Learning to pause: Fidelity of and biases in the developmental acquisition of gaps in the communicative signals of a songbird.

The temporal organization of sounds used in social contexts can provide information about signal function and evoke varying responses in listeners (receivers). For example, music is a universal and learned human behavior that is characterized by different rhythms and tempos that can evoke disparate responses in listeners. Similarly, birdsong is a social behavior in songbirds that is learned during critical periods in development and used to evoke physiological and behavioral responses in receivers. Recent investigations have begun to reveal the breadth of universal patterns in birdsong and their similarities to common patterns in speech and music, but relatively little is known about the degree to which biological predispositions and developmental experiences interact to shape the temporal patterning of birdsong. Here, we investigated how biological predispositions modulate the acquisition and production of an important temporal feature of birdsong, namely the duration of silent pauses ("gaps") between vocal elements ("syllables"). Through analyses of semi-naturally raised and experimentally tutored zebra finches, we observed that juvenile zebra finches imitate the durations of the silent gaps in their tutor's song. Further, when juveniles were experimentally tutored with stimuli containing a wide range of gap durations, we observed biases in the prevalence and stereotypy of gap durations. Together, these studies demonstrate how biological predispositions and developmental experiences differently affect distinct temporal features of birdsong and highlight similarities in developmental plasticity across birdsong, speech, and music. RESEARCH HIGHLIGHTS: The temporal organization of learned acoustic patterns can be similar across human cultures and across species, suggesting biological predispositions in acquisition. We studied how biological predispositions and developmental experiences affect an important temporal feature of birdsong, namely the duration of silent intervals between vocal elements ("gaps"). Semi-naturally and experimentally tutored zebra finches imitated the durations of gaps in their tutor's song and displayed some biases in the learning and production of gap durations and in gap variability. These findings in the zebra finch provide parallels with the acquisition of temporal features of speech and music in humans.

Cross-modal facilitation of auditory discrimination in a frog.

Stimulation in one sensory modality can affect perception in a separate modality, resulting in diverse effects including illusions in humans. This can also result in cross-modal facilitation, a process where sensory performance in one modality is improved by stimulation in another modality. For instance, a simple sound can improve performance in a visual task in both humans and cats. However, the range of contexts and underlying mechanisms that evoke such facilitation effects remain poorly understood. Here, we demonstrated cross-modal stimulation in wild-caught túngara frogs, a species with well-studied acoustic preferences in females. We first identified that a combined visual and seismic cue (vocal sac movement and water ripple) was behaviourally relevant for females choosing between two courtship calls in a phonotaxis assay. We then found that this combined cross-modal stimulus rescued a species-typical acoustic preference in the presence of background noise that otherwise abolished the preference. These results highlight how cross-modal stimulation can prime attention in receivers to improve performance during decision-making. With this, we provide the foundation for future work uncovering the processes and conditions that promote cross-modal facilitation effects.

Evolutionary and Allometric Insights into Anuran Auditory Sensitivity and Morphology.

As species change through evolutionary time, the neurological and morphological structures that underlie behavioral systems typically remain coordinated. This is especially important for communication systems, in which these structures must remain coordinated both within and between senders and receivers for successful information transfer. The acoustic communication of anurans ("frogs") offers an excellent system to ask when and how such coordination is maintained, and to allow researchers to dissociate allometric effects from independent correlated evolution. Anurans constitute one of the most speciose groups of vocalizing vertebrates, and females typically rely on vocalizations to localize males for reproduction. Here, we compile and compare data on various aspects of auditory morphology, hearing sensitivity, and call-dominant frequency across 81 species of anurans. We find robust, phylogenetically independent scaling effects of body size for all features measured. Furthermore, after accounting for body size, we find preliminary evidence that morphological evolution beyond allometry can correlate with hearing sensitivity and dominant frequency. These data provide foundational results regarding constraints imposed by body size on communication systems and motivate further data collection and analysis using comparative approaches across the numerous anuran species.

Covariation among multimodal components in the courtship display of the túngara frog.

Communication systems often include a variety of components, including those that span modalities, which may facilitate detection and decision-making. For example, female túngara frogs and fringe-lipped bats generally rely on acoustic mating signals to find male túngara frogs in a mating or foraging context, respectively. However, two additional cues (vocal sac inflation and water ripples) can enhance detection and choice behavior. To date, we do not know the natural variation and covariation of these three components. To address this, we made detailed recordings of calling males, including call amplitude, vocal sac volume and water ripple height, in 54 frogs (2430 calls). We found that all three measures correlated, with the strongest association between the vocal sac volume and call amplitude. We also found that multimodal models predicted the mass of calling males better than unimodal models. These results demonstrate how multimodal components of a communication system relate to each other and provide an important foundation for future studies on how receivers integrate and compare complex displays.

Phylogeny and mechanisms of shared hierarchical patterns in birdsong.

Organizational patterns can be shared across biological systems, and revealing the factors shaping common patterns can provide insight into fundamental biological mechanisms. The behavioral pattern that elements with more constituents tend to consist of shorter constituents (Menzerath's law [ML]) was described first in speech and language (e.g., words with more syllables consist of shorter syllables) and subsequently in music and animal communication. Menzerath's law is hypothesized to reflect efficiency in information transfer, but biases and constraints in motor production can also lead to this pattern. We investigated the evolutionary breadth of ML and the contribution of production mechanisms to ML in the songs of 15 songbird species. Negative relationships between the number and duration of constituents (e.g., syllables in phrases) were observed in all 15 species. However, negative relationships were also observed in null models in which constituents were randomly allocated into observed element durations, and the observed negative relationship for numerous species did not differ from the null model; consequently, ML in these species could simply reflect production constraints and not communicative efficiency. By contrast, ML was significantly different from the null model for more than half the cases, suggesting additional organizational rules are imposed onto birdsongs. Production mechanisms are also underscored by the finding that canaries and zebra finches reared without auditory experiences that guide vocal development produced songs with nearly identical ML patterning as typically reared birds. These analyses highlight the breadth with which production mechanisms contribute to this prevalent organizational pattern in behavior.

Introductory gestures before songbird vocal displays are shaped by learning and biological predispositions.

Numerous animal displays begin with introductory gestures. For example, lizards start their head-bobbing displays with introductory push-ups, and many songbirds begin their vocal displays by repeating introductory notes (INs) before producing their learned song. Among songbirds, the acoustic structure and the number of INs produced before song vary considerably between individuals in a species. While similar variation in songs between individuals is a result of learning, whether variations in INs are also due to learning remains poorly understood. Here, using natural and experimental tutoring with male zebra finches, we show that mean IN number and IN acoustic structure are learned from a tutor. Interestingly, IN properties and how well INs were learned, were not correlated with the accuracy of song imitation and only weakly correlated with some features of songs that followed. Finally, birds artificially tutored with songs lacking INs still repeated vocalizations that resembled INs, before their songs, suggesting biological predispositions in IN production. These results demonstrate that INs, just like song elements, are shaped both by learning and biological predispositions. More generally, our results suggest mechanisms for generating variation in introductory gestures between individuals while still maintaining the species-specific structure of complex displays like birdsong.

Manipulations of sensory experiences during development reveal mechanisms underlying vocal learning biases in zebra finches.

Biological predispositions in learning can bias and constrain the cultural evolution of social and communicative behaviors (e.g., speech and birdsong), and lead to the emergence of behavioral and cultural "universals." For example, surveys of laboratory and wild populations of zebra finches (Taeniopygia guttata) document consistent patterning of vocal elements ("syllables") with respect to their acoustic properties (e.g., duration, mean frequency). Furthermore, such universal patterns are also produced by birds that are experimentally tutored with songs containing randomly sequenced syllables ("tutored birds"). Despite extensive demonstrations of learning biases, much remains to be uncovered about the nature of biological predispositions that bias song learning and production in songbirds. Here, we examined the degree to which "innate" auditory templates and/or biases in vocal motor production contribute to vocal learning biases and production in zebra finches. Such contributions can be revealed by examining acoustic patterns in the songs of birds raised without sensory exposure to song ("untutored birds") or of birds that are unable to hear from early in development ("early-deafened birds"). We observed that untutored zebra finches and early-deafened zebra finches produce songs with positional variation in some acoustic features (e.g., mean frequency) that resemble universal patterns observed in tutored birds. Similar to tutored birds, early-deafened birds also produced song motifs with alternation in acoustic features across adjacent syllables. That universal acoustic patterns are observed in the songs of both untutored and early-deafened birds highlights the contribution motor production biases to the emergence of universals in culturally transmitted behaviors.

Statistical learning for vocal sequence acquisition in a songbird.

Birdsong is a learned communicative behavior that consists of discrete acoustic elements ("syllables") that are sequenced in a controlled manner. While the learning of the acoustic structure of syllables has been extensively studied, relatively little is known about sequence learning in songbirds. Statistical learning could contribute to the acquisition of vocal sequences, and we investigated the nature and extent of sequence learning at various levels of song organization in the Bengalese finch, Lonchura striata var. domestica. We found that, under semi-natural conditions, pupils (sons) significantly reproduced the sequence statistics of their tutor's (father's) songs at multiple levels of organization (e.g., syllable repertoire, prevalence, and transitions). For example, the probability of syllable transitions at "branch points" (relatively complex sequences that are followed by multiple types of transitions) were significantly correlated between the songs of tutors and pupils. We confirmed the contribution of learning to sequence similarities between fathers and sons by experimentally tutoring juvenile Bengalese finches with the songs of unrelated tutors. We also discovered that the extent and fidelity of sequence similarities between tutors and pupils were significantly predicted by the prevalence of sequences in the tutor's song and that distinct types of sequence modifications (e.g., syllable additions or deletions) followed distinct patterns. Taken together, these data provide compelling support for the role of statistical learning in vocal production learning and identify factors that could modulate the extent of vocal sequence learning.

Behavioural responses to video and live presentations of females reveal a dissociation between performance and motivational aspects of birdsong.

Understanding the regulation of social behavioural expression requires insight into motivational and performance aspects. While a number of studies have independently assessed these aspects of social behaviours, few have examined how they relate to each other. By comparing behavioural variation in response to live or video presentations of conspecific females, we analysed how variation in the motivation to produce courtship song covaries with variation in performance aspects of courtship song in male zebra finches (Taeniopygia guttata). In agreement with previous reports, we observed that male zebra finches were less motivated to produce courtship songs to videos of females than to live presentations of females. However, we found that acoustic features that reflect song performance were not significantly different between songs produced in response to videos of females, and those produced in response to live females. For example, songs directed at video presentations of females were just as fast and stereotyped as songs directed at live females. These experimental manipulations and correlational analyses reveal a dissociation between motivational and performance aspects of birdsong and suggest a refinement of neural models of song production and control. In addition, they support the efficacy of videos to study both motivational and performance aspects of social behaviours.

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.

Complexity is complicated and so too is comparing complexity metrics-A response to Mikula et al. (2018).

In a recent publication (Pearse et al. 2018b), we explored the macroevolution and macroecology of passerine song using a large citizen science database of bird songs and powerful machine learning tools. Mikula et al. (2018) examine a small subset (<8%) of the data we used, and suggest that our metric of song complexity, the SD of frequency (SDF), does not correlate to other metrics of birdsong complexity, specifically syllable repertoire size and syllable diversity. We comment on the diversity of complexity metrics that exist in the field at present, and, while acknowledging that metrics may differ, outline how this variety allows us to ask more biologically nuanced questions. We see no reason or need for all complexity metrics to be correlated. Since different complexity metrics have been, and will continue to be, used, we outline how metrics could be fairly compared in the future.

Ability to modulate birdsong across social contexts develops without imitative social learning.

Many important behaviours are socially learned. For example, the acoustic structure of courtship songs in songbirds is learned by listening to and interacting with conspecifics during a sensitive period in development. Signallers modify the spectral and temporal structures of their vocalizations depending on the social context, but the degree to which this modulation requires imitative social learning remains unknown. We found that male zebra finches (Taeniopygia guttata) that were not exposed to context-dependent song modulations throughout development significantly modulated their song in ways that were typical of socially reared birds. Furthermore, the extent of these modulations was not significantly different between finches that could or could not observe these modulations during tutoring. These data suggest that this form of vocal flexibility develops without imitative social learning in male zebra finches.

Global macroevolution and macroecology of passerine song.

Studying the macroevolution of the songs of Passeriformes (perching birds) has proved challenging. The complexity of the task stems not just from the macroevolutionary and macroecological challenge of modeling so many species, but also from the difficulty in collecting and quantifying birdsong itself. Using machine learning techniques, we extracted songs from a large citizen science dataset, and then analyzed the evolution, and biotic and abiotic predictors of variation in birdsong across 578 passerine species. Contrary to expectations, we found few links between life-history traits (monogamy and sexual dimorphism) and the evolution of song pitch (peak frequency) or song complexity (standard deviation of frequency). However, we found significant support for morphological constraints on birdsong, as reflected in a negative correlation between bird size and song pitch. We also found that broad-scale biogeographical and climate factors such as net primary productivity, temperature, and regional species richness were significantly associated with both the evolution and present-day distribution of bird song features. Our analysis integrates comparative and spatial modeling with newly developed data cleaning and curation tools, and suggests that evolutionary history, morphology, and present-day ecological processes shape the distribution of song diversity in these charismatic and important birds.

Learning Biases Underlie "Universals" in Avian Vocal Sequencing.

Biological predispositions in vocal learning have been proposed to underlie commonalities in vocal sequences, including for speech and birdsong, but cultural propagation could also account for such commonalities [1-4]. Songbirds such as the zebra finch learn the sequencing of their acoustic elements ("syllables") during development [5-8]. Zebra finches are not constrained to learn a specific sequence of syllables, but significant consistencies in the positioning and sequencing of syllables have been observed between individuals within populations and between populations [8-10]. To reveal biological predispositions in vocal sequence learning, we individually tutored juvenile zebra finches with randomized and unbiased sequences of syllables and analyzed the extent to which birds produced common sequences. In support of biological predispositions, birds tutored with randomized sequences produced songs with striking similarities. Birds preferentially started and ended their song sequence with particular syllables, consistently positioned shorter and higher frequency syllables in the middle of their song, and sequenced their syllables such that pitch alternated across adjacent syllables. These patterns are reminiscent of those observed in normally tutored birds, suggesting that birds "creolize" aberrant sequence inputs to produce normal sequence outputs. Similar patterns were also observed for syllables that were not used for tutoring (i.e., unlearned syllables), suggesting that motor biases could contribute to sequence learning biases. Furthermore, zebra finches spontaneously produced acoustic patterns that are commonly observed in speech and music, suggesting that sensorimotor processes that are shared across a wide range of vertebrates could underlie these patterns in humans.

Advantages of comparative studies in songbirds to understand the neural basis of sensorimotor integration.

Sensorimotor integration is the process through which the nervous system creates a link between motor commands and associated sensory feedback. This process allows for the acquisition and refinement of many behaviors, including learned communication behaviors such as speech and birdsong. Consequently, it is important to understand fundamental mechanisms of sensorimotor integration, and comparative analyses of this process can provide vital insight. Songbirds offer a powerful comparative model system to study how the nervous system links motor and sensory information for learning and control. This is because the acquisition, maintenance, and control of birdsong critically depend on sensory feedback. Furthermore, there is an incredible diversity of song organizations across songbird species, ranging from songs with simple, stereotyped sequences to songs with complex sequencing of vocal gestures, as well as a wide diversity of song repertoire sizes. Despite this diversity, the neural circuitry for song learning, control, and maintenance remains highly similar across species. Here, we highlight the utility of songbirds for the analysis of sensorimotor integration and the insights about mechanisms of sensorimotor integration gained by comparing different songbird species. Key conclusions from this comparative analysis are that variation in song sequence complexity seems to covary with the strength of feedback signals in sensorimotor circuits and that sensorimotor circuits contain distinct representations of elements in the vocal repertoire, possibly enabling evolutionary variation in repertoire sizes. We conclude our review by highlighting important areas of research that could benefit from increased comparative focus, with particular emphasis on the integration of new technologies.

Predicting plasticity: acute context-dependent changes to vocal performance predict long-term age-dependent changes.

Understanding the factors that predict and guide variation in behavioral change can lend insight into mechanisms of motor plasticity and individual differences in behavior. The performance of adult birdsong changes with age in a manner that is similar to rapid context-dependent changes to song. To reveal mechanisms of vocal plasticity, we analyzed the degree to which variation in the direction and magnitude of age-dependent changes to Bengalese finch song could be predicted by variation in context-dependent changes. Using a repeated-measures design, we found that variation in age-dependent changes to the timing, sequencing, and structure of vocal elements ("syllables") was significantly predicted by variation in context-dependent changes. In particular, the degree to which the duration of intersyllable gaps, syllable sequencing at branch points, and fundamental frequency of syllables within spontaneous [undirected (UD)] songs changed over time was correlated with the degree to which these features changed from UD song to female-directed (FD) song in young-adult finches (FDyoung). As such, the structure of some temporal features of UD songs converged over time onto the structure of FDyoung songs. This convergence suggested that the FDyoung song could serve as a stable target for vocal motor plasticity. Consequently, we analyzed the stability of FD song and found that the temporal structure of FD song changed significantly over time in a manner similar to UD song. Because FD song is considered a state of heightened performance, these data suggest that age-dependent changes could reflect practice-related improvements in vocal motor performance.

Vocal motor changes beyond the sensitive period for song plasticity.

Behavior is critically shaped during sensitive periods in development. Birdsong is a learned vocal behavior that undergoes dramatic plasticity during a sensitive period of sensorimotor learning. During this period, juvenile songbirds engage in vocal practice to shape their vocalizations into relatively stereotyped songs. By the time songbirds reach adulthood, their songs are relatively stable and thought to be "crystallized." Recent studies, however, highlight the potential for adult song plasticity and suggest that adult song could naturally change over time. As such, we investigated the degree to which temporal and spectral features of song changed over time in adult Bengalese finches. We observed that the sequencing and timing of song syllables became more stereotyped over time. Increases in the stereotypy of syllable sequencing were due to the pruning of infrequently produced transitions and, to a lesser extent, increases in the prevalence of frequently produced transitions. Changes in song tempo were driven by decreases in the duration and variability of intersyllable gaps. In contrast to significant changes to temporal song features, we found little evidence that the spectral structure of adult song syllables changed over time. These data highlight differences in the degree to which temporal and spectral features of adult song change over time and support evidence for distinct mechanisms underlying the control of syllable sequencing, timing, and structure. Furthermore, the observed changes to temporal song features are consistent with a Hebbian framework of behavioral plasticity and support the notion that adult song should be considered a form of vocal practice.