Vocal Production Learning Research Articles

Auditory discrimination learning and acoustic cue weighing in female zebra finches with localized FoxP1 knockdowns.

Rare disruptions of the transcription factor FOXP1 are implicated in a human neurodevelopmental disorder characterized by autism and/or intellectual disability with prominent problems in speech and language abilities. Avian orthologues of this transcription factor are evolutionarily conserved and highly expressed in specific regions of songbird brains, including areas associated with vocal production learning and auditory perception. Here, we investigated possible contributions of FoxP1 to song discrimination and auditory perception in juvenile and adult female zebra finches. They received lentiviral knockdowns of FoxP1 in one of two brain areas involved in auditory stimulus processing, HVC (proper name) or CMM (caudomedial mesopallium). Ninety-six females, distributed over different experimental and control groups were trained to discriminate between two stimulus songs in an operant Go/Nogo paradigm and subsequently tested with an array of stimuli. This made it possible to assess how well they recognized and categorized altered versions of training stimuli and whether localized FoxP1 knockdowns affected the role of different features during discrimination and categorization of song. Although FoxP1 expression was significantly reduced by the knockdowns, neither discrimination of the stimulus songs nor categorization of songs modified in pitch, sequential order of syllables or by reversed playback were affected. Subsequently, we analyzed the full dataset to assess the impact of the different stimulus manipulations for cue weighing in song discrimination. Our findings show that zebra finches rely on multiple parameters for song discrimination, but with relatively more prominent roles for spectral parameters and syllable sequencing as cues for song discrimination.NEW & NOTEWORTHY In humans, mutations of the transcription factor FoxP1 are implicated in speech and language problems. In songbirds, FoxP1 has been linked to male song learning and female preference strength. We found that FoxP1 knockdowns in female HVC and caudomedial mesopallium (CMM) did not alter song discrimination or categorization based on spectral and temporal information. However, this large dataset allowed to validate different cue weights for spectral over temporal information for song recognition.

Vocal learning-associated convergent evolution in mammalian proteins and regulatory elements.

Vocal production learning ("vocal learning") is a convergently evolved trait in vertebrates. To identify brain genomic elements associated with mammalian vocal learning, we integrated genomic, anatomical, and neurophysiological data from the Egyptian fruit bat (Rousettus aegyptiacus) with analyses of the genomes of 215 placental mammals. First, we identified a set of proteins evolving more slowly in vocal learners. Then, we discovered a vocal motor cortical region in the Egyptian fruit bat, an emergent vocal learner, and leveraged that knowledge to identify active cis-regulatory elements in the motor cortex of vocal learners. Machine learning methods applied to motor cortex open chromatin revealed 50 enhancers robustly associated with vocal learning whose activity tended to be lower in vocal learners. Our research implicates convergent losses of motor cortex regulatory elements in mammalian vocal learning evolution.

Evolution of the syrinx of Apodiformes, including the vocal-learning Trochilidae (Aves: Strisores)

Abstract The vocal organ of birds, the syrinx, represents a key innovation in the evolutionary history of vertebrate communication. Three major avian clades: passerines, parrots, and hummingbirds, independently acquired both specialized syringeal structures and vocal-production learning, between which a functional relationship has been proposed but remains poorly understood. In hummingbirds, the syrinx has never been studied comparatively alongside non-learning relatives in the parent clade Strisores. Here we describe the anatomy of the syrinx in three swift species using enhanced-contrast computed tomography, which reveals structures previously unreported in the clade. We also tested for correlations between syringeal and acoustic traits in a sample of hummingbirds and swifts using phylogenetically informed regressions. The swift syrinx presents lateral labia located on the first pair of bronchial half-rings, which are present in hummingbirds and may be ancestral to Strisores. The further enlarged lateral labia of hummingbirds are found to be significantly correlated to the reduction in length of their trachea and m. tracheolateralis. Acquisition of intrinsic muscles and loss of the sternotrachealis muscle co-occur with these shifts. We recover a significant negative correlation between tracheal elongation and maximum vocalization frequency, suggesting that tracheal shortening in hummingbirds facilitated the acquisition of high-frequency vocalizing.

Examining the capability for rhythmic synchronization and music production in vocal learning parrot species.

Vocal production learning and beat perception and synchronization (BPS) share some common characteristics, which makes the vocal learning and rhythmic synchronization hypothesis (VLH) a reasonable explanation for the evolution of the capability for rhythmic synchronization. However, even in vocal learners, it is rare to see non-human animals demonstrate BPS to human music. Therefore, the first objective of this article is to propose some possible reasons why we do not see BPS in budgerigars, an excellent vocal learning species, while presenting some of my own findings. The second objective of this article is to propose a seamless bridge to connect the capability for vocal learning and BPS in locomotion. For this purpose, I present my own findings, wherein cockatiels spontaneously sang in synchrony with a melody of human music. This behavior can be considered a vocal version of BPS. Therefore, it can establish a connection between these two capabilities. This article agrees with the possibility that some mechanisms other than the vocal learning system may enable BPS, contrary to the original idea of VLH. Nevertheless, it is still reasonable to connect the capability for vocal learning and that for BPS. At the very least, the capability for vocal learning may contribute to the evolution of BPS. From these arguments, this article also proposes a scenario which includes vocalizing in synchrony as a driving force for the evolution of BPS and the capability for music production.

Song system neuroanatomy, and immediate early gene expression in a finch species with extensive male and female song.

Birdsong is a relatively well-studied behavior, both due to its importance as a model for vocal production learning and as an intriguing complex social behavior. Until the last few decades, work on birdsong focused almost exclusively on males. However, it is now widely accepted that female song not only exists, but is fairly common throughout the oscine passerines. Despite this, and the large number of researchers who have begun exploring female song in the field, researchers in the lab have been slow to adopt model species with female song. Studying female song in the lab is critical for our understanding of sex-specific factors in the physiology controlling this fascinating behavior. Additionally, as a model for vocal production learning in humans, understanding the mechanistic and neuroendocrine control of female song is clearly important. In this study, we examined the red-cheeked cordon bleu (RCCB), an Estrildid finch species with extensive female song. Specifically, we found that there were no significant sex differences in circulating levels of testosterone and progesterone, nor in song production rate. There were no significant differences in cell densities in the three nuclei of the song control system we examined. Additionally, the volume of the robust nucleus of the arcopallium was not significantly different and we report the smallest sex difference in HVC yet published in a songbird. Finally, we demonstrated similar levels of motor driven immediate early gene expression in both males and females after song production.

An ecological and neurobiological perspective on the evolution of vocal learning

Vocal production learning (VPL) involves the use of auditory experience to guide the production of novel signals or to modify pre-existing signals. It allows animals to develop signals that are more complex and/or more flexible than innately developed signals. It has evolved rarely in vocal animals, widespread only in three avian and four mammalian taxa. The evolution of VPL was accompanied by innovations of the vocal motor neural circuitry. VPL is rare because of its various costs. Ecology, social spacing, and social fluidity can favor the evolution of VPL. It is striking that most taxa with VPL evolved in visually limited habitats, where sound is the only effective channel for communicating over distance from sender to receiver. Selective factors that favor the ability to produce complex and/or flexible signals would act predominantly on acoustic signals, and favor the evolution of VPL. Learning may be the only practical way to develop a signal complex enough to encode different types of information for assessment by receivers in animals that rely on acoustic communication, or to modify signals as local social factors dictate.

Bottlenose dolphin mothers modify signature whistles in the presence of their own calves

Human caregivers interacting with children typically modify their speech in ways that promote attention, bonding, and language acquisition. Although this "motherese," or child-directed communication (CDC), occurs in a variety of human cultures, evidence among nonhuman species is very rare. We looked for its occurrence in a nonhuman mammalian species with long-term mother-offspring bonds that is capable of vocal production learning, the bottlenose dolphin (Tursiops truncatus). Dolphin signature whistles provide a unique opportunity to test for CDC in nonhuman animals, because we are able to quantify changes in the same vocalizations produced in the presence or absence of calves. We analyzed recordings made during brief catch-and-release events of wild bottlenose dolphins in waters near Sarasota Bay, Florida, United States, and found that females produced signature whistles with significantly higher maximum frequencies and wider frequency ranges when they were recorded with their own dependent calves vs. not with them. These differences align with the higher fundamental frequencies and wider pitch ranges seen in human CDC. Our results provide evidence in a nonhuman mammal for changes in the same vocalizations when produced in the presence vs. absence of offspring, and thus strongly support convergent evolution of motherese, or CDC, in bottlenose dolphins. CDC may function to enhance attention, bonding, and vocal learning in dolphin calves, as it does in human children. Our data add to the growing body of evidence that dolphins provide a powerful animal model for studying the evolution of vocal learning and language.

A survey of vocal mimicry in companion parrots

Parrots are one of the rare animal taxa with life-long vocal learning. Parrot vocal repertoires are difficult to study in the wild, but companion parrots offer a valuable data source. We surveyed the public about mimicry repertoires in companion parrots to determine whether vocal learning varied by (1) species, (2) sex, (3) age, and (4) social interaction with other parrots. Species differed significantly in mimicry ability, with grey parrots (Psittacus erithacus) having the largest mimicry repertoires. Analyses of all birds (n = 877) found no overarching effects of sex, age, or parrot-parrot social interactions on mimicry repertoires. Follow up analyses (n = 671), however, revealed a human bias to assume that talking parrots are male, and indicated that five of the 19 best-sampled species exhibited sex differences. Age-specific analyses of grey parrots (n = 187) indicated that repertoire size did not increase during adulthood. Most parrots were capable of improvisation (e.g. rearranging words) and used mimicry in appropriate human contexts. Results indicate that parrot vocal production learning varies among and within species, suggesting that the mechanisms and functions of learning also vary. Our data provide a rich foundation for future comparative research on avian vocalizations, and broaden our understanding of the underpinnings of communicative behavior and learning across all animals.

Spontaneous rhythm discrimination in a mammalian vocal learner.

Rhythm and vocal production learning are building blocks of human music and speech. Vocal learning has been hypothesized as a prerequisite for rhythmic capacities. Yet, no mammalian vocal learner but humans have shown the capacity to flexibly and spontaneously discriminate rhythmic patterns. Here we tested untrained rhythm discrimination in a mammalian vocal learning species, the harbour seal (Phoca vitulina). Twenty wild-born seals were exposed to music-like playbacks of conspecific call sequences varying in basic rhythmic properties. These properties were called length, sequence regularity, and overall tempo. All three features significantly influenced seals' reaction (number of looks and their duration), demonstrating spontaneous rhythm discrimination in a vocal learning mammal. This finding supports the rhythm–vocal learning hypothesis and showcases pinnipeds as promising models for comparative research on rhythmic phylogenies.

Selective alarm call mimicry in the sexual display of the male superb lyrebird (Menura novaehollandiae)

Despite much research on mimicry, little is known about the ecology of dynamic mimetic signals involving mimicry of multiple species. Some of the most conspicuous examples of phenotypically plastic mimicry are produced by oscine passerines, where vocal production learning enables some species to mimic multiple models and flexibly adjust what they mimic and when. While singing from a perch, male superb lyrebirds (Menura novaehollandiae) accurately imitate multiple songs and calls of over 20 species of bird. However, at key moments within their multimodal displays performed on display arenas on the forest floor, males mimic a small number of mobbing-alarm calls creating the acoustic illusion of a mixed-species mobbing flock (‘D-song’). Using observations from camera footage and a field-based playback experiment, we tested six hypotheses for alarm call model selection within D-song. Mimicked species were remarkably invariant, with 79% of D-song made up of imitations of just three different bird species. Males did not mimic the most common species in their general environment, but neither did they mimic rare species. Instead, males imitated the mobbing-alarm calls of heterospecific birds that foraged on or near the forest floor. Indeed, males primarily mimicked the alarm calls of heterospecific species that foraged alongside lyrebirds and were likely to appear together in experimentally-induced, terrestrial mobbing flocks. These findings support the hypothesis that males mimic a cue of a terrestrial predatory threat to lyrebirds, most likely to exploit the antipredator behaviour of female lyrebirds. Our study illustrates the importance of investigating the drivers of model selection in dynamic multi-model mimicry.

Are song sequencing rules learned by song sparrows?

Although the effects of learning on song structure have been extensively studied in songbirds, little attention has been given to the learning of syntax at the level of song sequences. Here we investigate song syntax learning in two cohorts of hand-reared song sparrows, Melospiza melodia : an isolate group, consisting of four males raised with no exposure to external song models, and a trained group, consisting of 17 males exposed to recorded song sequences during the sensitive period for song learning. The isolate males followed three syntactical rules previously described for field-recorded song sparrows: (1) they produced their song type repertoires with eventual variety, repeating a song type multiple times before switching to another; (2) they cycled through their repertoires using close to the minimum number of bouts; and (3) they showed consistent preferences for singing certain of their song types more than others. The trained males were tutored with sequences with exaggerated eventual variety and cycling patterns and no usage preferences, but their syntax was little affected by any of these training features. One syntactical pattern that was affected by external experience was the rule that long bouts of a song type are followed by long recurrence intervals before that type is produced again. Isolate males showed no bout length/recurrence interval correlations while trained males showed reduced correlations relative to field-recorded males, implicating learning in the development of the normal pattern. Other songbird species have been found to preferentially use song type transitions as adults that they were tutored with as juveniles, but the trained song sparrows in this study showed no evidence of such effects. • We examined the development of between-song syntax in song sparrows. • Singing with eventual variety is one syntactical pattern little affected by learning. • A second is the tendency to cycle efficiently through the song type repertoire. • Song sparrows do not learn first-order transition preferences from tutor sequences. • Usage learning is thus less prevalent than vocal production learning in this species.

Parselmouth for bioacoustics: Analysis pipelines for seal vocalizations

Every empirical research project includes bottlenecks at various levels. In bioacoustics, one of these time-consuming bottlenecks corresponds to the step of transforming a long stream of audio into acoustic properties of specific sounds. Here, we describe a data-extraction pipeline which integrates manual annotation with Parselmouth’s powerful computational analyses. This semi-supervised method allows extracting a large volume of sound features with limited repetitive human “point and click.” We illustrate this using recently published empirical research, where we focused on vocal production learning and plasticity in pinnipeds. Faced with a species capable of imitating sounds, fully automatic methods may misclassify individuals (because of imitation), while the large number of calls make fully manual approaches suboptimal and error-prone. Focusing on early vocal development, we tested 1–3 weeks-old harbor seal pups (Phoca vitulina). Noise playbacks served to induce seal pups to shift their fundamental frequency. Pups' spontaneous calls were recorded while exposed to bandpass-filtered noise, which spanned and masked the animals’ fundamental frequency range. After a summary manual annotation of calls’ boundaries, Parselmouth identified these boundaries in the files, and automatically extracted multiple sound parameters. Based on this, we found that pups modified their vocalizations by lowering their fundamental frequency in response to noise.

A cross-species framework to identify vocal learning abilities in mammals

Vocal production learning (VPL) is the experience-driven ability to produce novel vocal signals through imitation or modification of existing vocalizations. A parallel strand of research investigates acoustic allometry, namely how information about body size is conveyed by acoustic signals. Recently, we proposed that deviation from acoustic allometry principles as a result of sexual selection may have been an intermediate step towards the evolution of vocal learning abilities in mammals. Adopting a more hypothesis-neutral stance, here we perform phylogenetic regressions and other analyses further testing a potential link between VPL and being an allometric outlier. We find that multiple species belonging to VPL clades deviate from allometric scaling but in the opposite direction to that expected from size exaggeration mechanisms. In other words, our correlational approach finds an association between VPL and being an allometric outlier. However, the direction of this association, contra our original hypothesis, may indicate that VPL did not necessarily emerge via sexual selection for size exaggeration: VPL clades show higher vocalization frequencies than expected. In addition, our approach allows us to identify species with potential for VPL abilities: we hypothesize that those outliers from acoustic allometry lying above the regression line may be VPL species. Our results may help better understand the cross-species diversity, variability and aetiology of VPL, which among other things is a key underpinning of speech in our species.This article is part of the theme issue ‘Voice modulation: from origin and mechanism to social impact (Part II)’.

A researcher's guide to the comparative assessment of vocal production learning.

Vocal production learning (VPL) is the capacity to learn to produce new vocalizations, which is a rare ability in the animal kingdom and thus far has only been identified in a handful of mammalian taxa and three groups of birds. Over the last few decades, approaches to the demonstration of VPL have varied among taxa, sound production systems and functions. These discrepancies strongly impede direct comparisons between studies. In the light of the growing number of experimental studies reporting VPL, the need for comparability is becoming more and more pressing. The comparative evaluation of VPL across studies would be facilitated by unified and generalized reporting standards, which would allow a better positioning of species on any proposed VPL continuum. In this paper, we specifically highlight five factors influencing the comparability of VPL assessments: (i) comparison to an acoustic baseline, (ii) comprehensive reporting of acoustic parameters, (iii) extended reporting of training conditions and durations, (iv) investigating VPL function via behavioural, perception-based experiments and (v) validation of findings on a neuronal level. These guidelines emphasize the importance of comparability between studies in order to unify the field of vocal learning. This article is part of the theme issue 'Vocal learning in animals and humans'.

Vocal production learning in mammals revisited.

Vocal production learning, the ability to modify the structure of vocalizations as a result of hearing those of others, has been studied extensively in birds but less attention has been given to its occurrence in mammals. We summarize the available evidence for vocal learning in mammals from the last 25 years, updating earlier reviews on the subject. The clearest evidence comes from cetaceans, pinnipeds, elephants and bats where species have been found to copy artificial or human language sounds, or match acoustic models of different sound types. Vocal convergence, in which parameter adjustments within one sound type result in similarities between individuals, occurs in a wider range of mammalian orders with additional evidence from primates, mole-rats, goats and mice. Currently, the underlying mechanisms for convergence are unclear with vocal production learning but also usage learning or matching physiological states being possible explanations. For experimental studies, we highlight the importance of quantitative comparisons of seemingly learned sounds with vocal repertoires before learning started or with species repertoires to confirm novelty. Further studies on the mammalian orders presented here as well as others are needed to explore learning skills and limitations in greater detail.This article is part of the theme issue ‘Vocal learning in animals and humans’.

The role of vocal learning in call acquisition of wild grey seal pups.

Pinnipeds have been identified as one of the best available models for the study of vocal learning. Experimental evidence for their learning skills is demonstrated with advanced copying skills, particularly in formant structure when copying human speech sounds and melodies. By contrast, almost no data are available on how learning skills are used in their own communication systems. We investigated the impact of playing modified seal sounds in a breeding colony of grey seals (Halichoerus grypus) to study how acoustic input influenced vocal development of eight pups. Sequences of two or three seal pup calls were edited so that the average peak frequency between calls in a sequence changed up or down. We found that seals copied the specific stimuli played to them and that copies became more accurate over time. The differential response of different groups showed that vocal production learning was used to achieve conformity, suggesting that geographical variation in seal calls can be caused by horizontal cultural transmission. While learning of pup calls appears to have few benefits, we suggest that it also affects the development of the adult repertoire, which may facilitate social interactions such as mate choice.This article is part of the theme issue ‘Vocal learning in animals and humans’.

Variation in vocal production learning across songbirds.

Songbirds as a whole are considered to be vocal production learners, meaning that they modify the structure of their vocalizations as a result of experience with the vocalizations of others. The more than 4000 species of songbirds, however, vary greatly in crucial features of song development. Variable features include: (i) the normality of the songs of early-deafened birds, reflecting the importance of innate motor programmes in song development; (ii) the normality of the songs of isolation-reared birds, reflecting the combined importance of innate auditory templates and motor programmes; (iii) the degree of selectivity in choice of external models; (iv) the accuracy of copying from external models; and (v) whether or not learning from external models continues into adulthood. We suggest that because of this variability, some songbird species, specifically those that are able to develop songs in the normal range without exposure to external models, can be classified as limited vocal learners. Those species that require exposure to external models to develop songs in the normal range can be considered complex vocal learners. This article is part of the theme issue 'Vocal learning in animals and humans'.

Cross-species parallels in babbling: animals and algorithms.

A key feature of vocal ontogeny in a variety of taxa with extensive vocal repertoires is a developmental pattern in which vocal exploration is followed by a period of category formation that results in a mature species-specific repertoire. Vocal development preceding the adult repertoire is often called ‘babbling’, a term used to describe aspects of vocal development in species of vocal-learning birds, some marine mammals, some New World monkeys, some bats and humans. The paper summarizes the results of research on babbling in examples from five taxa and proposes a unifying definition facilitating their comparison. There are notable similarities across these species in the developmental pattern of vocalizations, suggesting that vocal production learning might require babbling. However, the current state of the literature is insufficient to confirm this suggestion. We suggest directions for future research to elucidate this issue, emphasizing the importance of (i) expanding the descriptive data and seeking species with complex mature repertoires where babbling may not occur or may occur only to a minimal extent; (ii) (quasi-)experimental research to tease apart possible mechanisms of acquisition and/or self-organizing development; and (iii) computational modelling as a methodology to test hypotheses about the origins and functions of babbling.This article is part of the theme issue ‘Vocal learning in animals and humans’.

Prenatal auditory learning in avian vocal learners and non-learners.

Understanding when learning begins is critical for identifying the factors that shape both the developmental course and the function of information acquisition. Until recently, sufficient development of the neural substrates for any sort of vocal learning to begin in songbirds was thought to be reached well after hatching. New research shows that embryonic gene activation and the outcome of vocal learning can be modulated by sound exposure in ovo. We tested whether avian embryos across lineages differ in their auditory response strength and sound learning in ovo, which we studied in vocal learning (Maluridae, Geospizidae) and vocal non-learning (Phasianidae, Spheniscidae) taxa. While measuring heart rate in ovo, we exposed embryos to (i) conspecific or heterospecific vocalizations, to determine their response strength, and (ii) conspecific vocalizations repeatedly, to quantify cardiac habituation, a form of non-associative learning. Response strength towards conspecific vocalizations was greater in two species with vocal production learning compared to two species without. Response patterns consistent with non-associative auditory learning occurred in all species. Our results demonstrate a capacity to perceive and learn to recognize sounds in ovo, as evidenced by habituation, even in species that were previously assumed to have little, if any, vocal production learning.This article is part of the theme issue ‘Vocal learning in animals and humans’.

The multi-dimensional nature of vocal learning.

How learning affects vocalizations is a key question in the study of animal communication and human language. Parallel efforts in birds and humans have taught us much about how vocal learning works on a behavioural and neurobiological level. Subsequent efforts have revealed a variety of cases among mammals in which experience also has a major influence on vocal repertoires. Janik and Slater (Anim. Behav. 60, 1–11. (doi:10.1006/anbe.2000.1410)) introduced the distinction between vocal usage and production learning, providing a general framework to categorize how different types of learning influence vocalizations. This idea was built on by Petkov and Jarvis (Front. Evol. Neurosci. 4, 12. (doi:10.3389/fnevo.2012.00012)) to emphasize a more continuous distribution between limited and more complex vocal production learners. Yet, with more studies providing empirical data, the limits of the initial frameworks become apparent. We build on these frameworks to refine the categorization of vocal learning in light of advances made since their publication and widespread agreement that vocal learning is not a binary trait. We propose a novel classification system, based on the definitions by Janik and Slater, that deconstructs vocal learning into key dimensions to aid in understanding the mechanisms involved in this complex behaviour. We consider how vocalizations can change without learning, and a usage learning framework that considers context specificity and timing. We identify dimensions of vocal production learning, including the copying of auditory models (convergence/divergence on model sounds, accuracy of copying), the degree of change (type and breadth of learning) and timing (when learning takes place, the length of time it takes and how long it is retained). We consider grey areas of classification and current mechanistic understanding of these behaviours. Our framework identifies research needs and will help to inform neurobiological and evolutionary studies endeavouring to uncover the multi-dimensional nature of vocal learning.This article is part of the theme issue ‘Vocal learning in animals and humans’.