Cross-species conservation in the regulation of parvalbumin by perineuronal nets.

Parvalbumin (PV) neurons play an integral role in regulating neural dynamics and plasticity. Therefore, understanding the factors that regulate PV expression is important for revealing modulators of brain function. While the contribution of PV neurons to neural processes has been studied in mammals, relatively little is known about PV function in non-mammalian species, and discerning similarities in the regulation of PV across species can provide insight into evolutionary conservation in the role of PV neurons. Here we investigated factors that affect the abundance of PV in PV neurons in sensory and motor circuits of songbirds and rodents. In particular, we examined the degree to which perineuronal nets (PNNs), extracellular matrices that preferentially surround PV neurons, modulate PV abundance as well as how the relationship between PV and PNN expression differs across brain areas and species and changes over development. We generally found that cortical PV neurons that are surrounded by PNNs (PV+PNN neurons) are more enriched with PV than PV neurons without PNNs (PV-PNN neurons) across both rodents and songbirds. Interestingly, the relationship between PV and PNN expression in the vocal portion of the basal ganglia of songbirds (Area X) differed from that in other areas, with PV+PNN neurons having lower PV expression compared to PV-PNN neurons. These relationships remained consistent across development in vocal motor circuits of the songbird brain. Finally, we discovered a causal contribution of PNNs to PV expression in songbirds because degradation of PNNs led to a diminution of PV expression in PV neurons. These findings in reveal a conserved relationship between PV and PNN expression in sensory and motor cortices and across songbirds and rodents and suggest that PV neurons could modulate plasticity and neural dynamics in similar ways across songbirds and rodents.

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-species conservation in the regulation of parvalbumin by perineuronal nets.

Parvalbumin (PV) neurons play an integral role in regulating neural dynamics and plasticity. Therefore, understanding the factors that regulate PV expression is important for revealing modulators of brain function. While the contribution of PV neurons to neural processes has been studied in mammals, relatively little is known about PV function in non-mammalian species, and discerning similarities in the regulation of PV across species can provide insight into evolutionary conservation in the role of PV neurons. Here we investigated factors that affect the abundance of PV in PV neurons in sensory and motor circuits of songbirds and rodents. In particular, we examined the degree to which perineuronal nets (PNNs), extracellular matrices that preferentially surround PV neurons, modulate PV abundance as well as how the relationship between PV and PNN expression differs across brain areas and species and changes over development. We generally found that cortical PV neurons that are surrounded by PNNs (PV+PNN neurons) are more enriched with PV than PV neurons without PNNs (PV-PNN neurons) across both rodents and songbirds. Interestingly, the relationship between PV and PNN expression in the vocal portion of the basal ganglia of songbirds (Area X) differed from that in other areas, with PV+PNN neurons having lower PV expression compared to PV-PNN neurons. These relationships remained consistent across development in vocal motor circuits of the songbird brain. Finally, we discovered a causal contribution of PNNs to PV expression in songbirds because degradation of PNNs led to a diminution of PV expression in PV neurons. These findings reveal a conserved relationship between PV and PNN expression in sensory and motor cortices and across songbirds and rodents and suggest that PV neurons could modulate plasticity and neural dynamics in similar ways across songbirds and rodents.

The role of parvalbumin neurons in the evolution of skilled behaviours.

Understanding how animals display diverse and complex behaviours remains a central question in biology. A new study in PLOS Biology suggests that the emergence of clusters of parvalbumin neurons in the forebrain could reflect a convergent mechanism underlying the evolution of skilled behaviours in birds.

Alarm cues and alarmed conspecifics: neural activity during social learning from different cues in Trinidadian guppies.

Learning to respond appropriately to novel dangers is often essential to survival and success, but carries risks. Learning about novel threats from others (social learning) can reduce these risks. Many species, including the Trinidadian guppy (Poecilia reticulata), respond defensively to both conspecific chemical alarm cues and conspecific anti-predator behaviours, and in other fish such social information can lead to a learned aversion to novel threats. However, relatively little is known about the neural substrates underlying social learning and the degree to which different forms of learning share similar neural mechanisms. Here, we explored the neural substrates mediating social learning of novel threats from two different conspecific cues (i.e. social cue-based threat learning). We first demonstrated that guppies rapidly learn about threats paired with either alarm cues or with conspecific threat responses (demonstration). Then, focusing on acquisition rather than recall, we discovered that phospho-S6 expression, a marker of neural activity, was elevated in guppies during learning from alarm cues in the putative homologue of the mammalian lateral septum and the preoptic area. Surprisingly, these changes in neural activity were not observed in fish learning from conspecific demonstration. Together, these results implicate forebrain areas in social learning about threat but raise the possibility that circuits contribute to such learning in a stimulus-specific manner.

Wearable Neck Surface Accelerometers for Occupational Vocal Health Monitoring: Instrument and Analysis Validation Study.

BACKGROUND: Neck surface accelerometer (NSA) wearable devices have been developed for voice and upper airway health monitoring. As opposed to acoustic sounds, NSA senses mechanical vibrations propagated from the vocal tract to neck skin, which are indicative of a person's voice and airway conditions. NSA signals do not carry identifiable speech information and a speaker's privacy is thus protected, which is important and necessary for continuous wearable monitoring. Our device was already tested for its durable endurance and signal processing algorithms in controlled laboratory conditions. OBJECTIVE: This study aims to further evaluate both instrument and analysis validity in a group of occupational vocal users, namely, voice actors, who use their voices extensively at work in an ecologically valid setting. METHODS: A total of 16 professional voice actors (age range 21-50 years; 11 females and 5 males) participated in this study. All participants were mounted with an NSA on their sternal notches during the voice acting and voice assessment sessions. The voice acting session was 4-hour long, directed by a voice director in a professional sound studio. Voice assessment sessions were conducted before, during, and 48 hours after the acting session. The assessment included phonation tasks of passage reading, sustained vowels, maximum vowel phonation, and pitch glides. Clinical acoustic metrics (eg, fundamental frequency, cepstral measures) and a vocal dose measure (ie, accumulated distance dose from acting) were computed from NSA signals. A commonly used online questionnaire (Self-Administered Voice Rating questionnaire) was also implemented to track participants' perception of vocal fatigue. RESULTS: The NSA wearables stayed in place for all participants despite active body movements during the acting. The ensued body noise did not interfere with the NSA signal quality. All planned acoustic metrics were successfully derived from NSA signals and their numerical values were comparable with literature data. For a 4-hour long voice acting, the averaged distance dose was about 8354 m with no gender differences. Participants perceived vocal fatigue as early as 2 hours after the start of voice acting, with recovery 24-48 hours after the acting session. Among all acoustic metrics across phonation tasks, cepstral peak prominence and spectral tilt from the passage reading most closely mirrored trends in perceived fatigue. CONCLUSIONS: The ecological validity of an in-house NSA wearable was vetted in a workplace setting. One key application of this wearable is to prompt occupational voice users when their vocal safety limits are reached for duly protection. Signal processing algorithms can thus be further developed for near real-time estimation of clinically relevant metrics, such as accumulated distance dose, cepstral peak prominence, and spectral tilt. This functionality will enable continuous self-awareness of vocal behavior and protection of vocal safety in occupational voice users.

Mechanisms, development, and comparative perspectives on experience-dependent plasticity in social behavior.

Revealing the mechanisms underlying experience-dependent plasticity is a hallmark of behavioral neuroscience. While the study of social behavior has focused primarily on the neuroendocrine and neural control of social behaviors, the plasticity of these innate behaviors has received relatively less attention. Here, we review studies on mating-dependent changes to social behavior and neural circuitry across mammals, birds, and reptiles. We provide an overview of species similarities and differences in the effects of mating experiences on motivational and performative aspects of sexual behaviors, on sensory processing and preferences, and on the experience-dependent consolidation of sexual behavior. We also discuss recent insights into the neural mechanisms of and developmental influences on mating-dependent changes and outline promising approaches to investigate evolutionary parallels and divergences in experience-dependent plasticity.

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.

Norepinephrine in the avian auditory cortex enhances developmental song learning.

Sensory learning during critical periods in development has lasting effects on behavior. Neuromodulators like dopamine and norepinephrine (NE) have been implicated in various forms of sensory learning, but little is known about their contribution to sensory learning during critical periods. Songbirds like the zebra finch communicate with each other using vocal signals (e.g., songs) that are learned during a critical period in development, and the first crucial step in song learning is memorizing the sound of an adult conspecific's (tutor's) song. Here, we analyzed the extent to which NE modulates the auditory learning of a tutor's song and the fidelity of song imitation. Specifically, we paired infusions of NE or vehicle into the caudomedial nidopallium (NCM) with brief epochs of song tutoring. We analyzed the effect of NE in juvenile zebra finches that had or had not previously been exposed to song. Regardless of previous exposure to song, juveniles that received NE infusions into NCM during song tutoring produced songs that were more acoustically similar to the tutor song and that incorporated more elements of the tutor song than juveniles with control infusions. These data support the notion that NE can regulate the formation of sensory memories that shape the development of vocal behaviors that are used throughout an organism's life.NEW & NOTEWORTHY Although norepinephrine (NE) has been implicated in various forms of sensory learning, little is known about its contribution to sensory learning during critical periods in development. We reveal that pairing infusions of NE into the avian secondary auditory cortex with brief epochs of song tutoring significantly enhances auditory learning during the critical period for vocal learning. These data highlight the lasting impact of NE on sensory systems, cognition, and behavior.

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.

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.

Manipulations of inhibition in cortical circuitry differentially affect spectral and temporal features of Bengalese finch song.

The interplay between inhibition and excitation can regulate behavioral expression and control, including the expression of communicative behaviors like birdsong. Computational models postulate varying degrees to which inhibition within vocal motor circuitry influences birdsong, but few studies have tested these models by manipulating inhibition. Here we enhanced and attenuated inhibition in the cortical nucleus HVC (used as proper name) of Bengalese finches (Lonchura striata var. domestica). Enhancement of inhibition (with muscimol) in HVC dose-dependently reduced the amount of song produced. Infusions of higher concentrations of muscimol caused some birds to produce spectrally degraded songs, whereas infusions of lower doses of muscimol led to the production of relatively normal (nondegraded) songs. However, the spectral and temporal structures of these nondegraded songs were significantly different from songs produced under control conditions. In particular, muscimol infusions decreased the frequency and amplitude of syllables, increased various measures of acoustic entropy, and increased the variability of syllable structure. Muscimol also increased sequence durations and the variability of syllable timing and syllable sequencing. Attenuation of inhibition (with bicuculline) in HVC led to changes to song distinct from and often opposite to enhancing inhibition. For example, in contrast to muscimol, bicuculline infusions increased syllable amplitude, frequency, and duration and decreased the variability of acoustic features. However, like muscimol, bicuculline increased the variability of syllable sequencing. These data highlight the importance of inhibition to the production of stereotyped vocalizations and demonstrate that changes to neural dynamics within cortical circuitry can differentially affect spectral and temporal features of song.NEW & NOTEWORTHY We reveal that manipulations of inhibition in the cortical nucleus HVC affect the structure, timing, and sequencing of syllables in Bengalese finch song. Enhancing and blocking inhibition led to opposite changes to the acoustic structure and timing of vocalizations, but both caused similar changes to vocal sequencing. These data provide support for computational models of song control but also motivate refinement of existing models to account for differential effects on syllable structure, timing, and sequencing.

Towards a Physiological Scale of Vocal Fold Agent-Based Models of Surgical Injury and Repair: Sensitivity Analysis, Calibration and Verification.

Agent based models (ABM) were developed to numerically simulate the biological response to surgical vocal fold injury and repair at the physiological level. This study aimed to improve the representation of existing ABM through a combination of empirical and computational experiments. Empirical data of vocal fold cell populations including neutrophils, macrophages and fibroblasts were obtained using flow cytometry up to four weeks following surgical injury. Random Forests were used as a sensitivity analysis method to identify model parameters that were most influential to ABM outputs. Statistical Parameter Optimization Tool for Python was used to calibrate those parameter values to match the ABM-simulation data with the corresponding empirical data from Day 1 to Day 5 following surgery. Model performance was evaluated by verifying if the empirical data fell within the 95% confidence intervals of ABM outputs of cell quantities at Day 7, Week 2 and Week 4. For Day 7, all empirical data were within the ABM output ranges. The trends of ABM-simulated cell populations were also qualitatively comparable to those of the empirical data beyond Day 7. Exact values, however, fell outside of the 95% statistical confidence intervals. Parameters related to fibroblast proliferation were indicative to the ABM-simulation of fibroblast dynamics in final stages of wound healing.

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.

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.

EGR-1 Expression in Catecholamine-synthesizing Neurons Reflects Auditory Learning and Correlates with Responses in Auditory Processing Areas.

Distinguishing between familiar and unfamiliar individuals is an important task that shapes the expression of social behavior. As such, identifying the neural populations involved in processing and learning the sensory attributes of individuals is important for understanding mechanisms of behavior. Catecholamine-synthesizing neurons have been implicated in sensory processing, but relatively little is known about their contribution to auditory learning and processing across various vertebrate taxa. Here we investigated the extent to which immediate early gene expression in catecholaminergic circuitry reflects information about the familiarity of social signals and predicts immediate early gene expression in sensory processing areas in songbirds. We found that male zebra finches readily learned to differentiate between familiar and unfamiliar acoustic signals ('songs') and that playback of familiar songs led to fewer catecholaminergic neurons in the locus coeruleus (but not in the ventral tegmental area, substantia nigra, or periaqueductal gray) expressing the immediate early gene, EGR-1, than playback of unfamiliar songs. The pattern of EGR-1 expression in the locus coeruleus was similar to that observed in two auditory processing areas implicated in auditory learning and memory, namely the caudomedial nidopallium (NCM) and the caudal medial mesopallium (CMM), suggesting a contribution of catecholamines to sensory processing. Consistent with this, the pattern of catecholaminergic innervation onto auditory neurons co-varied with the degree to which song playback affected the relative intensity of EGR-1 expression. Together, our data support the contention that catecholamines like norepinephrine contribute to social recognition and the processing of social information.

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.

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.