vocal tract movements, resulting in a trade-off between trillrate and frequency bandwidth. This trade-off defines a constrainton song production observed as a triangular distribution inacoustic space of trill rate by frequency bandwidth, with anupper boundary that represents a performance limit. Given thisbackground on song production constraints, we are able to identifya priori which songs are performed with a higher degree of proficiencyand, thus, which songs should be more attractive to females.We determined the performance limit for a population of swampsparrows and measured how well individual males performed songsrelative to this limit ("vocal performance"). We then comparedfemale solicitation responses to high-performance versus low-performanceversions of the same song type produced by different males.Females displayed significantly more to high-performance songsthan to low-performance songs, supporting the hypothesis thatfemales use vocal performance to assess males.     

Social Information Embedded in Vocalizations Induces Neurogenomic and Behavioral Responses

Social cues facilitate relationships within communities. Zebra finches form long-term stable mate pairs and produce offspring within a multi-family, multi-generational community that can include hundreds of birds. Males use song to communicate in this complex environment. Males sing as part of their courtship display but also abundantly throughout each day, suggesting a role for their vocal signature outside of a reproductive context. One advantage of a vocal social cue is that it can be exchanged when birds are out of visual contact, as regularly occurs in a zebra finch community. Previous works have demonstrated that females hearing song are affected by their social relationship to the bird singing it, and the immediate social context. Here, we probed the question of whether or not the song itself carried social information, as would be expected from the situations when males sing outside of view of the female. We quantified behavioral and neurogenomic responses to two songs we predicted would have distinct “attractive” qualities in adult females housed in either mixed sex or female-only social communities. Our results show that only mixed sex-housed females show distinctive behavioral and neurogenomic responses to attractive songs. These data are consistent with the idea that the acoustic properties of song carry social information, and that the current social situation modulates the neural and behavioral responses to these signals.     

The anatomy of onomatopoeia

Virtually every human faculty engage with imitation. One of the most natural and unexplored objects for the study of the mimetic elements in language is the onomatopoeia, as it implies an imitative-driven transformation of a sound of nature into a word. Notably, simple sounds are transformed into complex strings of vowels and consonants, making difficult to identify what is acoustically preserved in this operation. In this work we propose a definition for vocal imitation by which sounds are transformed into the speech elements that minimize their spectral difference within the constraints of the vocal system. In order to test this definition, we use a computational model that allows recovering anatomical features of the vocal system from experimental sound data. We explore the vocal configurations that best reproduce non-speech sounds, like striking blows on a door or the sharp sounds generated by pressing on light switches or computer mouse buttons. From the anatomical point of view, the configurations obtained are readily associated with co-articulated consonants, and we show perceptual evidence that these consonants are positively associated with the original sounds. Moreover, the pairs vowel-consonant that compose these co-articulations correspond to the most stable syllables found in the knock and click onomatopoeias across languages, suggesting a mechanism by which vocal imitation naturally embeds single sounds into more complex speech structures. Other mimetic forces received extensive attention by the scientific community, such as cross-modal associations between speech and visual categories. The present approach helps building a global view of the mimetic forces acting on language and opens a new venue for a quantitative study of word formation in terms of vocal imitation.     

Circuits,hormones, and learning: Vocal behavior in songbirds

Species-typical vocal patterns subserve species identification and communication for individual organisms. Only a few groups of organisms learn the sounds used for vocal communication, including songbirds, humans, and cetaceans. Vocal learning in songbirds has come to serve as a model system for the study of brain-behavior relationships and neural mechanisms of learning and memory. Songbirds learn specific vocal patterns during a sensitive period of development via a complex assortment of neurobehavioral mechanisms. In many species of songbirds, the production of vocal behavior by adult males is used to defend territories and attract females, and both males and females must perceive vocal patterns and respond to them. In both juveniles and adults, specific types of auditory experience are necessary for initial song learning as well as the maintenance of stable song patterns. External sources of experience such as acoustic cues must be integrated with internal regulatory factors such as hormones, neurotransmitters, and cytokines for vocal patterns to be learned and produced. Thus, vocal behavior in songbirds is a culturally acquired trait that is regulated by multiple intrinsic as well as extrinsic factors. Here, we focus on functional relationships between circuitry and behavior in male songbirds. In that context, we consider in particular the influence of sex hormones on vocal behavior and its underlying circuitry, as well as the regulatory and functional mechanisms suggested by morphologic changes in the neural substrate for song control. We describe new data on the architecture of the song system that suggests strong similarities between the songbird vocal control system and neural circuits for memory, cognition, and use-dependent plasticity in the mammalian brain. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 602–618, 1997     

Delayed vocal ontogeny in songbirds: a laboratory study validates a model for delayed development derived from field studies

Based on field studies, we proposed a model that describes how vocal ontogeny proceeds over a 2-year period in wild brown-headed cowbirds (Molothrus ater). We tested this model in the laboratory by exposing yearling male cowbirds (n?=?7 tutees), trapped at the start of the breeding season in a southern California dialect, to adult tutors with unfamiliar song types from a different dialect. As adults at the start of their second season, the tutees all had enlarged repertoires based almost entirely on tutor song types. Thus, tutees dropped song types in their yearling repertoires that did not match tutor types and added tutor songs that they had heard for the first time as yearlings in captivity. We discuss these findings in the context of a previous captivity study in which tutees also changed their yearling repertoires but generally failed to copy their tutors’ songs. This is the first laboratory study to fully replicate the delayed ontogeny we have described for wild cowbirds, and validates the delayed vocal development model we proposed. This model is important in a more general context, because it explains how song dialects can remain temporally stable despite immigration by young males with non-local songs.