Song Acquisition Research Articles

Weight Transfer in the Reinforcement Learning Model of Songbird Acquisition.

Song acquisition behavior observed in the songbird system provides a notable example of learning through trial- and-error which parallels human speech acquisition. Studying songbird vocal learning can offer insights into mechanisms underlying human language. We present a computational model of song learning that integrates reinforcement learning (RL) and Hebbian learning and agrees with known songbird circuitry. The song circuit outputs activity from nucleus RA, which receives two primary inputs: timing information from area HVC and stochastic activity from nucleus LMAN. Additionally, song learning relies on Area X, a basal ganglia area that receives dopaminergic inputs from VTA. In our model, song is first acquired in the HVC-to-Area X connectivity, employing an RL mechanism that involves node perturbation. This information is then consolidated into HVC-to-RA synapses through a Hebbian mechanism. The transfer of weights from Area X to RA takes place via the thalamus, utilizing a specific form of spike-timing-dependent plasticity (STDP). Thus, we present a computational model grounded in songbird circuitry in which the optimal policy is initially guided by RL and subsequently transferred to another circuit through Hebbian plasticity.

Global analysis of acoustic frequency characteristics in birds.

Animal communication plays a crucial role in biology, yet the wide variability in vocalizations is not fully understood. Previous studies in birds have been limited in taxonomic and analytical breadth. Here, we analyse an extensive dataset of >140 000 recordings of vocalizations from 8450 bird species, representing nearly every avian order and family, under a structural causal model framework, to explore the influence of eco-evolutionary traits on acoustic frequency characteristics. We find that body mass, beak size, habitat associations and geography influence acoustic frequency characteristics, with varying degrees of interaction with song acquisition type. We find no evidence for the influence of vegetation density, sexual dimorphism, range size and competition on our measures of acoustic frequency characteristics. Our results, built on decades of researchers' empirical observations collected across the globe, provide a new breadth of evidence about how eco-evolutionary processes shape bird communication.

Parental developmental experience affects vocal learning in offspring

Cultural and genetic inheritance combine to enable rapid changes in trait expression, but their relative importance in determining trait expression across generations is not clear. Birdsong is a socially learned cognitive trait that is subject to both cultural and genetic inheritance, as well as being affected by early developmental conditions. We sought to test whether early-life conditions in one generation can affect song acquisition in the next generation. We exposed one generation (F1) of nestlings to elevated corticosterone (CORT) levels, allowed them to breed freely as adults, and quantified their son’s (F2) ability to copy the song of their social father. We also quantified the neurogenetic response to song playback through immediate early gene (IEG) expression in the auditory forebrain. F2 males with only one corticosterone-treated parent copied their social father’s song less accurately than males with two control parents. Expression of ARC in caudomedial nidopallium (NCM) correlated with father-son song similarity, and patterns of expression levels of several IEGs in caudomedial mesopallium (CMM) in response to father song playback differed between control F2 sons and those with a CORT-treated father only. This is the first study to demonstrate that developmental conditions can affect social learning and neurogenetic responses in a subsequent generation.

Translocated wild birds are predisposed to learn songs of their ancestral population

Population differences in socially learned mating signals like oscine birdsong are particularly vulnerable to breakdown through dispersal.1 Despite this challenge, geographic variation in learned signals is ubiquitous.2 A proposed explanation for this pattern is that birds express predispositions to selectively learn and produce population-typical songs.3,4,5 While experimental studies on lab-reared birds have shown the existence of within-species learning predispositions,6,7,8,9,10 it remains unclear whether and how learning predispositions influence song acquisition in the wild. Here, we investigated innate song learning predispositions in wild pied flycatchers (Ficedula hypoleuca) by measuring the songs of individuals translocated as eggs from a Dutch population to a breeding population in Sweden. We compared the songs of the adult males hatched from these translocated eggs with those from the ancestral and receiving populations. Songs of translocated males closely resemble the local Swedish songs to which they were exposed during development, supporting the importance of social learning. However, translocated males selectively learned those local Swedish song elements that sound the most "Dutch-like." As a result, their songs are significantly shifted toward those of the ancestral Dutch population. This suggests that innate learning predispositions track ongoing song evolution in wild populations of pied flycatchers. We propose that as songs continue to diverge over time, this coevolutionary relationship between song and learning predispositions may contribute to the emergence of incipient pre-mating barriers.

The Effects of Modeling and Sequence on the Expressivity of Young Voices

Choral method textbooks include various strategies on when and how to introduce expression in song acquisition including vocal modeling. In two previous studies, participants who learned expressive elements early in a song-learning sequence (infused-expression) performed those elements more accurately than those who learned them at the end of the sequence (post-expression). However, the infused-expression sequence had an expressive model throughout, whereas the post-expression sequence had an expressive model only at the beginning and end. The purpose of this study was to remove the modeling variance between sequences. Middle schoolers learned two songs with an expressive model throughout, using two different sequences (infused-expression and post-expression). We found no significant difference in expressive accuracy between sequences. When students learned a song with an expressive model, regardless of sequence, students sang with expression. Teachers should consider always modeling with expression regardless of whether or not the objective of the rehearsal is about expressive elements.

Singing in Class: Analysis of Children Learning a New Song

<p style="text-align:justify">Teaching and learning new songs in class is an integral cultural practice. This paper focuses on a singing lesson and studies the complex relations among the target song, children’s song acquisition and the teacher’s instructions. However, instead of simply examining pitch accuracy or ratings, this paper proposes a novel methodology for analysing song learning in class. First, a transcription method is used to document a video-recorded lesson. Second, syllables are identified as both the essential components of the grammar of songs for children and the fundamental units for analysing singing in terms of pitch, timing and articulation. The individual singing of three children, divided into the syllables of the target song, is examined for these three properties. Third, a comparison between the song model and the children’s singing reveals how rule-breaking in the song corresponds to the children’s difficulties in singing. This detailed and subject-related analysis exemplifies the complex dynamic among the teacher, the object and the learner and is a contribution to the research of subject-related didactics.</p>

RoboFinch: A versatile audio‐visual synchronised robotic bird model for laboratory and field research on songbirds

Abstract Singing in birds is accompanied by beak, head and throat movements. The role of these visual cues has long been hypothesised to be an important facilitator in vocal communication, including social interactions and song acquisition, but has seen little experimental study. To address whether audio‐visual cues are relevant for birdsong we used high‐speed video recording, 3D scanning, 3D printing technology and colour‐realistic painting to create RoboFinch, an open source adult‐mimicking robot which matches temporal and chromatic properties of songbird vision. We exposed several groups of juvenile zebra finches during their song developmental phase to one of six singing robots that moved their beaks synchronised to their song and compared them with birds in a non‐synchronised and two control treatments. Juveniles in the synchronised treatment approached the robot setup from the start of the experiment and progressively increased the time they spent singing, contra to the other treatment groups. Interestingly, birds in the synchronised group seemed to actively listen during tutor song playback, as they sung less during the actual song playback compared to the birds in the asynchronous and audio‐only control treatments. Our open source RoboFinch setup thus provides an unprecedented tool for systematic study of the functionality and integration of audio‐visual cues associated with song behaviour. Realistic head and beak movements aligned to specific song elements may allow future studies to assess the importance of multisensory cues during song development, sexual signalling and social behaviour. All software and assembly instructions are open source, and the robot can be easily adapted to other species. Experimental manipulations of stimulus combinations and synchronisation can further elucidate how audio‐visual cues are integrated by receivers and how they may enhance signal detection, recognition, learning and memory.

WORKING MEMORY IN THE PROCESS OF TEACHING SONGS

The control processes and mnemonic strategies used in working memory are important both in the general learning process and in the music learning process. In the acquisition of music, the working memory determines the formation of auditory notions, which is an essential dimension in the development of musicality. Its qualitative indicators are (1) accuracy - accurate perception and reproduction of memorized music material; (2) persistence - duration of remembrance. Therefore, it is pedagogically important to improve it at the primary school age, because working memory forms the basis for creating more complex conceptual content constructions both in music and in other fields. The aim of the research is to promote the development of working memory in the process of teaching songs. In order to achieve the goal of the research, a song teaching strategy for the development of working memory has been developed, a pedagogical observation of the music learning process for a duration of three years at the primary school level has been performed, and the obtained data have been analysed using descriptive statistics. The sample of the study consists of 200 primary school students. The data obtained in the article allow us to conclude that the purposefulness and regularity with which the chosen exercises are used, the quality of music perception and attention, and musical thinking all contribute to the development of musical memory in primary school music education. The relationship between song acquisition and working memory described in this publication expands the understanding of music educators and helps them improve their professional skills.

Song Preference in Female and Juvenile Songbirds: Proximate and Ultimate Questions.

Birdsong has long been a subject of extensive research in the fields of ethology as well as neuroscience. Neural and behavioral mechanisms underlying song acquisition and production in male songbirds are particularly well studied, mainly because birdsong shares some important features with human speech such as critical dependence on vocal learning. However, birdsong, like human speech, primarily functions as communication signals. The mechanisms of song perception and recognition should also be investigated to attain a deeper understanding of the nature of complex vocal signals. Although relatively less attention has been paid to song receivers compared to signalers, recent studies on female songbirds have begun to reveal the neural basis of song preference. Moreover, there are other studies of song preference in juvenile birds which suggest possible functions of preference in social context including the sensory phase of song learning. Understanding the behavioral and neural mechanisms underlying the formation, maintenance, expression, and alteration of such song preference in birds will potentially give insight into the mechanisms of speech communication in humans. To pursue this line of research, however, it is necessary to understand current methodological challenges in defining and measuring song preference. In addition, consideration of ultimate questions can also be important for laboratory researchers in designing experiments and interpreting results. Here we summarize the current understanding of song preference in female and juvenile songbirds in the context of Tinbergen’s four questions, incorporating results ranging from ethological field research to the latest neuroscience findings. We also discuss problems and remaining questions in this field and suggest some possible solutions and future directions.

Seasonal regulation of singing-driven gene expression associated with song plasticity in the canary, an open-ended vocal learner

Songbirds are one of the few animal taxa that possess vocal learning abilities. Different species of songbirds exhibit species-specific learning programs during song acquisition. Songbirds with open-ended vocal learning capacity, such as the canary, modify their songs during adulthood. Nevertheless, the neural molecular mechanisms underlying open-ended vocal learning are not fully understood. We investigated the singing-driven expression of neural activity-dependent genes (Arc, Egr1, c-fos, Nr4a1, Sik1, Dusp6, and Gadd45β) in the canary to examine a potential relationship between the gene expression level and the degree of seasonal vocal plasticity at different ages. The expression of these genes was differently regulated throughout the critical period of vocal learning in the zebra finch, a closed-ended song learner. In the canary, the neural activity-dependent genes were induced by singing in the song nuclei throughout the year. However, in the vocal motor nucleus, the robust nucleus of the arcopallium (RA), all genes were regulated with a higher induction rate by singing in the fall than in the spring. The singing-driven expression of these genes showed a similar induction rate in the fall between the first year juvenile and the second year adult canaries, suggesting a seasonal, not age-dependent, regulation of the neural activity-dependent genes. By measuring seasonal vocal plasticity and singing-driven gene expression, we found that in RA, the induction intensity of the neural activity-dependent genes was correlated with the state of vocal plasticity. These results demonstrate a correlation between vocal plasticity and the singing-driven expression of neural activity-dependent genes in RA through song development, regardless of whether a songbird species possesses an open- or closed-ended vocal learning capacity.

Differential development of myelin in zebra finch song nuclei.

Songbirds learn vocalizations by hearing and practicing songs. As song develops, the tempo becomes faster and more precise. In the songbird brain, discrete nuclei form interconnected myelinated circuits that control song acquisition and production. The myelin sheath increases the speed of action potential propagation by insulating the axons of neurons and by reducing membrane capacitance. As the brain develops, myelin increases in density, but the time course of myelin development across discrete song nuclei has not been systematically studied in a quantitative fashion. We tested the hypothesis that myelination develops differentially across time and song nuclei. We examined myelin development in the brains of the zebra finch (Taeniopygia guttata) from chick at posthatch day (d) 8 to adult (up to 147 d) in five major song nuclei: HVC (proper name), robust nucleus of the arcopallium (RA), Area X, lateral magnocellular nucleus of the anterior nidopallium, and medial portion of the dorsolateral thalamic nucleus (DLM). All of these nuclei showed an increase in the density of myelination during development but at different rates and to different final degrees. Exponential curve fits revealed that DLM showed earlier myelination than other nuclei, and HVC showed the slowest myelination of song nuclei. Together, these data show differential maturation of myelination in different portions of the song system. Such differential maturation would be well placed to play a role in regulating the development of learned song.

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.

Extraordinary variation in a simple song: No geographical patterns in initial phrase variation of the Yellowhammer, a passerine with pronounced dialects

AbstractGeographical variation of birdsong is used to study various topics from cultural evolution to mechanisms responsible for reproductive barriers or song acquisition. In species with pronounced dialects, however, patterns of variation in non-dialect parts of the song are usually overlooked. We focused on the individually variable initial phrase of the song of the Yellowhammer (Emberiza citrinella), a common Palearctic passerine which became a model species for dialect research. We used a quantitative method to compare the similarity of initial phrases from the repertoires of 237 males recorded at different spatial scales in a central European country covering all main dialect types. We hypothesized that patterns of initial phrase sharing and/or phrase similarity are affected by dialect boundaries and geographical proximity (i.e. that birds from the same dialect regions use more similar phrases or share them more often). Contrary to our expectations, initial phrase variation seems unrelated to dialects, as we did not find higher similarity either among recordings from the same dialect areas or among those from the same locality. Interestingly, despite the immense variability of phrase types detected (only 16% of 368 detected initial phrase types were shared between at least 2 males), a relatively high proportion of males (45%) was involved in sharing, and males using the same initial phrase were located anywhere from tens of meters to hundreds of kilometers apart. The patterns of variation suggest that precise copying during song learning as well as improvisation play important roles in forming individual repertoires in the Yellowhammer. Our data also confirm previous indications that the repertoires of Yellowhammer males (i.e. the composition of initial phrases) are individually unique and temporally stable. This makes the species a good candidate for individual acoustic monitoring, useful for detailed population or behavioral studies without the need for physical capture and marking of males.

Sexual dimorphism of inhibitory synaptic transmission in RA projection neurons of songbirds

The song control system in the brain of songbirds is important for the production and acquisition of song and exhibits some of the largest neural sex differences observed in vertebrates. The robust nucleus of the arcopallium (RA) is a premotor nucleus, playing a key role in controlling singing. RA projection neurons (PNs) receives denser synapse inputs including excitatory in males than in females. However, the inhibitory synaptic transmission in the RA has not been reported. In the present study, using whole-cell voltage-clamp recording, spontaneous inhibitory postsynaptic currents (sIPSCs) and miniature inhibitory postsynaptic currents (mIPSCs) of the males and females were recorded. The average frequency and amplitude of sIPSCs/mIPSCs in males were higher than females. These results demonstrate the sexually dimorphic of the inhibitory synaptic transmission in the RA PNs and the RA PNs in males receive more inhibitory synaptic transmission. These findings contribute to further illuminate the neural mechanisms under the sexually dimorphism song production of adult zebra finches.

Interpersonal synchronization of inferior frontal cortices tracks social interactive learning of a song

Much of human learning emerges as a result of interaction with others. Yet, this interpersonal process has been poorly characterized from a neurophysiological perspective. This study investigated (i) whether Interpersonal Brain Synchronization (IBS) can reliably mark social interactive learning, and specifically (ii) during what kind of interactive behavior. We recorded brain activity from learner-instructor dyads using functional Near-Infrared Spectroscopy (fNIRS) during the acquisition of a music song. We made four fundamental observations. First, during the interactive learning task, brain activity recorded from the bilateral Inferior Frontal Cortex (IFC) synchronized across the learner and the instructor. Second, such IBS was observed in particular when the learner was observing the instructor's vocal behavior and when the learning experience entailed a turn-taking and more active mode of interaction. Third, this specific enhancement of IBS predicted learner's behavioral performance. Fourth, Granger causality analyses further disclosed that the signal recorded from the instructor's brain better predicted that recorded from the learner's brain than vice versa. Together, these results indicate that social interactive learning can be neurophysiologically characterized in terms of IBS. Furthermore, they suggest that the learner's involvement in the learning experience, alongside the instructor's modeling, are key factors driving the alignment of neural processes across learner and instructor. Such alignment impacts upon the real-time acquisition of new information and eventually upon the learning (behavioral) performance. Hence, besides providing a biological characterization of social interactive learning, our results hold relevance for clinical and pedagogical practices.

A neuronal signature of accurate imitative learning in wild-caught songbirds (swamp sparrows, Melospiza georgiana)

In humans and other animals, behavioural variation in learning has been associated with variation in neural features like morphology and myelination. By contrast, it is essentially unknown whether cognitive performance scales with electrophysiological properties of individual neurons. Birdsong learning offers a rich system to investigate this topic as song acquisition is similar to human language learning. Here, we address the interface between behavioural learning and neurophysiology in a cohort of wild-caught, hand-reared songbirds (swamp sparrows, Melospiza georgiana). We report the discovery in the forebrain HVC of sensorimotor ‘bridge’ neurons that simultaneously and selectively represent two critical learning-related schemas: the bird’s own song, and the specific tutor model from which that song was copied. Furthermore, the prevalence and response properties of bridge neurons correlate with learning ability – males that copied tutor songs more accurately had more bridge neurons. Our results are consistent with the hypothesis that accurate imitative learning depends on a successful bridge, within single cortical neurons, between the representation of learning models and their sensorimotor copies. Whether such bridge neurons are a necessary mechanism for accurate learning or an outcome of learning accuracy is unknown at this stage, but can now be addressed in future developmental studies.

Effect of no-night light environment on behaviour, learning performance and personality in zebra finches

A periodic day–night environment is critical for daily behavioural patterns and advanced brain functions such as learning and cognition in animals. We investigated whether a no-night light environment would impair these functions in parent and F1 and F2 zebra finches, Taeniopygia guttata . Particularly, we examined song acquisition as a measure of learning, tested cognitive performance with reference to spatial and colour association tasks, and assessed personality with respect to an exploratory trait, first in the parent (P) and subsequently in F1 and F2 birds born and raised under 12:12 h light:dark or constant light (hence no-night, LL) environments. Daily patterns in activity and singing were monitored as circadian response indicators. After initial decay, the rhythmic patterns in daily activity and singing were restored after several weeks in the majority of P and F1 birds under LL; F2 birds displayed robust circadian rhythms in both behavioural patterns under LL. Further, LL decreased participation and performance in cognitive tests and reduced exploratory behaviour in birds from all generations. Overall, we found negative effects of the LL environment on daily behavioural patterns, advanced brain functions (i.e. learning and cognition) and personality in zebra finches when adult and in subsequent generations. These results give insights into the possible impact on animals of night-time illumination such as in an overly lit urban habitat.

Geographic patterns of song variation reveal timing of song acquisition in a wild avian population

Geographic patterns of song variation are common in passerines and can develop as a consequence of the mechanisms of song acquisition and dispersal. In particular, the timing of dispersal relative to the sensory learning phase and the time of song crystallization is important. For example, when the sensory phase continues after dispersal or when males learn new songs every breeding season, i.e. open-ended learner, neighborhoods can develop where males share their songs. In this study, we utilize a unique, comprehensive dispersal and song recording dataset to investigate the existence and development of micro-geographic song variation in a wild passerine population. Machine learning song analysis methods allow us to overcome perceptual bias in the classification of the songs of New Zealand hihi (Notiomystis cincta). We show that males share more song elements of their repertoire with their neighbors than with more distant males or with males from the same natal area, implying that repertoire is acquired post-dispersal. Finally, we suggest that high levels of male competition have driven the development of post-dispersal vocal learning behavior in this species.

Overproduction and attrition: the fates of songs memorized during song learning in songbirds

Most songbirds learn their songs through imitation. However, what a male sings as an adult is not necessarily a complete inventory of what he memorized at some earlier point in time: songbirds commonly memorize more material than they eventually sing as adults. Work with swamp sparrows, Melospiza georgiana, first confirmed that males rehearse many of the song models to which they are exposed during the sensory phase of song acquisition but subsequently include only a subset of those rehearsed songs in their adult repertoire. This process of overproduction and selective attrition has since been demonstrated in other species as well. More recently, the persistent memory of tutor songs rehearsed but not included in the adult repertoire has been demonstrated at the neural level. Furthermore, memories of song models heard during the sensory phase of acquisition but never detected during rehearsal in the sensorimotor phase also may persist into adulthood. Here we review behavioural and neural studies of overproduction and attrition in song learning. We discuss factors that may trigger the persistence of some models and the rejection of others in an individual's repertoire and possible functional consequences of this phenomenon. Data from human speech research indicates that humans also may unconsciously retain memories of features of languages heard early in life but never spoken.

Sex and seasonal differences in neurogenesis and volume of the song-control system are associated with song in brood-parasitic and non-brood-parasitic icterid songbirds.

The song-control system in the brain of songbirds is important for the production and acquisition of song and exhibits both remarkable seasonal plasticity and some of the largest neural sex differences observed in vertebrates. We measured sex and seasonal differences in two nuclei of the song-control system of brood-parasitic brown-headed cowbirds (Molothrus ater) and closely-related non-parasitic red-winged blackbirds (Agelaius phoeniceus). These species differ in both the development and function of song. Brown-headed cowbirds have a larger sex difference in song than red-winged blackbirds. Female cowbirds never sing, whereas female blackbirds do though much less than males. In cowbirds, song primarily functions in mate choice and males modify their song as they approach sexual maturity and interact with females. In red-winged blackbirds, song is used primarily in territorial defence and is crystalized earlier in life. We found that the HVC was more likely to be discernable in breeding female blackbirds than in breeding female cowbirds. Compared to males, females had a smaller HVC and a smaller robust nucleus of the arcopallium (RA). However, females had higher doublecortin immunoreactivity (DCX+) in HVC, a measure of neurogenesis. Consistent with sex differences in song, the sex difference in RA volume was greater in cowbirds than in blackbirds. Males of both species had a smaller HVC with higher DCX+ in post-breeding condition than in breeding condition when song is more plastic. Sex and seasonal differences in the song-control system were closely related to variation in song in these two icterid songbirds. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 76: 1226-1240, 2016.