Zebra Finch Song Research Articles

Balanced imitation sustains song culture in zebra finches

Songbirds acquire songs by imitation, as humans do speech. Although imitation should drive convergence within a group and divergence through drift between groups, zebra finch songs sustain high diversity within a colony, but mild variation across colonies. We investigated this phenomenon by analyzing vocal learning statistics in 160 tutor-pupil pairs from a large breeding colony. Song imitation is persistently accurate in some families, but poor in others. This is not attributed to genetic differences, as fostered pupils copied their tutors’ songs as accurately or poorly as biological pupils. Rather, pupils of tutors with low song diversity make more improvisations compared to pupils of tutors with high song diversity. We suggest that a frequency dependent balanced imitation prevents extinction of rare song elements and overabundance of common ones, promoting repertoire diversity within groups, while constraining drift across groups, which together prevents the collapse of vocal culture into either complete uniformity or chaos.

Behavioral discrimination and time-series phenotyping of birdsong performance.

Variation in the acoustic structure of vocal signals is important to communicate social information. However, relatively little is known about the features that receivers extract to decipher relevant social information. Here, we took an expansive, bottom-up approach to delineate the feature space that could be important for processing social information in zebra finch song. Using operant techniques, we discovered that female zebra finches can consistently discriminate brief song phrases (“motifs”) from different social contexts. We then applied machine learning algorithms to classify motifs based on thousands of time-series features and to uncover acoustic features for motif discrimination. In addition to highlighting classic acoustic features, the resulting algorithm revealed novel features for song discrimination, for example, measures of time irreversibility (i.e., the degree to which the statistical properties of the actual and time-reversed signal differ). Moreover, the algorithm accurately predicted female performance on individual motif exemplars. These data underscore and expand the promise of broad time-series phenotyping to acoustic analyses and social decision-making.

Songbirds are excellent auditory discriminators, irrespective of age and experience

Human infants but not adults possess the ability to perceive differences between non-native language phoneme categories. The predominant explanation for this age-related decline in discriminative ability is the effect of statistical learning driven by sensory exposure: phoneme categories of the native language take precedence, have a higher frequency of occurrence and may encompass category distinctions in non-native languages. Alternatively, one could explain the decline through a reduction in discriminative abilities attributable to ageing. Thus, to what extent is auditory perception influenced either by experience or by age-related processes? Here, we attempted to answer this question, which cannot easily be disentangled in humans, in songbirds, which share many properties with humans: both learn the statistical distribution of sounds in their environment, both possess neural circuits to process vocalizations of their own species and plasticity in these circuits is subject to critical periods. To study the effects of experience and ageing, we trained zebra finches, Taeniopygia guttata , to discriminate short from long versions of a single zebra finch song syllable type. Birds in four groups distinguished by their age (old versus young) and level of auditory experience (with song experience versus completely isolated from song) could learn to discriminate arbitrarily fine differences between song syllables, although we found a trend that upholds the statistical learning hypothesis: birds with song experience performed better than birds with no experience. Furthermore, birds in all groups were able to generalize their learning to new stimuli of the same type, and they were able to rapidly adapt their learned discrimination boundaries. Finally, we found that songbirds could accurately discriminate randomly selected renditions of a stereotyped adult song syllable, revealing a flexible ability to discriminate conspecific vocalizations. • Sensory experience matters more than age for auditory perception in songbirds. • Songbirds generalize learned categories to novel stimuli. • Learned categories are flexible and category boundaries can be relearned easily. • Songbirds can learn random categories accurately. • Their auditory systems represent species-specific sounds accurately and flexibly.

Humans Discriminate Individual Zebra Finches by their Song

Comparative experiments have greatly advanced the field of biolinguistics in the 21st century, but so far very little research has focused on human perception of non-human animal vocalizations. Studies with zebra finch (Taeniopygia guttata) songs found that humans cannot perceive the full range of acoustic cues that zebra finches hear in their songs, although it remained unclear how much individual information is lost. Individual heterospecific discrimination by humans has only been shown with rhesus monkey (Macaca mulatta) voices. The present study examined whether human adults could discriminate two individual zebra finches by their songs, using a forced- choice Same-Different Paradigm. Results showed that adults can discriminate two individual zebra finches with high accuracy and without prior training. Discrimination mostly relied on differences in pitch contour, but discrimination was still possible with lower accuracy when pitch contour was removed. Future studies should expand these findings with more diverse non-human animal vocalizations.

Birdsong fails to support object categorization in human infants.

Recent evidence reveals a precocious link between language and cognition in human infants: listening to their native language supports infants’ core cognitive processes, including object categorization, and does so in a way that other acoustic signals (e.g., time-reversed speech; sine-wave tone sequences) do not. Moreover, language is not the only signal that confers this cognitive advantage: listening to vocalizations of non-human primates also supports object categorization in 3- and 4-month-olds. Here, we move beyond primate vocalizations to clarify the breadth of acoustic signals that promote infant cognition. We ask whether listening to birdsong, another naturally produced animal vocalization, also supports object categorization in 3- and 4-month-old infants. We report that listening to zebra finch song failed to confer a cognitive advantage. This outcome brings us closer to identifying a boundary condition on the range of non-linguistic acoustic signals that initially support infant cognition.

Nonlinear effects of intrinsic dynamics on temporal encoding in a model of avian auditory cortex.

Neurons exhibit diverse intrinsic dynamics, which govern how they integrate synaptic inputs to produce spikes. Intrinsic dynamics are often plastic during development and learning, but the effects of these changes on stimulus encoding properties are not well known. To examine this relationship, we simulated auditory responses to zebra finch song using a linear-dynamical cascade model, which combines a linear spectrotemporal receptive field with a dynamical, conductance-based neuron model, then used generalized linear models to estimate encoding properties from the resulting spike trains. We focused on the effects of a low-threshold potassium current (KLT) that is present in a subset of cells in the zebra finch caudal mesopallium and is affected by early auditory experience. We found that KLT affects both spike adaptation and the temporal filtering properties of the receptive field. The direction of the effects depended on the temporal modulation tuning of the linear (input) stage of the cascade model, indicating a strongly nonlinear relationship. These results suggest that small changes in intrinsic dynamics in tandem with differences in synaptic connectivity can have dramatic effects on the tuning of auditory neurons.

Discrimination of natural acoustic variation in vocal signals

Studies of acoustic communication often focus on the categories and units of vocalizations, but subtle variation also occurs in how these signals are uttered. In human speech, it is not only phonemes and words that carry information but also the timbre, intonation, and stress of how speech sounds are delivered (often referred to as “paralinguistic content”). In non-human animals, variation across utterances of vocal signals also carries behaviorally relevant information across taxa. However, the discriminability of these cues has been rarely tested in a psychophysical paradigm. Here, we focus on acoustic communication in the zebra finch (Taeniopygia guttata), a songbird species in which the male produces a single stereotyped motif repeatedly in song bouts. These motif renditions, like the song repetitions of many birds, sound very similar to the casual human listener. In this study, we show that zebra finches can easily discriminate between the renditions, even at the level of single song syllables, much as humans can discriminate renditions of speech sounds. These results support the notion that sensitivity to fine acoustic details may be a primary channel of information in zebra finch song, as well as a shared, foundational property of vocal communication systems across species.

Statistical structure of the trial-to-trial timing variability in synfire chains.

Timing and its variability are crucial for behavior. Consequently, neural circuits that take part in the control of timing and in the measurement of temporal intervals have been the subject of much research. Here we provide an analytical and computational account of the temporal variability in what is perhaps the most basic model of a timing circuit-the synfire chain. First we study the statistical structure of trial-to-trial timing variability in a reduced but analytically tractable model: a chain of single integrate-and-fire neurons. We show that this circuit's variability is well described by a generative model consisting of local, global, and jitter components. We relate each of these components to distinct neural mechanisms in the model. Next we establish in simulations that these results carry over to a noisy homogeneous synfire chain. Finally, motivated by the fact that a synfire chain is thought to underlie the circuit that takes part in the control and timing of the zebra finch song, we present simulations of a biologically realistic synfire chain model of the zebra finch timekeeping circuit. We find the structure of trial-to-trial timing variability to be consistent with our previous findings and to agree with experimental observations of the song's temporal variability. Our study therefore provides a possible neuronal account of behavioral variability in zebra finches.

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.

Neural mechanisms for developing species-universal and individually unique song of zebra finch.

Neural mechanisms for developing species-universal and individually unique song of zebra finch.

Auditory processing in the zebra finch midbrain: single unit responses and effect of rearing experience.

In birds the auditory system plays a key role in providing the sensory input used to discriminate between conspecific and heterospecific vocal signals. In those species that are known to learn their vocalizations, for example, songbirds, it is generally considered that this ability arises and is manifest in the forebrain, although there is no a priori reason why brainstem components of the auditory system could not also play an important part. To test this assumption, we used groups of normal reared and cross-fostered zebra finches that had previously been shown in behavioural experiments to reduce their preference for conspecific songs subsequent to cross fostering experience with Bengalese finches, a related species with a distinctly different song. The question we asked, therefore, is whether this experiential change also changes the bias in favour of conspecific song displayed by auditory midbrain units of normally raised zebra finches. By recording the responses of single units in MLd to a variety of zebra finch and Bengalese finch songs in both normally reared and cross-fostered zebra finches, we provide a positive answer to this question. That is, the difference in response to conspecific and heterospecific songs seen in normal reared zebra finches is reduced following cross-fostering. In birds the virtual absence of mammalian-like cortical projections upon auditory brainstem nuclei argues against the interpretation that MLd units change, as observed in the present experiments, as a result of top-down influences on sensory processing. Instead, it appears that MLd units can be influenced significantly by sensory inputs arising directly from a change in auditory experience during development.

Categorical Rhythms Are Shared between Songbirds and Humans

Rhythm is a prominent feature of music. Of the infinite possible ways of organizing events in time, musical rhythms are almost always distributed categorically. Such categories can facilitate the transmission of culture-a feature that songbirds and humans share. We compared rhythms of live performances of music to rhythms of wild thrush nightingale and domestic zebra finch songs. In nightingales, but not in zebra finches, we found universal rhythm categories, with patterns that were surprisingly similar to those of music. Isochronous 1:1 rhythms were similarly common. Interestingly, a bias toward small ratios (around 1:2 to 1:3), which is highly abundant in music, was observed also in thrush nightingale songs. Within that range, however, there was no statistically significant bias toward exact integer ratios (1:2 or 1:3) in the birds. High-ratio rhythms were abundant in the nightingale song and are structurally similar to fusion rhythms (ornaments) in music. In both species, preferred rhythms remained invariant over extended ranges of tempos, indicating natural categories. The number of rhythm categories decreased at higher tempos, with a threshold above which rhythm became highly stereotyped. In thrush nightingales, this threshold occurred at a tempo twice faster than in humans, indicating weaker structural constraints and a remarkable motor proficiency. Together, the results suggest that categorical rhythms reflect similar constraints on learning motor skills across species. The saliency of categorical rhythms across humans and thrush nightingales suggests that they promote, or emerge from, the cultural transmission of learned vocalizations. VIDEO ABSTRACT.

Contingent parental responses are naturally associated with zebra finch song learning

Active guidance of vocal learning by conspecifics has recently been found in several species, including some cetaceans and primates. However, in the zebra finch, Taeniopygia guttata, a commonly studied songbird, vocal learning was traditionally considered the product of memorization and imitation of a song model. Only recently have specific social feedback cues been shown to enhance song learning. What mechanisms drive the superior learning associated with social interactions? We recently found that ‘fluff-ups’, a nonvocal female arousal cue, facilitated song learning when played over video contingently on juvenile song production throughout development. However, it is unknown whether adults naturally respond in a contingent fashion to immature song, and whether young finches incorporate naturally occurring feedback into song learning. To investigate whether social influences affect song learning, the present study addressed the nature and significance of maternal and paternal cues associated with song development. We recorded unmanipulated zebra finch families throughout juvenile development and analysed their social interactions. We found that behaviours of both parents were associated with offspring song outcomes. Juvenile song learning could be predicted by the amount of contingent ‘fluff-up’ behaviours they received from their mothers throughout development. Fathers often sang immediately after a juvenile had sung, and paternal singing after juvenile singing was positively correlated with more accurate song learning in their sons. Conversely, when fathers sang before the juvenile sang, juveniles learned song less accurately. Our data suggest that parental vocal and gestural feedback plays a reinforcing role for song learning in zebra finches. There are many nonavian species, including chiropterans, pachyderms and pinnipeds, that modify their vocalizations in different developmental or social contexts but whose mechanisms of vocal learning are not known. Our findings suggest that these species should be closely examined for adult sensitivity to immature vocalizations and developmental capacity to learn from social feedback.

Statistical learning of transition patterns in the songbird auditory forebrain

Statistical learning of transition patterns between sounds—a striking capability of the auditory system—plays an essential role in animals’ survival (e.g., detect deviant sounds that signal danger). However, the neural mechanisms underlying this capability are still not fully understood. We recorded extracellular multi-unit and single-unit activity in the auditory forebrain of awake male zebra finches while presenting rare repetitions of a single sound in a long sequence of sounds (canary and zebra finch song syllables) patterned in either an alternating or random order at different inter-stimulus intervals (ISI). When preceding stimuli were regularly alternating (alternating condition), a repeated stimulus violated the preceding transition pattern and was a deviant. When preceding stimuli were in random order (control condition), a repeated stimulus did not violate any regularities and was not a deviant. At all ISIs tested (1 s, 3 s, or jittered at 0.8–1.2 s), deviant repetition enhanced neural responses in the alternating condition in a secondary auditory area (caudomedial nidopallium, NCM) but not in the primary auditory area (Field L2); in contrast, repetition suppressed responses in the control condition in both Field L2 and NCM. When stimuli were presented in the classical oddball paradigm at jittered ISI (0.8–1.2 s), neural responses in both NCM and Field L2 were stronger when a stimulus occurred as deviant with low probability than when the same stimulus occurred as standard with high probability. Together, these results demonstrate: (1) classical oddball effect exists even when ISI is jittered and the onset of a stimulus is not fully predictable; (2) neurons in NCM can learn transition patterns between sounds at multiple ISIs and detect violation of these transition patterns; (3) sensitivity to deviant sounds increases from Field L2 to NCM in the songbird auditory forebrain. Further studies using the current paradigms may help us understand the neural substrate of statistical learning and even speech comprehension.

Intramuscular antagonism of the G-protein coupled estrogen receptor 1 partially affects dimorphic characteristics of the syrinx, but is ineffective within the neural song circuit of zebra finches

Within the zebra finch song system, robust sex differences exist that enable singing behavior in males, but not females. Estradiol is a potent contributor to this process, but how and through which receptor(s) it acts is not clear. Historically, pharmacological manipulations of nuclear estrogen receptors have yielded conflicting results possibly due to method of drug delivery. More recently, the membrane bound G-protein coupled estrogen receptor 1 (GPER1) has also been identified as a potential candidate, but its function has not been fully described. To further investigate the role of GPER1, and the importance of the route of drug administration, a specific antagonist (G-15) was intramuscularly administered to zebra finches for 25 days, starting on the day of hatching. G-15 significantly decreased muscle fiber sizes of ventralis and dorsalis in the syrinx of males only. Dimorphic characteristics of the neural song system were unaffected by this manipulation in either sex. These results contrast with a study in which G-15 was intracranially delivered. In males, select song nuclei were decreased in volume, and in females, syrinx muscle fiber size was increased. Together, these results support the hypothesis that estrogens acting through GPER1 influence dimorphic development of the song system, and that method of drug administration is important in this species.

Do songbirds hear songs syllable by syllable?

Songbirds as vocal learners have been one of the most popular model species to investigate the biological prerequisite to human language. Their songs consist of syllables, which appear as pulse trains in sound spectrograms. When describing the song sequence, researchers consider the syllable to be the unit of the song. Moreover, artificial grammar learning studies asking whether songbirds recognize structural regularities observed in human language often design stimuli using song syllables as components. However, whether syllables are perceptual units is yet to be determined. We found that Bengalese finches, a species of songbird, responded significantly less to one specific syllable when it was temporally placed close to the preceding syllable. The proximity, or silent interval was within the range of what is produced in the natural songs of both Bengalese and zebra finches, and what has been used in other artificial grammar learning studies using zebra finches. Our results suggest the need for a reinterpretation of the description of birdsong structure and of previous artificial grammar learning studies.

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.

Mechanisms of Convergent Egg Provisioning in Poison Frogs.

Parental provisioning of offspring with physiological products (nursing) occurs in many animals, yet little is known about the neuroendocrine basis of nursing in non-mammalian species. Within amphibians, maternal provisioning has evolved multiple times, with mothers of some species feeding unfertilized eggs to their developing offspring until tadpoles complete metamorphosis [1-3]. We conducted field studies in Ecuador and Madagascar to ask whether convergence at the behavioral level provides similar benefits to offspring and relies on shared neural mechanisms in dendrobatid and mantellid poison frogs. At an ecological level, we found that nursing allows poison frogs to provide chemical defenses to their tadpoles in both species. At the neural level, nursing was associated with increased activity in the lateral septum and preoptic area, demonstrating recruitment of shared brain regions in the convergent evolution of nursing within frogs and across vertebrates [4]. In contrast, only mantellids showed increased oxytocin neuron activity akin to that in nursing mammals [5], suggesting evolutionary versatility in molecular mechanisms. Our findings demonstrate that maternal provisioning provides similar potential benefits to offspring and relies on similar brain regions in poison frog species with convergently evolved toxicity and maternal care. VIDEO ABSTRACT.

Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds.

Learning of most motor skills is constrained in a species-specific manner. However, the proximate mechanisms underlying species-specific learned behaviors remain poorly understood. Songbirds acquire species-specific songs through learning, which is hypothesized to depend on species-specific patterns of gene expression in functionally specialized brain regions for vocal learning and production, called song nuclei. Here, we leveraged two closely related songbird species, zebra finch, owl finch, and their interspecific first-generation (F1) hybrids, to relate transcriptional regulatory divergence between species with the production of species-specific songs. We quantified genome-wide gene expression in both species and compared this with allele-specific expression in F1 hybrids to identify genes whose expression in song nuclei is regulated by species divergence in either cis- or trans-regulation. We found that divergence in transcriptional regulation altered the expression of approximately 10% of total transcribed genes and was linked to differential gene expression between the two species. Furthermore, trans-regulatory changes were more prevalent than cis-regulatory and were associated with synaptic formation and transmission in song nucleus RA, the avian analog of the mammalian laryngeal motor cortex. We identified brain-derived neurotrophic factor (BDNF) as an upstream mediator of trans-regulated genes in RA, with a significant correlation between individual variation in BDNF expression level and species-specific song phenotypes in F1 hybrids. This was supported by the fact that the pharmacological overactivation of BDNF receptors altered the expression of its trans-regulated genes in the RA, thus disrupting the learned song structures of adult zebra finch songs at the acoustic and sequence levels. These results demonstrate functional neurogenetic associations between divergence in region-specific transcriptional regulation and species-specific learned behaviors.

Developmental modulation and predictability of age-dependent vocal plasticity in adult zebra finches

Predicting the nature of behavioral plasticity can provide insight into mechanisms of behavioral expression and control. Songbirds like the zebra finch rely on vocal signals for communication, and the performance of these signals demonstrate considerable plasticity over development. Traditionally, these signals were thought to be fixed in adulthood, but recent studies have revealed significant age-dependent changes to spectral and temporal features of song in adult songbirds. A number of age-dependent changes to song resemble acute changes to adult song performance across social contexts (e.g., when an adult male sings to a female relative to when he sings in isolation). The ability of variation in social context-dependent changes to predict variation in age-dependent plasticity would suggest shared mechanisms, but little is known about this predictability. In addition, although developmental experiences can shape adult plasticity, little is known about the extent to which social interactions during development affect age-dependent change to adult song. To this end, we systematically analyzed age- and context-dependent changes to adult zebra finch song, and then examined the degree to which age-dependent changes varied across birds that were social or non-socially tutored birds and to which social context-dependent changes predicted age-dependent changes. Non-socially tutored birds showed more dramatic changes to the broad structure of their motif over time than socially tutored birds, but non-socially and socially tutored birds did not differ in the extent of changes to various spectral and temporal features of song. Overall, we found that adult zebra finches produced longer and more spectrally stereotyped songs when they were older than when they were younger. Moreover, regardless of developmental tutoring, individual variation in age-dependent changes to song bout duration and syllable repetition were predicted by variation in social context-dependent changes to these features. These data indicate that social experiences during development can shape some aspects of adult plasticity and that acute context-dependent and long-term age-dependent changes to some song features could be mediated by modifications within similar neural substrates.