Song Learning Process Research Articles

Song learning and plasticity in songbirds.

Birdsong provides a fascinating system to study both behavioral and neural plasticity. Oscine songbirds learn to sing, exhibiting behavioral plasticity both during and after the song-learning process. As a bird learns, its song progresses from a plastic and highly variable vocalization into a more stereotyped, crystallized song. However, even after crystallization, song plasticity can occur: some species' songs become more stereotyped over time, whereas other species can incorporate new song elements. Alongside the changes in song, songbirds' brains are also plastic. Both song and neural connections change with the seasons in many species, and new neurons can be added to the song system throughout life. In this review, we highlight important research on behavioral and neural plasticity at multiple timescales, from song development in juveniles to lifelong modifications of learned song.

Gene manipulation to test links between genome, brain and behavior in developing songbirds: a test case.

Songbird research has made many seminal contributions to the fields of ethology, endocrinology, physiology, ecology, evolution and neurobiology. Genome manipulation is thus a promising new methodological strategy to enhance the existing strengths of the songbird system to advance and expand fundamental knowledge of how genetic sequences and regulation of genomic function support complex natural learned behaviors. In zebra finches (Taeniopygia guttata) in particular, a rich set of questions about the complex process of developmental song learning in juvenile males has been defined. This Review uses one area of zebra finch song learning to demonstrate how genome editing can advance causal investigations into known genome-brain-behavior relationships. Given the number and diversity of songbird species, comparative work leveraging genome manipulation would expand the influence of these birds in additional fields of ecology and evolution for song learning and other behaviors.

Hemispheric asymmetry of calbindin-positive neurons is associated with successful song imitation

The plasticity that facilitates learning during critical (sensitive) periods in development is tightly regulated by inhibitory neurons. Song acquisition in birds is one example of a learning process that occurs during a sensitive period early in development. Sensory experience with a song ‘tutor’ during this sensitive period prunes excitatory and inhibitory synapses in the song production nucleus HVC (proper noun). Neurons in the caudomedial nidopallium (NCM), a secondary auditory region, lose their tutor song selectivity when gamma-aminobutyric acid (GABA) signaling is blocked. Given the importance of inhibition in the song learning process, we investigated whether individual differences in learning outcomes can be explained by the distribution of specific populations of (mostly) inhibitory neurons in HVC and NCM. We measured the densities of distinct neuronal populations (defined by their expression of the calcium-binding proteins calbindin, calretinin, and parvalbumin) in these two regions. We found that lateralization of calbindin-positive neurons was related to successful song learning: good learners were characterized by hemispheric asymmetry of calbindin-positive neurons in the medial NCM (fewer CB+ neurons in the left hemisphere), whereas poor learners did not show any asymmetry. In contrast, the density of all three neuronal populations in HVC did not differ between good and poor learners. These findings not only identify a specific (presumably) inhibitory cell type (calbindin-expressing neurons) that is related to song learning, but also emphasize the role of hemispheric asymmetry in auditory memory formation.

Vocal Learning: Shaping by Social Reinforcement

Animals modulate their behavior by interacting with others. Nevertheless, popular theories of vocal learning frequently overlook the role of ongoing social interactions. New research suggests that a social feedback loop between young male zebra finches and adult females guides the process of song learning.

Volumetric development of the zebra finch brain throughout the first 200 days of post-hatch life traced by in vivo MRI

The first months of life are characterized by massive neuroplastic processes that parallel the acquisition of skills and abilities vital for proper functioning in later life. Likewise, juvenile songbirds learn the song sung by their tutor during the first months after hatching. To date, most studies targeting brain development in songbirds exclusively focus on the song control and auditory pathways. To gain a comprehensive insight into structural developmental plasticity of the entire zebra finch brain throughout the different subphases of song learning, we designed a longitudinal study in a group of male (16) and female (19) zebra finches. We collected T2-weighted 3-dimensional anatomical scans at six developmental milestones throughout the process of song learning, i.e. 20, 30, 40, 65, 90 and 120 days post hatching (dph), and one additional time point well after song crystallization, i.e. 200 dph. We observed that the total brain volume initially increases, peaks around 30–40 dph and decreases towards the end of the study. Further, we performed brain-wide voxel-based volumetric analyses to create spatio-temporal maps indicating when specific brain areas increase or decrease in volume, relative to the subphases of song learning. These maps informed (1) that most areas implicated in song control change early, i.e. between 20 and 65 dph, and are embedded in large clusters that cover major subdivisions of the zebra finch brain, (2) that volume changes between consecutive subphases of vocal learning appear highly similar in males and females, and (3) that only more rostrally situated brain regions change in volume towards later ages. Lastly, besides detecting sex differences in local tissue volume that align with previous studies, we uncovered two additional brain loci that are larger in male compared to female zebra finches. These volume differences co-localize with areas related to the song control and auditory pathways and can therefore be associated to the behavioral difference as only male zebra finches sing. In sum, our data point to clear heterochronous patterns of brain development similar to brain development in mammalian species and this work can serve as a reference for future neurodevelopmental imaging studies in zebra finches.

Neurotensin and neurotensin receptor 1 mRNA expression in song-control regions changes during development in male zebra finches.

Learned vocalizations are important for communication in some vertebrate taxa. The neural circuitry for the learning and production of vocalizations is well known in songbirds, many of which learn songs initially during a critical period early in life. Dopamine is essential for motor learning, including song learning, and dopamine-related measures change throughout development in song-control regions such as HVC, the lateral magnocellular nucleus of the anterior nidopallium (LMAN), Area X, and the robust nucleus of the arcopallium (RA). In mammals, the neuropeptide neurotensin strongly interacts with dopamine signaling. This study investigated a potential role for the neurotensin system in song learning by examining how neurotensin (Nts) and neurotensin receptor 1 (Ntsr1) expression change throughout development. Nts and Ntsr1 mRNA expression was analyzed in song-control regions of male zebra finches in four stages of the song learning process: pre-subsong (25 days posthatch; dph), subsong (45 dph), plastic song (60 dph), and crystallized song (130 dph). Nts expression in LMAN during the subsong stage was lower compared to other time points. Ntsr1 expression was highest in HVC, Area X, and RA during the pre-subsong stage. Opposite and complementary expression patterns for the two genes in song nuclei and across the whole brain suggest distinct roles for regions that produce and receive Nts. The expression changes at crucial time points for song development are similar to changes observed in dopamine studies and suggest Nts may be involved in the process of vocal learning. © 2018 Wiley Periodicals, Inc. Develop Neurobiol 78: 671-686, 2018.

Seasonal plasticity of song behavior relies on motor and syntactic variability induced by a basal ganglia–forebrain circuit

The plasticity of nervous systems allows animals to quickly adapt to a changing environment. In particular, seasonal plasticity of brain structure and behavior is often critical to survival or mating in seasonal climates. Songbirds provide striking examples of seasonal changes in neural circuits and vocal behavior and have emerged as a leading model for adult brain plasticity. While seasonal plasticity and the well-characterized process of juvenile song learning may share common neural mechanisms, the extent of their similarity remains unclear. Especially, it is unknown whether the basal ganglia (BG)–forebrain loop which implements song learning in juveniles by driving vocal exploration participates in seasonal plasticity. To address this issue, we performed bilateral lesions of the output structure of the song-related BG–forebrain circuit (the magnocellular nucleus of the anterior nidopallium) in canaries during the breeding season, when song is most stereotyped, and just after resuming singing in early fall, when canaries sing their most variable songs and may produce new syllable types. Lesions drastically reduced song acoustic variability, increased song and phrase duration, and decreased syntax variability in early fall, reverting at least partially seasonal changes observed between the breeding season and early fall. On the contrary, lesions did not affect singing behavior during the breeding season. Our results therefore indicate that the BG–forebrain pathway introduces acoustic and syntactic variability in song when canaries resume singing in early fall. We propose that BG–forebrain circuits actively participate in seasonal plasticity by injecting variability in behavior during non-breeding season. Significance StatementThe study of seasonal plasticity in temperate songbirds has provided important insights into the mechanisms of structural and functional plasticity in the central nervous system. The precise function and mechanisms of seasonal song plasticity however remain poorly understood. We show here that a basal ganglia–forebrain circuit involved in the acquisition and maintenance of birdsong is actively inducing song variability outside the breeding season, when singing is most variable, while having little effect on the stereotyped singing during the breeding season. Our results suggest that seasonal plasticity reflects an active song-maintenance process akin to juvenile learning, and that basal ganglia–forebrain circuits can drive plasticity in a learned vocal behavior during the non–injury-induced degeneration and reconstruction of the neural circuit underlying its production.

Birdsong learning as a social process

This paper describes a 30-year investigation into the role of social and ecological factors affecting song learning in song sparrows, Melospiza melodia. It addresses the question of why song sparrows learn the songs they do, given that they are exposed to many more songs than they will keep for their final repertoire of 7–11 song types. A young song sparrow moves from his natal area at about 1 month of age, eventually settling in an area where he learns the songs of the resident males and attempts to establish his own territory. Birds that share many songs with their neighbours in their first breeding season (the spring following their hatch summer) survive for more years on territory than birds that do not. Many features of the song-learning process lead to a high level of sharing with first-year neighbours, including preferentially learning the songs of their tutor-neighbours who survive the winter, and learning songs that are shared by several tutors. Social interaction appears to be critical in song learning, but indirect effects (eavesdropping on adults countersinging) seem to be at least as important as direct interaction between the young bird and his tutor-neighbours. Although our evidence suggests that the song-learning strategy of young song sparrows is beneficial to them, a preliminary analysis suggests it may not benefit their tutors.

Effects of fragmentation and hybridization on geographical patterns of song variation in the endangered Yellow Cardinal Gubernatrix cristata

The song learning process may lead to small‐scale geographical variation in vocalizations of oscine birds. This variation can be further enhanced by the effects of habitat fragmentation or hybridization. Populations of the endangered Yellow Cardinal Gubernatrix cristata are now patchily distributed in the southern South American thorny shrubland forests and are small as a consequence of the pressure exerted by increased habitat transformation and illegal trade. We study the Yellow Cardinal's vocalizations throughout its distribution and assess how habitat characteristics and fragmentation, as well as hybridization with the Common Diuca Diuca diuca, have affected song patterns of different populations. We expected to find song differences among populations and songs to be more similar to those of the Common Diuca in areas where hybridization occurs. Multivariate analyses revealed significant differences in song between the four populations studied and confirmed that songs are more similar to those of Common Diuca where hybridization takes place. These results, in conjunction with genetic studies, can help to establish management units that preserve genetic and cultural variation in this endangered species.

Habitat fragmentation effects and variations in repertoire size and degree of song sharing among close Dupont’s Lark Chersophilus duponti populations

We describe the song type repertoire variation and degree of song sharing in three isolated and declining Dupont’s Lark (Chersophilus duponti) populations located close to each other in eastern Spain, studied over two years. We found no differences between sites either in song rate or individual repertoire size. We detected great differences in song type diversity at the population level, ranging from five to 18 song types. We used, for the first time, the SIMPROF test, a method that objectively discriminates significant groups resulting from agglomerative clustering methods, to study geographic variation in bird song. We found four microdialects in the study area with a low degree of song sharing among populations, which may be related to the influence of habitat fragmentation and the song learning process and ecology of the species. We detected different patterns of song sharing among sites. All males of two populations shared about 80–100 % of their song types throughout the habitat patch. At the other site, we found two microdialects within the same habitat patch, where song types were only shared among neighbouring males. The high degree of song sharing found can be explained by the reduced dispersal movements of the species. We also detected a high consistency in the song types between years. The creation of corridors and habitat management in potential habitat patches surrounding Dupont’s Lark populations could act as stepping-stones, improving the connection between populations and thereby song transmission between patches.

Female zebra finches learn to prefer more than one song and from more than one tutor

Birdsong is a culturally transmitted mating signal: young birds learn specific variants of species-specific song(s) from conspecific models. Female song preferences are also learned early in life, but despite the potential functional implications of such learned mating preferences, we still have a poor understanding of when and from whom females learn. This also holds true for one of the foremost models of vocal learning, the zebra finch, Taeniopygia guttata. Both male and female zebra finches memorize their tutor's song motif: as adults, males will sing and females prefer their tutor's song. We here tested whether juvenile females would also learn to prefer the songs of several individuals, and whether the timing and propensity of song preference learning were condition dependent. Young females raised and cross-fostered in experimentally manipulated brood sizes were exposed to several model songs: first their foster father's song until nutritional independence (days 0e35) and then as subadults to playbacks of two different tutor songs (days 35e65). As adults, females preferred all three model songs over unfa-miliar songs. There were no interaction effects between females' early rearing conditions (brood size) and preference strength for the different tutor songs. An additional live-tutored group had equally strong preferences for the foster father's song (only heard before day 35) as the tape-tutored females. The combined results demonstrate that subadult females memorize several song types during different times of development and as adults prefer these songs over unfamiliar songs. These findings imply that multiple song learning needs to be taken into account for avian mate choice studies even in species that lack song type repertoires but show individual differences in song. O 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Learned mating preferences are increasingly recognized as an evolutionary force but to estimate their qualitative and quantitative impact on population dynamics, the strength and direction of learned versus experience-dependent preferences need to be bet-ter documented (e.g. Verzijden et al., 2012) in order to improve modelling approaches (Lachlan & Nowicki, 2012). In songbirds (oscines), (learned) song is an important mating signal (Catchpole & Slater, 2008) but while the process of (male) song learning is relatively well studied, our understanding of female song produc-tion and preference learning lags behind in all aspects (Kroodsma, Vielliard, & Stiles, 1996; Riebel, 2003b; Riebel, Hall, & Langmore, 2005) although the 'when' and 'from whom' females learn their preferences have turned out to be crucial parameters in theoretical models for the evolution of learned birdsong (Lachlan & Nowicki, 2012; Ritchie, Kirby, & Hawkey, 2008). Zebra finches, Taeniopygia guttata, are one of the few species in which song acquisition in females has seen some systematic study (for reviews see Riebel, 2003a, 2009). Complex courtship song in zebra finches is pro-duced only by adult males: each male sings an individually distinctive song motif that closely resembles an adult song model (the 'tutor song'). As shown by sequential exposure to different tutors, the peak of the sensitive phase for (male) song production learning is between 35 and 65 days posthatching (Slater, Eales, & Clayton, 1988). Although females do not sing, several experi-mental studies have shown that females learn about songs as ju-veniles too: after maturation, which can be as early as 100 days (Zann, 1996), adult females have been shown to prefer the song of the adult male with which they had been housed between 35 and 65 days posthatching over the song of an unfamiliar male, showing cultural transmission of song preferences is possible along nonge-netic lines (Clayton, 1988, 1990; Miller, 1979; Riebel, Smallegange, Terpstra, & Bolhuis, 2002). Song preferences in female zebra finches have been validated as predictors of live male preferences and mating decisions (for a review see Riebel, 2009). Cross-fostering between the subspecies T. g. guttata and T. g. castanostis has shown that females not only learn preferences for specific songs but also generalize some of the subspecies' structural

Developmental ecology

In this article we provide a case history of the development of a communicative system in songbirds. In particular, we explore how brown-headed cowbirds, male and female, cooperate in the development and use of species-typical song. The goal is to show how social interactions between and within sexes create a platform for the production and perception of song. We consider six perspectives. First, we discuss the nature of the acoustic signal. Second, we look at the process of song learning. Third, we describe a specific song mechanism, social shaping. Fourth, we look at the more general developmental process of neophenogenesis. Fifth, we consider the developmental ecology for social learning. Finally, we describe how social networks measures can be used to capture the nature of social interactions as the engines of song learning. Taken as a whole, we argue that culturally transmitted behaviors structure social interactions that predict the acquisition of species' typical behaviors necessary for successful reproduction.

Song Learning in Song Sparrows: Relative Importance of Autumn vs. Spring Tutoring

AbstractWe examined ‘late’ song learning in song sparrows (Melospiza melodia), i.e., song learning that occurs after the first few months, or classical sensitive period, of the natal summer. Fledgling juveniles were brought into the laboratory at 2–3 mo of age and exposed to computer‐simulated song tutors in three different time periods: late in the natal summer, the autumn, and the next spring. As expected, the birds’ final repertoires consisted mostly of songs heard in the field, but 30% of the birds’ songs were influenced by songs heard in the laboratory (selective retention) and another 8% were learned de novo in the laboratory. Parallel results were obtained for a second group of birds who received laboratory tutoring only in the spring. In fact, the results suggested that autumn tutoring may even be inhibitory. We conclude that the songs a young song sparrow hears in his first spring may be critical to his final repertoire development, indicating that the song learning process in song sparrows is longer and more flexible than previously supposed.

Does learning produce song conformity or novelty in white-crowned sparrows, Zonotrichia leucophrys?

Song learning in birds makes it possible for males to faithfully imitate tutors and also to generate novel improvisations. Within local dialects of the Puget Sound white-crowned sparrow, most males share the terminal trill phrase in their songs. In contrast, the introductory note complex is more variable within local populations and appears to encode individual identity. We studied the song-learning process during initial territory establishment in a wild population of white-crowned sparrows. Although most adult males sing a single song type, many yearling males overproduce song types early in their first singing season before deleting all but one song type from their repertoire. We asked whether this attrition process favours retention of a song with a note complex that resembles that of a male's neighbour, as would be predicted by various hypotheses assuming a benefit to song sharing, or whether it favours retention of a distinctive note complex, which would produce individuality in song. We found that males that initially overproduced song types retained shared note complexes, and that these males were more likely to share their adult note complex with neighbours than were young males that did not overproduce. Only 51% of recruits overproduced, however, and we close by speculating that overproduction and close song sharing may be correlates of male quality and learning ability.

Song learning in domesticated canaries in a restricted acoustic environment.

Many songbirds learn their songs early in life from a song model. In the absence of such a model, they develop an improvised song that often lacks the species-typical song structure. Open-ended learners, such as the domesticated canary, are able to modify their songs in adulthood, although the mechanisms that guide and time the song-learning process are still not fully understood. In a previous study, we showed that male domesticated canaries lacking an adult song model in their first year substantially change their song repertoire and composition when exposed to normally reared conspecifics in their second year. Here, we investigate song development in descendants of canaries that were raised and kept as a peer group without a song model. Such males represent tutors with abnormal song characteristics. Interestingly, the F(1) generation developed quite normal song structure, and when brought into an environment with normally raised canaries in their second year, they did not modify their songs substantially. These results suggest that contact with an adult song model early in life is crucial for song crystallization, but also that song development is at least partly guided by innate rules. They also question the existing classification of canaries as open-ended learners.

Selective attrition and individual song repertoire development in song sparrows

We compared the songs of young male song sparrows, Melospiza melodia, in the early ‘plastic’ phase (while the songs may still be modified, or dropped altogether) and in the later ‘crystallized’ phase. Birds in this sample dropped 1–3 songs from their plastic repertoire on their way to a crystallized repertoire of 8–11 songs. Consistent with theory of selective attrition, the songs the young birds tended to drop were songs that matched fewer neighbours and matched them more poorly than the songs they retained. At the same time, however, the birds often modified the songs they retained so that these crystallized versions were less similar to the songs of their neighbours than the plastic versions had been. They were more likely to do this for songs they shared with more neighbours. Thus, the song learning process appears to consist of two opposing processes: a tendency to copy and retain the songs of the birds who will be the young bird's neighbours in the first breeding season; and a tendency to modify at least some of these songs so that they are more individually distinctive.

Songbird genomics: methods, mechanisms, opportunities, and pitfalls.

The biology of songbirds poses fundamental questions about the interplay between gene, brain, and behavior. New tools of genomic analysis will be invaluable in pursuing answers to these questions. This review begins with a summary of the broad properties of the songbird genome and how songbird brain gene expression has been measured in past studies. Four key problems in songbird biology are then considered from a genomics perspective: What role does differential gene expression play in the development, maintenance, and functional organization of the song control circuit? Does gene regulation set boundaries on the process of juvenile song learning? What is the purpose of song-induced gene activity in the adult brain? How does the genome underlie the profound sexual differentiation of the song control circuit? Finally, the range of genomic technologies currently or soon to be available to songbird researchers is briefly reviewed. These technologies include online databases of expressed genes ("expressed sequence tags" or ESTs); a complete library of the zebra finch genome maintained as a bacterial artificial chromosome (BAC) library; DNA microarrays for simultaneous measurement of many genes in a single experiment; and techniques for gene manipulation in the organism. Collectively, these questions and techniques define the field of songbird neurogenomics.

Song development: in search of the error-signal.

Song development provides an opportunity to study the mechanisms of vocal learning dynamically at molecular, cellular and systems levels, and across time scales ranging from minutes to months. To exploit these opportunities one needs to identify appropriate units, types and time scales of vocal change in nearly real time. The previous chapter by Tchernikovski et al. in this volume described techniques that make this research strategy feasible by allowing us to observe the song learning process through a "temporal microscope" with variable degrees of resolution. In this chapter we summarize some of the new observations and raise hypotheses about the learning strategy of the bird. We focus on inferences that can be drawn from behavioral observations to the nature and complexity of the instructive signal that guides the vocal change (error-signal). We examine two effects: i) the emergence of syllable types and ii) changes in features within a syllable type. We found that different features of the same syllable change during different and sometimes disjointed developmental windows. We discuss the possibility that song imitation is achieved by correcting partial errors, and that features of those partial errors change adaptively during development, perhaps concurrently with changes in perception and in motor proficiency. Those hypotheses can be best examined by across levels investigation, starting from identifying critical moments in song development and recording of articulatory dynamics and neural patterns when only a few features of specific syllables undergo rapid changes. Such investigation could relate behavioral events to brain mechanisms that guide song learning from moment-to-moment and across extended periods.

Respiratory units of motor production and song imitation in the zebra finch.

Juvenile male zebra finches (Taeniopygia guttata) learn a stereotyped song by imitating sounds from adult male tutors. Their song is composed of a series of syllables, which are separated by silent periods. How acoustic units of song are translated into respiratory and syringeal motor gestures during the song learning process is not well understood. To learn about the respiratory contribution to the imitation process, we recorded air sac pressure in 38 male zebra finches and compared the acoustic structures and air sac pressure patterns of similar syllables qualitatively and quantitatively. Acoustic syllables correspond to expiratory pressure pulses and most often (74%) entire syllables are copied using similar air sac pressure patterns. Even notes placed within different syllables are generated with similar air sac pressure patterns when only segments of syllables are copied (9%). A few of the similar syllables (17%) are generated with a modified pressure pattern, typically involving addition or deletion of an inspiration. The high similarity of pressure patterns for like syllables indicates that generation of particular sounds is constrained to a narrow range of air sac pressure conditions. Following presentation of stroboscope flashes, song was typically interrupted at the end of an expiratory pressure pulse, confirming that expirations and, therefore, syllables are the smallest unit of motor production of song. Silent periods, which separate syllables acoustically, are generated by switching from expiration to inspiration. Switching between respiratory phases, therefore, appears to play a dominant role in organizing the stereotyped motor program for song production.

The development of within-song type variation in song sparrows

We investigated the development of within-song type variation in song sparrows, Melospiza melodia , with two experiments designed to determine how exposure to within-type variation influences the song-learning process and whether within-type variation itself is a learned trait. In the first experiment, we compared learning between two groups of males, one group tutored exclusively with song models presented with no variation, and the other group tutored exclusively with song models presented with a range of within-type variation that is normally produced by birds in the field. The two groups in this experiment did not differ significantly in any measure of how well they learned, suggesting that exposure to within-type variation has no measurable influence on the learning process overall. Nor did the groups differ in the expression of within-song type variation in their own adult songs, demonstrating that within-type variation is not a learned feature of song sparrow song. In the second experiment, we tutored a single group of birds with both invariant and variable models, allowing us to ask how within-type variability affects learning preferences. Young birds preferentially copied song type models presented with variation significantly more than invariant models. Taken together, these experiments provide insight into the evolution of within-song type variation in song sparrows, although the functional significance of this level of variation and learning preferences based on variation remain enigmatic.