Maturation-dependent control of vocal temporal plasticity in a songbird.

Birdsong is a unique model to address learning mechanisms of the timing control of sequential behaviors, with characteristic temporal structures consisting of serial sequences of brief vocal elements (syllables) and silent intervals (gaps). Understanding the neural mechanisms for plasticity of such sequential behavior should be aided by characterization of its developmental changes. Here, we assessed the level of acute vocal plasticity between young and adult Bengalese finches, and also quantified developmental change in variability of temporal structure. Acute plasticity was tested by delivering aversive noise bursts contingent on duration of a target gap, such that birds could avoid the noise by modifying their song. We found that temporal variability of song features decreased with birds' maturation. Noise-avoidance experiments demonstrated that maximal changes of gap durations were larger in young that in adult birds. After these young birds matured, the maximal change decreased to a similar level as adults. The variability of these target gaps also decreased as the birds matured. Such parallel changes suggest that the level of acute temporal plasticity could be predicted from ongoing temporal variability. Further, we found that young birds gradually began to stop their song at the target gap and restart from the introductory part of song, whereas adults did not. According to a synaptic chain model for timing sequence generation in premotor nuclei, adult learning would be interpreted as adaptive changes in conduction delays between chain-to-chain connections, whereas the learning of young birds could mainly depend on changes of the connections. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 77: 995-1006, 2017.

A rhythm landscape approach to the developmental dynamics of birdsong.

Unlike simple biological rhythms, the rhythm of the oscine bird song is a learned time series of diverse sounds that change dynamically during vocal ontogeny. How to quantify rhythm development is one of the most important challenges in behavioural biology. Here, we propose a simple method, called 'rhythm landscape', to visualize and quantify how rhythm structure, which is measured as durational patterns of sounds and silences, emerges and changes over development. Applying this method to the development of Bengalese finch songs, we show that the rhythm structure begins with a broadband rhythm that develops into diverse rhythms largely through branching from precursors. Furthermore, an information-theoretic measure, the Jensen-Shannon divergence, was used to characterize the crystallization process of birdsong rhythm, which started with a high rate of rhythm change and progressed to a stage of slow refinement. This simple method provides a useful description of rhythm development, thereby helping to reveal key temporal constraints on complex biological rhythms.

Limitations of a habituation task to demonstrate discrimination of natural signals in songbirds.

The habituation-dishabituation (HDH) paradigm is a common method used to examine animal cognition. Recent studies reported that spontaneous vocalizations could be used as an index of song familiarity and novelty in songbirds. However, these studies assigned only a few stimulus sets for all subjects, which might cause pseudoreplication. Therefore, we examined universality and general applicability of this method in Bengalese finches using a variety of stimulus sets. Seven unfamiliar conspecific songs were collected as a stimulus pool and a habituation song was randomly chosen for each subject. The subject was exposed to the habituation song repeatedly over 2h. During the test phase, the habituation song and a novel song randomly chosen from the stimulus pool were presented. We compared the degree of increase in call production during playback of those two songs. Although the degree was greater for the novel song compared with the habituation song in some birds, the trend was not consistent across all stimulus sets tested in these birds. Our results show that the HDH paradigm is not suitable to test song discrimination in songbirds unless precautions are taken to increase external validity by utilizing a variety of stimulus sets for each subject.

Domestication changes innate constraints for birdsong learning.

Birdsongs are acquired by imitating the sounds produced by conspecifics. Within a species, songs diverge by cultural transmission, but the range of species-specific features is restricted by innate constraints. Bengalese finches (Lonchura striata var. domestica) are a domesticated strain of the wild White-rumped munia (Lonchura striata). The songs of the domesticated strain have more tonal sounds and more variable sequences than those of the wild strain. We compared the features of songs that were produced by normal birds, isolation-reared birds, and cross-fostered birds in both White-rumped munias and Bengalese finches to identify differences in the genetic and environmental factors of their songs. Factor analyses were conducted based on 17 song measurements. We found that isolated songs differed from normal and cross-fostered songs, especially in unstable prosodic features. In addition, there were significant differences in sound property of mean frequency between the two strains regardless of the rearing conditions. Thus, innate constraints that partially determine birdsong phenotypes may be altered through domestication.

Stepwise acquisition of vocal combinatorial capacity in songbirds and human infants.

Human language, as well as birdsong, relies on the ability to arrange vocal elements in new sequences. However, little is known about the ontogenetic origin of this capacity. Here we track the development of vocal combinatorial capacity in three species of vocal learners, combining an experimental approach in zebra finches (Taeniopygia guttata) with an analysis of natural development of vocal transitions in Bengalese finches (Lonchura striata domestica) and pre-lingual human infants. We find a common, stepwise pattern of acquiring vocal transitions across species. In our first study, juvenile zebra finches were trained to perform one song and then the training target was altered, prompting the birds to swap syllable order, or insert a new syllable into a string. All birds solved these permutation tasks in a series of steps, gradually approximating the target sequence by acquiring new pairwise syllable transitions, sometimes too slowly to accomplish the task fully. Similarly, in the more complex songs of Bengalese finches, branching points and bidirectional transitions in song syntax were acquired in a stepwise fashion, starting from a more restrictive set of vocal transitions. The babbling of pre-lingual human infants showed a similar pattern: instead of a single developmental shift from reduplicated to variegated babbling (that is, from repetitive to diverse sequences), we observed multiple shifts, where each new syllable type slowly acquired a diversity of pairwise transitions, asynchronously over development. Collectively, these results point to a common generative process that is conserved across species, suggesting that the long-noted gap between perceptual versus motor combinatorial capabilities in human infants may arise partly from the challenges in constructing new pairwise vocal transitions.

Differential androgen receptor expression and DNA methylation state in striatum song nucleus Area X between wild and domesticated songbird strains.

In songbirds, a specialized neural system, the song system, is responsible for acquisition and expression of species-specific vocal patterns. We report evidence for differential gene expression between wild and domesticated strains having different learned vocal phenotypes. A domesticated strain of the wild white-rumped munia, the Bengalese finch, has a distinct song pattern with a more complicated syntax than the wild strain. We identified differential androgen receptor (AR) expression in basal ganglia nucleus Area X GABAergic neurons between the two strains, and within different domesticated populations. Differences in AR expression were correlated with the mean coefficient of variation of the inter-syllable duration in the two strains. Differential AR expression in Area X was observed before the initiation of singing, suggesting that inherited and/or early developmental mechanisms may affect expression within and between strains. However, there were no distinct differences in regions upstream of the AR start codon among all the birds in the study. In contrast, an epigenetic modification, DNA methylation state in regions upstream of AR in Area X, was observed to differ between strains and within domesticated populations. These results provide insight into the molecular basis of behavioral evolution through the regulation of hormone-related genes and demonstrate the potential association between epigenetic modifications and behavioral phenotype regulation.

An invisible sign stimulus: completion of occluded visual images in the Bengalese finch in an ecological context.

An object that includes occluded parts is sometimes perceived as a complete image and this phenomenon is known as amodal or visual completion. A sign stimulus is a minimum set of information that elicits a behavior, but this notion raises questions about whether animals ever engage in the behavior when they cannot see the occluded sign stimulus, but they can visually complete it. Male Bengalese finches engage in courtship behavior toward video images of female finches. We conducted three experiments with Bengalese finches to show both sign stimuli and visual completion function in an ecological context. We used three types of visual images recorded from female finches as stimuli: the head, the body, and the whole. Results showed that male Bengalese finches showed courtship behavior toward the head-occluded stimuli whereas they did not toward the headless body image. The results imply that the males completed this occluded sign stimulus through the process of visual completion. Exposure to a sign stimulus combined with the process of visual completion may operate cooperatively to facilitate adaptive responses under conditions of limited information.

Developmental learning of complex syntactical song in the Bengalese finch: a neural network model.

We developed a neural network model for studying neural mechanisms underlying complex syntactical songs of the Bengalese finch, which result from interactions between sensori-motor nuclei, the nucleus HVC (HVC) and the nucleus interfacialis (NIf). Results of simulations are tested by comparison with the song development of real young birds learning the same songs from their fathers. The model shows that complex syntactical songs can be reproduced from the simple interaction between the deterministic dynamics of a recurrent neural network and random noise. Features of the learning process in the simulations show similar trends to those observed in empirical data on the song development of real birds. These observations suggest that the temporal note sequences of songs take the form of a dynamical process involving recurrent connections in the network of the HVC, as opposed to feedforward activities, the mechanism proposed in the previous model.

Song motor control organizes acoustic patterns on two levels in Bengalese finches (Lonchura striata var. domestica).

Based on statistical analyses of song sequences, Bengalese finch (Lonchura striata var. domestica) songs do not show unvarying motif repetition as has been found in zebra finches (Taeniopygia guttata). Instead, there are variations of partially stereotyped sequences of song syllables. Although these stereotyped sequences consist of multiple syllables, in most cases these syllables occur together. To examine whether such structures really exist as a vocal production unit, we subjected singing birds to a light flash and determined when the stimulus stopped the songs. When light interruptions were presented within the statistically stereotyped sequences, the subsequent syllables tended to be produced, whereas interruptions presented during the statistically variable sequences tended to cause instantaneous song termination. This suggests that the associations among the song syllables that compose the statistically stereotyped sequences are more order dependent than those for the statistically variable sequences, and the tolerances of syllable pairs to visual interruptions are consistent with the statistical song structures. Additionally, following interruptions, several types of song sequence variations were observed that had not been previously reported. These phenomena might be caused by various effects of the visual stimulus on the hierarchical motor control program.

Spatiotemporal properties of visual stimuli for song induction in Bengalese finches.

Male Bengalese finches sing directed songs in response to video images of females projected onto a thin-film transistor monitor. We used this experimental paradigm to elucidate which properties of visual stimuli are important for eliciting singing. When video recordings of female Bengalese or zebra finches were used as visual stimuli, only images of conspecific females elicited singing from male Bengalese finches. When images of female Bengalese finches were rotated by 0 degrees, 90 degrees, or 180 degrees, only the upright images elicited singing. Finally, temporally normal (forward playback) images were more effective than time-reversed images and still images for eliciting singing. These results suggest that both the spatial and temporal arrangements of visual stimuli affect the singing behavior of male finches.