Vocal Learning In Songbirds Research Articles

The hidden fitness of the male zebra finch courtship song.

Vocal learning in songbirds is thought to have evolved through sexual selection, with female preference driving males to develop large and varied song repertoires1-3. However, many songbird species learn only a single song in their lifetime4. How sexual selection drives the evolution of single-song repertoires is not known. Here, by applying dimensionality-reduction techniques to the singing behaviour of zebra finches (Taeniopygia guttata), we show that syllable spread in low-dimensional feature space explains how single songs function as honest indicators of fitness. We find that this Gestalt measure of behaviour captures the spectrotemporal distinctiveness of song syllables in zebra finches; that females strongly prefer songs that occupy more latent space; and that matching path lengths in low-dimensional space is difficult for young males. Our findings clarify how simple vocal repertoires may have evolved in songbirds and indicate divergent strategies for how sexual selection can shape vocal learning.

A brain circuit regulates vocal learning in songbirds

A brain circuit regulates vocal learning in songbirds

Forebrain nuclei linked to woodpecker territorial drum displays mirror those that enable vocal learning in songbirds.

Vocal learning is thought to have evolved in 3 orders of birds (songbirds, parrots, and hummingbirds), with each showing similar brain regions that have comparable gene expression specializations relative to the surrounding forebrain motor circuitry. Here, we searched for signatures of these same gene expression specializations in previously uncharacterized brains of 7 assumed vocal non-learning bird lineages across the early branches of the avian family tree. Our findings using a conserved marker for the song system found little evidence of specializations in these taxa, except for woodpeckers. Instead, woodpeckers possessed forebrain regions that were anatomically similar to the pallial song nuclei of vocal learning birds. Field studies of free-living downy woodpeckers revealed that these brain nuclei showed increased expression of immediate early genes (IEGs) when males produce their iconic drum displays, the elaborate bill-hammering behavior that individuals use to compete for territories, much like birdsong. However, these specialized areas did not show increased IEG expression with vocalization or flight. We further confirmed that other woodpecker species contain these brain nuclei, suggesting that these brain regions are a common feature of the woodpecker brain. We therefore hypothesize that ancient forebrain nuclei for refined motor control may have given rise to not only the song control systems of vocal learning birds, but also the drumming system of woodpeckers.

Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain.

Songbirds and humans share the ability to adaptively modify their vocalizations based on sensory feedback. Prior studies have focused primarily on the role that auditory feedback plays in shaping vocal output throughout life. In contrast, it is unclear how non-auditory information drives vocal plasticity. Here, we first used a reinforcement learning paradigm to establish that somatosensory feedback (cutaneous electrical stimulation) can drive vocal learning in adult songbirds. We then assessed the role of a songbird basal ganglia thalamocortical pathway critical to auditory vocal learning in this novel form of vocal plasticity. We found that both this circuit and its dopaminergic inputs are necessary for non-auditory vocal learning, demonstrating that this pathway is critical for guiding adaptive vocal changes based on both auditory and somatosensory signals. The ability of this circuit to use both auditory and somatosensory information to guide vocal learning may reflect a general principle for the neural systems that support vocal plasticity across species.

Developmentally regulated pathways for motor skill learning in songbirds.

Vocal learning in songbirds is mediated by cortico-basal ganglia circuits that govern diverse functions during different stages of development. We investigated developmental changes in axonal projections to and from motor cortical regions that underlie learned vocal behavior in juvenile zebra finches (Taeniopygia guttata). Neurons in LMAN-core project to RA, a motor cortical region that drives vocal output; these RA-projecting neurons send a transient collateral projection to AId, a region adjacent to RA, during early vocal development. Both RA and AId project to a region of dorsal thalamus (DLM), which forms a feedback pathway to cortico-basal ganglia circuitry. These projections provide pathways conveying efference copy and a means by which information about vocal motor output could be reintegrated into cortico-basal ganglia circuitry, potentially aiding in the refinement of juvenile vocalizations during learning. We used tract-tracing techniques to label the projections of LMAN-core to AId and of RA to DLM in juvenile songbirds. The volume and density of terminal label in the LMAN-core→AId projection declined substantially during early stages of sensorimotor learning. In contrast, the RA→DLM projection showed no developmental change. The retraction of LMAN-core→AId axon collaterals indicates a loss of efference copy to AId and suggests that projections that are present only during early stages of sensorimotor learning mediate unique, temporally restricted processes of goal-directed learning. Conversely, the persistence of the RA→DLM projection may serve to convey motor information forward to the thalamus to facilitate song production during both learning and maintenance of vocalizations.

Evolving the capacity for socially guided vocal learning in songbirds: a preliminary study.

Socially guided vocal learning, the ability to use contingent reactions from social partners to guide immature vocalizations to more mature forms, is thought to be a rare ability known to be used only by humans, marmosets and two unrelated songbird species (brown-headed cowbirds and zebra finches). However, this learning strategy has never been investigated in the vast majority of species that are known to modify their vocalizations over development. We propose a novel, preliminary evolutionary modelling approach that uses ecological, reproductive and developmental traits to predict which species may incorporate social influences as part of their vocal learning system. We demonstrate our model using data from 28 passerines. We found three highly predictive traits: temporal overlap between sensory (memorization) and sensorimotor (practice) phases of song learning, song used for mate attraction, and social gregariousness outside the breeding season. Species with these traits were distributed throughout the clade, suggesting that a trait-based approach may yield new insights into the evolution of learning strategies that cannot be gleaned from phylogenetic relatedness alone. Our model suggests several previously uninvestigated and unexpected species as likely socially guided vocal learners and offers new insight into the evolution and development of vocal learning. This article is part of the theme issue 'Vocal learning in animals and humans'.

Vocal learning in songbirds: the role of syllable order in song recognition.

Songbird vocal learning has interesting behavioural and neural parallels with speech acquisition in human infants. Zebra finch males sing one unique song that they imitate from conspecific males, and both sexes learn to recognize their father's song. Although males copy the stereotyped syllable sequence of their father's song, the role of sequential information in recognition remains unclear. Here, we investigated father's song recognition after changing the serial order of syllables (switching the middle syllables, first and last syllables, or playing all syllables in inverse order). Behavioural approach and call responses of adult male and female zebra finches to their father's versus unfamiliar songs in playback tests demonstrated significant recognition of father's song with all syllable-order manipulations. We then measured behavioural responses to normal versus inversed-order father's song. In line with our first results, the subjects did not differentiate between the two. Interestingly, when males' strength of song learning was taken into account, we found a significant correlation between song imitation scores and the approach responses to the father's song. These findings suggest that syllable sequence is not essential for recognition of father's song in zebra finches, but that it does affect responsiveness of males in proportion to the strength of vocal learning.This article is part of the theme issue ‘Vocal learning in animals and humans’.

Neuroanatomy of the grey seal brain: bringing pinnipeds into the neurobiological study of vocal learning.

Comparative animal studies of complex behavioural traits, and their neurobiological underpinnings, can increase our understanding of their evolution, including in humans. Vocal learning, a potential precursor to human speech, is one such trait. Mammalian vocal learning is under-studied: most research has either focused on vocal learning in songbirds or its absence in non-human primates. Here, we focus on a highly promising model species for the neurobiology of vocal learning: grey seals (Halichoerus grypus). We provide a neuroanatomical atlas (based on dissected brain slices and magnetic resonance images), a labelled MRI template, a three-dimensional model with volumetric measurements of brain regions, and histological cortical stainings. Four main features of the grey seal brain stand out: (i) it is relatively big and highly convoluted; (ii) it hosts a relatively large temporal lobe and cerebellum; (iii) the cortex is similar to that of humans in thickness and shows the expected six-layered mammalian structure; (iv) there is expression of FoxP2 present in deeper layers of the cortex; FoxP2 is a gene involved in motor learning, vocal learning, and spoken language. Our results could facilitate future studies targeting the neural and genetic underpinnings of mammalian vocal learning, thus bridging the research gap from songbirds to humans and non-human primates. Our findings are relevant not only to vocal learning research but also to the study of mammalian neurobiology and cognition more in general. This article is part of the theme issue 'Vocal learning in animals and humans'.

Vocal learning in Savannah sparrows: acoustic similarity to neighbours shapes song development and territorial aggression

Vocal learning is a biologically rare adaptation that underpins both human language and the songs of songbirds. The adaptive value of vocal learning in birds is still poorly understood, but a growing body of literature suggests that vocal learning allows songbirds to gain a fitness advantage by adopting songs that are structurally similar to the songs of individuals in neighbouring breeding territories. In this study, we investigate patterns of song development, acoustic similarity, and territorial aggression in Savannah sparrows, Passerculus sandwichensis. Four years of field data reveal that Savannah sparrows routinely overproduce songs during development; more than half of young males sang more than one song type early in their first breeding season, before their repertoire underwent attrition to a single song that males maintained throughout the remainder of their lives. We also found that the attrition of song types is a selective process, with males retaining songs that are similar to the songs of their territorial neighbours. Males that sang songs that were more similar to their neighbours may have faced lower levels of territorial aggression, as indicated by lower numbers of aggressive calls. Our results provide support for the hypothesis that vocal learning in songbirds allows animals to produce songs that match territorial neighbours, possibly providing a benefit in terms of decreased aggression during territorial defence.

Bilateral brain activity in auditory regions is necessary for successful vocal learning in songbirds

In humans and songbirds, neuronal activation for language and song shifts from bilateral- or diffuse-activation to left-hemispheric dominance while proficiency increases. Further parallels exist at the behavioural level: unstructured juvenile vocalizations become highly stereotyped adult vocalizations through a process of trial and error learning. Greater left-hemispheric dominance in the songbird caudomedial Nidopallium (NCM), a Wernicke-like region, is related to better imitation of the tutor’s song learned early in development, indicating a role for the left NCM in forming auditory memories. Here, we hypothesize that inhibition of the left NCM during interaction with a song tutor would impair imitation of the tutor’s song more than inhibition of the right NCM. We infused a transient sodium channel blocker (TTX) immediately prior to tutoring sessions in either the left or right auditory lobule of previously isolated juvenile male zebra finches (Taeniopygia guttata). Upon maturation, both right-infused and left-infused birds' tutor song imitation was significantly impaired. Left-infused birds also showed less consistency in the rhythmic stability of their song as well as increased pitch, suggesting a subtle division of function between the left and right auditory lobules.

Learning is enhanced by tailoring instruction to individual genetic differences.

It is widely argued that personalized instruction based on individual differences in learning styles or genetic predispositions could improve learning outcomes. However, this proposition has resisted clear demonstration in human studies, where it is difficult to control experience and quantify outcomes. Here, we take advantage of the tractable nature of vocal learning in songbirds (Lonchura striata domestica) to test the idea that matching instruction to individual genetic predispositions can enhance learning. We use both cross-fostering and computerized instruction with synthetic songs to demonstrate that matching the tutor song to individual predispositions can improve learning across genetic backgrounds. Moreover, we find that optimizing instruction in this fashion can equalize learning differences across individuals that might otherwise be construed as genetically determined. Our results demonstrate potent, synergistic interactions between experience and genetics in shaping song, and indicate the likely importance of such interactions for other complex learned behaviors.

Discrete Evaluative and Premotor Circuits Enable Vocal Learning in Songbirds

Virtuosic motor performance requires the ability to evaluate and modify individual gestures within a complex motor sequence. Where and how the evaluative and premotor circuits operate within the brain to enable such temporally precise learning is poorly understood. Songbirds can learn to modify individual syllables within their complex vocal sequences, providing a system for elucidating the underlying evaluative and premotor circuits. We combined behavioral and optogenetic methods to identify 2 afferents to the ventral tegmental area (VTA) that serve evaluative roles in syllable-specific learning and to establish that downstream cortico-basal ganglia circuits serve a learning role that is only premotor. Furthermore, song performance-contingent optogenetic stimulation of either VTA afferent was sufficient to drive syllable-specific learning, and these learning effects were of opposite valence. Finally, functional, anatomical, and molecular studies support the idea that these evaluative afferents bidirectionally modulate VTA dopamine neurons to enable temporally precise vocal learning.

Developmental Manipulations of Female Social Feedback Reveal Nonimitative Mechanisms of Vocal Learning in Songbirds

Learning of song in birds provides a powerful model for human speech development. However, the degree to which songbirds and humans share social mechanisms of vocal learning is unknown. Although it has been demonstrated as a vocal learning mechanism in human infants, learning via active social feedback is considered rare and atypical among non-human animals. We report here the first evidence that song learning in the zebra finch (Taeniopygia guttata), the most common model species of vocal learning and development, utilizes socially guided vocal learning. We demonstrate experimentally that the songs of juvenile zebra finches are guided towards mature vocal forms by real-time visual feedback from adult females that is contingent on their early, immature vocalizations. Using a video playback paradigm, we found that juvenile birds that received non-vocal female feedback contingently on their immature song learned significantly better and more accurate song than did yoked controls that received identical but non-contingent feedback. Both contingent and non-contingent groups sang at similar rates. Thus we have provided the first evidence suggesting that non-imitative social learning is a crucial, potentially widespread mechanism of vocal development, and have established a foundational parallel between humans and our most ubiquitous animal model of vocal learning – the crucial role of social feedback to immature vocalizations in the development of communication.

Inter- and intra-specific differences in muscarinic acetylcholine receptor expression in the neural pathways for vocal learning in songbirds.

Acetylcholine receptors (AChRs) abound in the central nervous system of vertebrates. Muscarinic AChRs (mAChRs), a functional subclass of AChRs, mediate neuronal responses via intracellular signal transduction. They also play roles in sensorimotor coordination and motor skill learning by enhancing cortical plasticity. Learned birdsong is a complex motor skill acquired through sensorimotor coordination during a critical period. However, the functions of AChRs in the neural circuits for vocal learning and production remain largely unexplored. Here, we report the unique expression of mAChRs subunits (chrm2-5) in the song nuclei of zebra finches. The expression of excitatory subunits (chrm3 and chrm5) was downregulated in the song nuclei compared with the surrounding brain regions. In contrast, the expression of inhibitory mAChRs (chrm2 and chrm4) was upregulated in the premotor song nucleus HVC relative to the surrounding nidopallium. Chrm4 showed developmentally different expression in HVC during the critical period. Compared with chrm4, individual differences in chrm2 expression emerged in HVC early in the critical period. These individual differences in chrm2 expression persisted despite testosterone administration or auditory deprivation, which altered the timing of song stabilization. Instead, the variability in chrm2 expression in HVC correlated with parental genetics. In addition, chrm2 expression in HVC exhibited species differences and individual variability among songbird species. These results suggest that mAChRs play an underappreciated role in the development of species and individual differences in song patterns by modulating the excitability of HVC neurons, providing a potential insight into the gating of auditory responses in HVC neurons.

Vocal practice regulates singing activity-dependent genes underlying age-independent vocal learning in songbirds.

The development of highly complex vocal skill, like human language and bird songs, is underlain by learning. Vocal learning, even when occurring in adulthood, is thought to largely depend on a sensitive/critical period during postnatal development, and learned vocal patterns emerge gradually as the long-term consequence of vocal practice during this critical period. In this scenario, it is presumed that the effect of vocal practice is thus mainly limited by the intrinsic timing of age-dependent maturation factors that close the critical period and reduce neural plasticity. However, an alternative, as-yet untested hypothesis is that vocal practice itself, independently of age, regulates vocal learning plasticity. Here, we explicitly discriminate between the influences of age and vocal practice using a songbird model system. We prevented zebra finches from singing during the critical period of sensorimotor learning by reversible postural manipulation. This enabled to us to separate lifelong vocal experience from the effects of age. The singing-prevented birds produced juvenile-like immature song and retained sufficient ability to acquire a tutored song even at adulthood when allowed to sing freely. Genome-wide gene expression network analysis revealed that this adult vocal plasticity was accompanied by an intense induction of singing activity-dependent genes, similar to that observed in juvenile birds, rather than of age-dependent genes. The transcriptional changes of activity-dependent genes occurred in the vocal motor robust nucleus of the arcopallium (RA) projection neurons that play a critical role in the production of song phonology. These gene expression changes were accompanied by neuroanatomical changes: dendritic spine pruning in RA projection neurons. These results show that self-motivated practice itself changes the expression dynamics of activity-dependent genes associated with vocal learning plasticity and that this process is not tightly linked to age-dependent maturational factors.

The cerebellum influences vocal timing

A circuit pathway from the cerebellum to the basal ganglia contributes to vocal learning in songbirds.

Chance, long tails, and inference in a non-Gaussian, Bayesian theory of vocal learning in songbirds

Traditional theories of sensorimotor learning posit that animals use sensory error signals to find the optimal motor command in the face of Gaussian sensory and motor noise. However, most such theories cannot explain common behavioral observations, for example, that smaller sensory errors are more readily corrected than larger errors and large abrupt (but not gradually introduced) errors lead to weak learning. Here, we propose a theory of sensorimotor learning that explains these observations. The theory posits that the animal controls an entire probability distribution of motor commands rather than trying to produce a single optimal command and that learning arises via Bayesian inference when new sensory information becomes available. We test this theory using data from a songbird, the Bengalese finch, that is adapting the pitch (fundamental frequency) of its song following perturbations of auditory feedback using miniature headphones. We observe the distribution of the sung pitches to have long, non-Gaussian tails, which, within our theory, explains the observed dynamics of learning. Further, the theory makes surprising predictions about the dynamics of the shape of the pitch distribution, which we confirm experimentally.

Vocal learning in songbirds requires cholinergic signaling in a motor cortex-like nucleus.

Cholinergic inputs to cortex modulate plasticity and sensory processing, yet little is known about their role in motor control. Here, we show that cholinergic signaling in a songbird vocal motor cortical area, the robust nucleus of the arcopallium (RA), is required for song learning. Reverse microdialysis of nicotinic and muscarinic receptor antagonists into RA in juvenile birds did not significantly affect syllable timing or acoustic structure during vocal babbling. However, chronic blockade over weeks reduced singing quantity and impaired learning, resulting in an impoverished song with excess variability, abnormal acoustic features, and reduced similarity to tutor song. The demonstration that cholinergic signaling in a motor cortical area is required for song learning motivates the songbird as a tractable model system to identify roles of the basal forebrain cholinergic system in motor control. NEW & NOTEWORTHY Cholinergic inputs to cortex are evolutionarily conserved and implicated in sensory processing and synaptic plasticity. However, functions of cholinergic signals in motor areas are understudied and poorly understood. Here, we show that cholinergic signaling in a songbird vocal motor cortical area is not required for normal vocal variability during babbling but is essential for developmental song learning. Cholinergic modulation of motor cortex is thus required for learning but not for the ability to sing.

MiR-9 regulates basal ganglia-dependent developmental vocal learning and adult vocal performance in songbirds.

miR-9 is an evolutionarily conserved miRNA that is abundantly expressed in Area X, a basal ganglia nucleus required for vocal learning in songbirds. Here, we report that overexpression of miR-9 in Area X of juvenile zebra finches impairs developmental vocal learning, resulting in a song with syllable omission, reduced similarity to the tutor song, and altered acoustic features. miR-9 overexpression in juveniles also leads to more variable song performance in adulthood, and abolishes social context-dependent modulation of song variability. We further show that these behavioral deficits are accompanied by downregulation of FoxP1 and FoxP2, genes that are known to be associated with language impairments, as well as by disruption of dopamine signaling and widespread changes in the expression of genes that are important in circuit development and functions. These findings demonstrate a vital role for miR-9 in basal ganglia function and vocal communication, suggesting that dysregulation of miR-9 in humans may contribute to language impairments and related neurodevelopmental disorders.

Genetic variation interacts with experience to determine interindividual differences in learned song

Learning reflects the influence of experience on genetically determined circuitry, but little is known about how experience and genetics interact to determine complex learned phenotypes. Here, we used vocal learning in songbirds to study how experience and genetics contribute to interindividual differences in learned song. Previous work has established that such differences in song within a species depend on learning, but in principle some of these differences could also depend on genetic variation. We focused on song tempo, a learned and quantifiable feature that is controlled by central neural circuitry. To identify genetic contributions to tempo we computer-tutored juvenile Bengalese finches (Lonchura striata domestica) from different genetic backgrounds with synthetic songs in which tempo was systematically varied. Computer-tutored birds exhibited unexpectedly strong heritability for song tempo and comparatively weak influence of experience. We then tested whether heritability was fixed and independent of experience by providing a second group of birds with enriched instruction via live social tutoring. Live tutoring resulted in not only a significant increase in the influence of experience on tempo but also a dramatic decrease in the influence of genetics, indicating that enriched instruction could overcome genetic biases evident under computer tutoring. Our results reveal strong heritable genetic contributions to interindividual variation in song tempo but that the degree of heritability depends profoundly on the quality of instruction. They suggest that for more complex learned phenotypes, where it can be difficult to identify and control relevant experiential variables, heritability may similarly be contingent on the specifics of experience.