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     

Effects of learning on song preferences and Zenk expression in female songbirds

Male songbirds learn to produce their songs, and females attend to these songs during mate choice. The evidence that female song preferences are learned early in life, however, is mixed. Here we review studies that have found effects of early song learning on adult song preferences, and those that have not. In at least some species, early experience with song can modify adult song preferences. Whether this learning needs to occur during an early sensitive phase, akin to male imitative vocal learning, or not remains an open question. Studies of the neural bases for female song preferences highlight activity (as measured by immediate-early gene induction) in regions of the auditory forebrain as often, but not always, being associated with song preferences. Immediate-early gene induction in these regions, however, is not specific to songs experienced early in life. On the whole, inherited factors, early experience, and adult experience all appear to play a role in shaping female songbirds preferences for male songs.     

Song learning in birds: the relation between perception and production

The vocal control system of oscine songbirds has some perplexing properties--e.g. laterality, adult neurogenesis, neuronal replacement--that are not predicted by common views of how vocal learning takes place. Similarly, we do not understand the relation between the direct pathway for the control of learned song and the recursive pathway necessary for song learning. Some of the paradoxes of the vocal system of birds may disappear once the relation between the perception and production of learned vocalizations is better understood. To some extent, perception and production may be two closely related states of a same system.     

Social influences during song development in the song sparrow: a laboratory experiment simulating field conditions

Oscine songbirds are exposed to many more songs than they keep for their final song repertoire and little is known about how a bird selects the particular song(s) to sing as an adult. We simulated in the laboratory the key variables of the natural song learning environment and examined the song selection process in nine hand-reared male song sparrows, Melospiza melodia, a species in which males sing 5-11 song types. During their second and third months (their presumed sensitive period), subjects were rotated equally among four live adult male tutors that had been neighbours in the field. Tutors were housed in individual aviary 'territories' in four corners of the roof of a building; subjects could see only one tutor at a time, but they could hear the others at a short distance. Later in their first year (months 5-12), half the subjects were again rotated among all four tutors and the other half were randomly stationed next to just one tutor. Results from this experiment confirm and extend the findings from our two previous field studies of song learning in this species. Young males in this experiment (1) learned whole song types, (2) learned songs from multiple tutors, (3) preferentially learned songs that were shared among their tutors, (4) learned songs that other young males in their group also chose, and (5) learned more songs from the tutor they were stationed next to during the later stage (stationary subjects). These last two results support the late influence hypothesis that interactions after a bird's sensitive period affect song repertoire development. Copyright 2000 The Association for the Study of Animal Behaviour.     

Representation of Early Sensory Experience in the Adult Auditory Midbrain: Implications for Vocal Learning

Vocal learning in songbirds and humans occurs by imitation of adult vocalizations. In both groups, vocal learning includes a perceptual phase during which juveniles birds and infants memorize adult vocalizations. Despite intensive research, the neural mechanisms supporting this auditory memory are still poorly understood. The present functional MRI study demonstrates that in adult zebra finches, the right auditory midbrain nucleus responds selectively to the copied vocalizations. The selective signal is distinct from selectivity for the bird''s own song and does not simply reflect acoustic differences between the stimuli. Furthermore, the amplitude of the selective signal is positively correlated with the strength of vocal learning, measured by the amount of song that experimental birds copied from the adult model. These results indicate that early sensory experience can generate a long-lasting memory trace in the auditory midbrain of songbirds that may support song learning.     

Introductory gestures before songbird vocal displays are shaped by learning and biological predispositions

Numerous animal displays begin with introductory gestures. For example, lizards start their head-bobbing displays with introductory push-ups, and many songbirds begin their vocal displays by repeating introductory notes (INs) before producing their learned song. Among songbirds, the acoustic structure and the number of INs produced before song vary considerably between individuals in a species. While similar variation in songs between individuals is a result of learning, whether variations in INs are also due to learning remains poorly understood. Here, using natural and experimental tutoring with male zebra finches, we show that mean IN number and IN acoustic structure are learned from a tutor. Interestingly, IN properties and how well INs were learned, were not correlated with the accuracy of song imitation and only weakly correlated with some features of songs that followed. Finally, birds artificially tutored with songs lacking INs still repeated vocalizations that resembled INs, before their songs, suggesting biological predispositions in IN production. These results demonstrate that INs, just like song elements, are shaped both by learning and biological predispositions. More generally, our results suggest mechanisms for generating variation in introductory gestures between individuals while still maintaining the species-specific structure of complex displays like birdsong.     

Hormonal acceleration of song development illuminates motor control mechanism in canaries

In songbirds, the ontogeny of singing behavior shows strong parallels with human speech learning. As in humans, development of learned vocal behavior requires exposure to an acoustic model of species‐typical vocalizations, and, subsequently, a sensorimotor practice period after which the vocalization is produced in a stereotyped manner. This requires mastering motor instructions driving the vocal organ and the respiratory system. Recently, it was shown that, in the case of canaries (Serinus canaria), the diverse syllables, constituting the song, are generated with air sac pressure patterns with characteristic shapes, remarkably, those belonging to a very specific mathematical family. Here, we treated juvenile canaries with testosterone at the onset of the sensorimotor practice period. This hormone exposure accelerated the development of song into stereotyped adultlike song. After 20 days of testosterone treatment, subsyringeal air sac pressure patterns of song resembled those produced by adults, while those of untreated control birds of the same age did not. Detailed temporal structure and modulation patterns emerged rapidly with testosterone treatment, and all previously identified categories of adult song were observed. This research shows that the known effect of testosterone on the neural circuits gives rise to the stereotyped categories of respiratory motor gestures. Extensive practice of these motor patterns during the sensorimotor phase is not required for their expression. © 2010 Wiley Periodicals, Inc. Develop Neurobiol 70: 943–960, 2010     

Age effect of deafening on stereotyped song maintenance in adult male bengalese finches Lonchura striata domestica

Birdsong is a complex learned vocal behavior that relies on auditory experience for development.However,it appears that among different species of close-ended songbirds,there are some variations in the necessity of auditory feedback for maintaining stereotyped adult song.In zebra finches,the deterioration of adult songs following deafness depends on the birds' age.It is unknown whether this age effect is a general rule in other avian species as well.Therefore,we chose Bengalese finches,whose songs show more...     

成年雄性斑胸草雀前脑与中脑对习得性发声控制的侧别差异

成年雄性鸣禽的习得性发声信号——长鸣(long call)和鸣唱(song)是由前脑高级发声中枢启动,以及由前脑最后一级输出核团弓状皮质栎核(robust nucleus of the arcopallium,RA)整合输出.RA投射神经元与位于中脑的基本发声中枢丘间复合体背内侧核(dorsomedial nucleus of the intercollicular,DM)形成突触连接.该文采用电损毁与声谱分析相结合的方法,通过依次损毁成年雄性斑胸草雀(Taeniopygia guttata)单侧RA和DM核团,探讨了前脑和中脑对习得性发声的影响.结果提示,RA核团与DM核团共同参与了对雄性斑胸草雀习得性声音的调控,而且这种控制具有右侧优势.     

Latent song type memories are accessible through auditory stimulation in a hand-reared songbird

The production of learned vocalizations such as in birdsong is often used to judge whether stimuli had been memorized upon their presentation. However, failures in the imitation of certain song patterns may also reflect impaired development of motor programmes or impaired memory retrieval rather than failures in stimulus memorization during auditory acquisition. To study this issue, we confronted adult hand-reared nightingales, Luscinia megarhynchos, with interactive playback experiments and used vocal matching as a behavioural tool to investigate their song type memories. Vocal matching is a common pattern-specific response that songbirds use in territorial countersinging. We distinguished two forms of pattern-specific matching: (1) song type matching (i.e. a bird replied with the same song type as the stimulus song), and (2) song group matching (i.e. the bird replied with a different song type which was, however, sequentially associated with the playback song presented earlier, i.e. during the tutoring). Some subjects used both song type and song group matching in response to song types they had not imitated from the tutor programme prior to the playback experiments. Our results indicate that nightingales store more song types in their sensory phase than they spontaneously recall from memory as adults. That is, memories of song types that were not performed in overt behaviour could be activated by vocal interactions, here induced by the interactive playback. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Dynamics of crowing development in the domestic Japanese quail (Coturnix coturnix japonica)

Species-specific behaviours gradually emerge, via incomplete patterns, to the final complete adult form. A classical example is birdsong, a learned behaviour ideally suited for studying the neural and molecular substrates of vocal learning. Young songbirds gradually transform primitive unstructured vocalizations (subsong, akin to human babbling) into complex, stereotyped sequences of syllables that constitute adult song. In comparison with birdsong, territorial and mating calls of vocal non-learner species are thought to exhibit little change during development. We revisited this issue using the crowing behaviour of domestic Japanese quail (Coturnix coturnix japonica). Crowing activity was continuously recorded in young males maintained in social isolation from the age of three weeks to four months. We observed developmental changes in crow structure, both the temporal and the spectral levels. Speed and trajectories of these developmental changes exhibited an unexpected high inter-individual variability. Mechanisms used by quails to transform sounds during ontogeny resemble those described in oscines during the sensorimotor phase of song learning. Studies on vocal non-learners could shed light on the specificity and evolution of vocal learning.     

Socially induced brain differentiation in a cooperatively breeding songbird

Birds living in social groups establish dominance hierarchies, and taking up the dominant position influences behaviour and physiological parameters. In cooperatively breeding white-browed sparrow weavers (Plocepasser mahali), the transition from subordinate helper to dominant breeder male induces the production of a new type of song. This song contains a large number of new syllables and differs in temporal pattern from duet songs produced by all other group members. Here we show that this change in social status of adult males affects the morphology of a behavioural control circuit, the song control system of songbirds that is composed of large neuron populations. The volume of the song control areas HVC and RA and their gene-expression levels depend on males' social status. Dominant males have several times larger testes than subordinates, which is not reflected in circulating androgen and oestrogen levels. Our findings suggest a remarkable differentiation of adult vertebrate brains in relation to changing social cues.     

Neurophysiological response selectivity for conspecific songs over synthetic sounds in the auditory forebrain of non-singing female songbirds

Female choice plays a critical role in the evolution of male acoustic displays. Yet there is limited information on the neurophysiological basis of female songbirds’ auditory recognition systems. To understand the neural mechanisms of how non-singing female songbirds perceive behaviorally relevant vocalizations, we recorded responses of single neurons to acoustic stimuli in two auditory forebrain regions, the caudal lateral mesopallium (CLM) and Field L, in anesthetized adult female zebra finches (Taeniopygia guttata). Using various metrics of response selectivity, we found consistently higher response strengths for unfamiliar conspecific songs compared to tone pips and white noise in Field L but not in CLM. We also found that neurons in the left auditory forebrain had lower response strengths to synthetics sounds, leading to overall higher neural selectivity for song in neurons of the left hemisphere. This laterality effect is consistent with previously published behavioral data in zebra finches. Overall, our results from Field L are in parallel and from CLM are in contrast with the patterns of response selectivity reported for conspecific songs over synthetic sounds in male zebra finches, suggesting some degree of sexual dimorphism of auditory perception mechanisms in songbirds.     

The song must go on: resilience of the songbird vocal motor pathway

Stereotyped sequences of neural activity underlie learned vocal behavior in songbirds; principle neurons in the cortical motor nucleus HVC fire in stereotyped sequences with millisecond precision across multiple renditions of a song. The geometry of neural connections underlying these sequences is not known in detail though feed-forward chains are commonly assumed in theoretical models of sequential neural activity. In songbirds, a well-defined cortical-thalamic motor circuit exists but little is known the fine-grain structure of connections within each song nucleus. To examine whether the structure of song is critically dependent on long-range connections within HVC, we bilaterally transected the nucleus along the anterior-posterior axis in normal-hearing and deafened birds. The disruption leads to a slowing of song as well as an increase in acoustic variability. These effects are reversed on a time-scale of days even in deafened birds or in birds that are prevented from singing post-transection. The stereotyped song of zebra finches includes acoustic details that span from milliseconds to seconds--one of the most precise learned behaviors in the animal kingdom. This detailed motor pattern is resilient to disruption of connections at the cortical level, and the details of song variability and duration are maintained by offline homeostasis of the song circuit.     

DEVELOPMENT OF VOCALISATIONS IN NESTLING AND FLEDGLING HOUSE WRENS IN NATURAL POPULATIONS

ABSTRACT

We conducted a field study of the ontogeny of vocal signals in the house wren Troglodytes aedon during the nestling and fledgling phases of life. We did spectrographic analyses and quantification of the developmental changes that occurred in the acoustic features of the vocalisations. Evidence of progress to adult-like vocal patterns was of two types. First, nestling calls changed into a harsh-sounding call that resembles the adult chatter call, functionally a warning call. Second, fledglings also uttered subsong, and these vocalisations were similar to notes typical of adult male song. When the vocalisations produced by developing young were broken down into their constituent vocal features, we found that the time course of development was not strictly linear. Instead of a unidirectional change through the course of nestling and fledgling life, the trajectories of the vocal features fluctuated through time and sometimes exhibited abrupt changes. These sudden shifts occurred during nestling life as well as at the time of fledging. We speculate on the possible causes of these abrupt transitions. Changes in acoustic features upon fledging appear to be linked to new social functions.     

The development of stimulus‐specific auditory responses requires song exposure in male but not female zebra finches

Juvenile male zebra finches develop their song by imitation. Females do not sing but are attracted to males' songs. With functional magnetic resonance imaging and event‐related potentials we tested how early auditory experience shapes responses in the auditory forebrain of the adult bird. Adult male birds kept in isolation over the sensitive period for song learning showed no consistency in auditory responses to conspecific songs, calls, and syllables. Thirty seconds of song playback each day over development, which is sufficient to induce song imitation, was also sufficient to shape stimulus‐specific responses. Strikingly, adult females kept in isolation over development showed responses similar to those of males that were exposed to songs. We suggest that early auditory experience with songs may be required to tune perception toward conspecific songs in males, whereas in females song selectivity develops even without prior exposure to song. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 2010     

Phylogenetic signal in the song of crests and kinglets (Aves: Regulus)

Territorial song structures are often the most prominent characters for distinguishing closely related taxa among songbirds. Learning processes may cause convergent evolution of passerine songs, but phylogenetic information of acoustic traits can be investigated with the help of molecular phylogenies, which are not affected by cultural evolutionary processes. We used a phylogeny based on cytochrome b sequences to trace the evolution of territorial song within the genus Regulus. Five discrete song units are defined as basic components of regulid song via sonagraphic measurements. Traits of each unit are traced on a molecular tree and a mean acoustic character difference between taxon pairs is calculated. Acoustic divergence between regulid taxa correlates strongly with genetic distances. Syntax features of complete songs and of single units are most consistent with the molecular data, whereas the abundance of certain element types is not. Whether song characters are innate or learned was interpreted using hand-reared birds in aviary experiments. We found that convergent character evolution seems to be most probable for learned acoustic traits. We conclude that syntax traits of whole verses or subunits of territorial song, especially innate song structures, are the most reliable acoustic traits for phylogenetic reconstructions in Regulus.     

Neural correlates of experience-induced deficits in learned vocal communication

Songbirds are one of the few vertebrate groups (including humans) that evolved the ability to learn vocalizations. During song learning, social interactions with adult models are crucial and young songbirds raised without direct contacts with adults typically produce abnormal songs showing phonological and syntactical deficits. This raises the question of what functional representation of their vocalizations such deprived animals develop. Here we show that young starlings that we raised without any direct contact with adults not only failed to differentiate starlings' typical song classes in their vocalizations but also failed to develop differential neural responses to these songs. These deficits appear to be linked to a failure to acquire songs' functions and may provide a model for abnormal development of communicative skills, including speech.     

Difficulties when assessing birdsong learning programmes under field conditions: a re-evaluation of song repertoire flexibility in the great tit

There is a remarkable diversity of song-learning strategies in songbirds. Establishing whether a species is closed- or open-ended is important to be able to interpret functional and evolutionary consequences of variation in repertoire size. Most of our knowledge regarding the timing of vocal learning is based on laboratory studies, despite the fact that these may not always replicate the complex ecological and social interactions experienced by birds in the wild. Given that field studies cannot provide the experimental control of laboratory studies, it may not be surprising that species such as the great tit that were initially assumed to be closed-ended learners have later been suggested to be open-ended learners. By using an established colour-ringed population, by following a standardized recording protocol, and by taking into account the species' song ecology (using only recordings obtained during peak of singing at dawn), we replicated two previous studies to assess song repertoire learning and flexibility in adult wild great tits elicited by social interactions. First, we performed a playback experiment to test repertoire plasticity elicited by novel versus own songs. Additionally, in a longitudinal study, we followed 30 males in two consecutive years and analysed whether new neighbours influenced any change in the repertoire. Contrary to the previous studies, song repertoire size and composition were found to be highly repeatable both between years and after confrontation with a novel song. Our results suggest that great tits are closed-ended learners and that their song repertoire probably does not change during adulthood. Methodological differences that may have led to an underestimation of the repertoires or population differences may explain the discrepancy in results with previous studies. We argue that a rigorous and standardized assessment of the repertoire is essential when studying age- or playback-induced changes in repertoire size and composition under field conditions.