Vocal Production Learning Research Articles

Vocal learning in animals and humans.

Vocal learning in animals and humans.

Vocal imitations and production learning by Australian musk ducks (Biziura lobata).

Acquiring vocalizations by learning them from other individuals is only known from a limited number of animal groups. For birds, oscine and some suboscine songbirds, parrots and hummingbirds demonstrate this ability. Here, we provide evidence for vocal learning in a member of a basal clade of the avian phylogeny: the Australian musk duck (Biziura lobata). A hand-reared individual imitated a slamming door and a human voice, and a female-reared individual imitated Pacific black duck quacks. These sounds have been described before, but were never analysed in any detail and went so far unnoticed by researchers of vocal learning. The imitations were produced during the males' advertising display. The hand-reared male used at least three different vocalizations in the display context, with each one produced in the same stereotyped and repetitive structure as the normal display sounds. Sounds of different origins could be combined in one vocalization and at least some of the imitations were memorized at an early age, well before they were produced later in life. Together with earlier observations of vocal differences between populations and deviant vocalizations in captive-reared individuals, these observations demonstrate the presence of advanced vocal learning at a level comparable to that of songbirds and parrots. We discuss the rearing conditions that may have given rise to the imitations and suggest that the structure of the duck vocalizations indicates a quite sophisticated and flexible control over the vocal production mechanism. The observations support the hypothesis that vocal learning in birds evolved in several groups independently rather than evolving once with several losses.This article is part of the theme issue ‘Vocal learning in animals and humans’.

Re-evaluating vocal production learning in non-oscine birds.

The study of vocal production learning in birds is heavily biased towards oscine songbirds, making the songbird model the reference for comparative studies. However, as vocal learning was probably ancestral in songbirds, interspecific variations might all be variations on a single theme and need not be representative of the nature and characteristics of vocal learning in other bird groups. To assess the possible mechanisms of vocal learning and its evolution therefore requires knowledge about independently evolved incidences of vocal learning. This review examines the presence and nature of vocal production learning in non-songbirds. Using a broad definition of vocal learning and a comparative phylogenetic framework, I evaluate the evidence for vocal learning and its characteristics in non-oscine birds, including well-known vocal learners such as parrots and hummingbirds but also (putative) cases from other taxa. Despite the sometimes limited evidence, it is clear that vocal learning occurs in a range of different, non-related, taxa and can be caused by a variety of mechanisms. It is more widespread than often realized, calling for more systematic studies. Examining this variation may provide a window onto the evolution of vocal learning and increase the value of comparative research for understanding vocal learning in humans.This article is part of the theme issue ‘Vocal learning in animals and humans’.

Operant control and call usage learning in African elephants.

Elephants exhibit remarkable vocal plasticity, and case studies reveal that individuals of African savannah (Loxodonta africana) and Asian (Elephas maximus) elephants are capable of vocal production learning. Surprisingly, however, little is known about contextual learning (usage and comprehension learning) in elephant communication. Usage learning can be demonstrated by training animals to vocalize in an arbitrary (cue-triggered) context. Here we show that adult African savannah elephants (n = 13) can vocalize in response to verbal cues, reliably producing social call types such as the low-frequency rumble, trumpets and snorts as well as atypical sounds using various mechanisms, thus displaying compound vocal control. We further show that rumbles emitted upon trainer cues differ significantly in structure from rumbles triggered by social contexts of the same individuals (n = 6). Every form of social learning increases the complexity of a communication system. In elephants, we only poorly understand their vocal learning abilities and the underlying cognitive mechanisms. Among other research, this calls for controlled learning experiments in which the prerequisite is operant/volitional control of vocalizations.This article is part of the theme issue ‘Vocal learning in animals and humans’.

Constraints on vocal production learning in budgerigars (Melopsittacus undulates)

Budgerigars (Melopsittacus undulatus) are small Australian parrots with a well-documented, learned vocal repertoire and a high degree of vocal production learning. These birds live in large, social flocks and they vocally interact with each other in a dynamic, reciprocal manner. We assume that budgerigars must process and integrate a wide variety of sensory stimuli when selecting appropriate vocal responses to conspecifics during vocal interactions, but the relative contributions of these different stimuli to that process are next to impossible to tease apart in a natural context. Here we show that budgerigars, under operant control, can learn to respond to specific stimuli with a specific vocal response. Budgerigars were trained to produce contact calls to a combination of auditory and visual cues. Birds learned to produce specific contact calls to stimuli that differed either in location (visual or auditory) or quality (visual). Interestingly, the birds could not learn to associate different vocal responses with different auditory stimuli coming from the same location. Surprisingly, this was so even when the auditory stimuli and the responses were the same (i.e., the bird’s own contact call). These results show that even in a highly controlled operant context, acoustic cues alone were not sufficient to support vocal production learning in budgerigars. From a different perspective, these results highlight the significant role that social interaction likely plays in vocal production learning so elegantly shown by Irene Pepperberg’s work in parrots.

Do Bats Have the Necessary Prerequisites for Symbolic Communication?

Training animals such as apes, gray parrots, or dolphins that communicate via arbitrary symbols with humans has revealed astonishing mental capacities that may have otherwise gone unnoticed. Albeit bats have not yet been trained to communicate via symbols with humans, we are convinced that some species, especially captive Pteropodid bats (“flying foxes”), show the potential to master this cognitive task. Here, we briefly review what is known about bats’ cognitive skills that constitute relevant prerequisites for symbolic communication with humans. We focus on social learning in general, trainability by humans, associative learning from humans, imitation, vocal production learning and usage learning, and social knowledge. Moreover, we highlight potential training paradigms that could be used to elicit simple “symbolic” bat-human communication, i.e., training bats to select arbitrary symbols on a touchscreen to elicit a desired behavior of the human caregiver. Touchscreen-proficient bats could participate in cognition research, e.g., to study their numerical competence or categorical perception, to further elucidate how nonhuman animals learn and perceive the world.

An Unbiased Molecular Approach Using 3′-UTRs Resolves the Avian Family-Level Tree of Life

Presumably, due to a rapid early diversification, major parts of the higher-level phylogeny of birds are still resolved controversially in different analyses or are considered unresolvable. To address this problem, we produced an avian tree of life, which includes molecular sequences of one or several species of ∼90% of the currently recognized family-level taxa (429 species, 379 genera) including all 106 family-level taxa of the nonpasserines and 115 of the passerines (Passeriformes). The unconstrained analyses of noncoding 3-prime untranslated region (3′-UTR) sequences and those of coding sequences yielded different trees. In contrast to the coding sequences, the 3′-UTR sequences resulted in a well-resolved and stable tree topology. The 3′-UTR contained, unexpectedly, transcription factor binding motifs that were specific for different higher-level taxa. In this tree, grebes and flamingos are the sister clade of all other Neoaves, which are subdivided into five major clades. All nonpasserine taxa were placed with robust statistical support including the long-time enigmatic hoatzin (Opisthocomiformes), which was found being the sister taxon of the Caprimulgiformes. The comparatively late radiation of family-level clades of the songbirds (oscine Passeriformes) contrasts with the attenuated diversification of nonpasseriform taxa since the early Miocene. This correlates with the evolution of vocal production learning, an important speciation factor, which is ancestral for songbirds and evolved convergent only in hummingbirds and parrots. As 3′-UTR-based phylotranscriptomics resolved the avian family-level tree of life, we suggest that this procedure will also resolve the all-species avian tree of life

Shared calls in repertoires of two locally distant gray parrots (Psittacus erithacus)

Parrots belong to the handful of animal species capable of vocal production learning. They are considered to be open-ended learners with complex and variable vocalizations. It is not known, however, to what extent their repertoires are shared among individuals within a group or between vocally isolated individuals or groups. In study 1, we mapped the repertoire of four captive African gray parrots (Psittacus erithacus) using a combination of three acoustic analyses. In study 2, we compared the repertoire of two female African gray parrots from two different laboratories who had never been in vocal contact with each other or any member of the other parrot’s social group. Results of study 1 showed a relatively large agreement between all three methods used to analyze the vocalizations. Almost three quarters (72.8%) of categories determined by visual-acoustic analysis were confirmed by at least one of the two computer-aided methods used, i.e., by spectrographic cross-correlation and/or a multiparametric statistical method. In study 2, we found a relatively large proportion of calls shared between the repertoires of the two gray parrot subjects. Over half and over a fourth of calls produced by parrots with the smaller and the larger repertoire, respectively, were shared between the two. No previous study identified such a large proportion of intergroup shared calls within this parrot species. It seems that some calls tend to reappear in vocally isolated groups based on inherited predispositions, similarly as has been documented in songbirds.

The hummingbird syrinx morphome: a detailed three-dimensional description of the black jacobin\u2019s vocal organ

BackgroundThe ability to imitate sounds depends on a process called vocal production learning, a rare evolutionary trait. In addition to the few mammalian groups that possess this ability, vocal production learning has evolved independently in three avian clades: songbirds, parrots, and hummingbirds. Although the anatomy and mechanisms of sound production in songbirds are well understood, little is known about the hummingbird’s vocal anatomy.ResultsWe use high-resolution micro-computed tomography (μCT) and microdissection to reveal the three-dimensional structure of the syrinx, the vocal organ of the black jacobin (Florisuga fusca), a phylogenetically basal hummingbird species. We identify three features of the black jacobin’s syrinx: (i) a shift in the position of the syrinx to the outside of the thoracic cavity and the related loss of the sterno-tracheal muscle, (ii) complex intrinsic musculature, oriented dorso-ventrally, and (iii) ossicles embedded in the medial vibratory membranes.ConclusionsThe extra-thoracic placement of the black jacobin’s syrinx and the dorso-ventrally oriented musculature likely aid to uncoupling syrinx movements from extensive flight-related thorax constraints. The syrinx morphology further allows for vibratory decoupling, precise control of complex acoustic parameters, and a large motor redundancy that may be key biomechanical factors leading to acoustic complexity and thus facilitating the occurrence of vocal production learning.

Comparison of methods for rhythm analysis of complex animals' acoustic signals.

Analyzing the rhythm of animals' acoustic signals is of interest to a growing number of researchers: evolutionary biologists want to disentangle how these structures evolved and what patterns can be found, and ecologists and conservation biologists aim to discriminate cryptic species on the basis of parameters of acoustic signals such as temporal structures. Temporal structures are also relevant for research on vocal production learning, a part of which is for the animal to learn a temporal structure. These structures, in other words, these rhythms, are the topic of this paper. How can they be investigated in a meaningful, comparable and universal way? Several approaches exist. Here we used five methods to compare their suitability and interpretability for different questions and datasets and test how they support the reproducibility of results and bypass biases. Three very different datasets with regards to recording situation, length and context were analyzed: two social vocalizations of Neotropical bats (multisyllabic, medium long isolation calls of Saccopteryx bilineata, and monosyllabic, very short isolation calls of Carollia perspicillata) and click trains of sperm whales, Physeter macrocephalus. Techniques to be compared included Fourier analysis with a newly developed goodness-of-fit value, a generate-and-test approach where data was overlaid with varying artificial beats, and the analysis of inter-onset-intervals and calculations of a normalized Pairwise Variability Index (nPVI). We discuss the advantages and disadvantages of the methods and we also show suggestions on how to best visualize rhythm analysis results. Furthermore, we developed a decision tree that will enable researchers to select a suitable and comparable method on the basis of their data.

Vocal production learning in the pale spear-nosed bat, Phyllostomus discolor.

Vocal production learning (VPL), or the ability to modify vocalizations through the imitation of sounds, is a rare trait in the animal kingdom. While humans are exceptional vocal learners, few other mammalian species share this trait. Owing to their singular ecology and lifestyle, bats are highly specialized for the precise emission and reception of acoustic signals. This specialization makes them ideal candidates for the study of vocal learning, and several bat species have previously shown evidence supportive of vocal learning. Here we use a sophisticated automated set-up and a contingency training paradigm to explore the vocal learning capacity of pale spear-nosed bats. We show that these bats are capable of directional change of the fundamental frequency of their calls according to an auditory target. With this study, we further highlight the importance of bats for the study of vocal learning and provide evidence for the VPL capacity of the pale spear-nosed bat.

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.

Towards a new taxonomy of primate vocal production learning.

The extent to which vocal learning can be found in nonhuman primates is key to reconstructing the evolution of speech. Regarding the adjustment of vocal output in relation to auditory experience (vocal production learning in the narrow sense), effects on the ontogenetic trajectory of vocal development as well as adjustment to group-specific call features have been found. Yet, a comparison of the vocalizations of different primate genera revealed striking similarities in the structure of calls and repertoires in different species of the same genus, indicating that the structure of nonhuman primate vocalizations is highly conserved. Thus, modifications in relation to experience only appear to be possible within relatively tight species-specific constraints. By contrast, comprehension learning may be extremely rapid and open-ended. In conjunction, these findings corroborate the idea of an ancestral independence of vocal production and auditory comprehension learning. To overcome the futile debate about whether or not vocal production learning can be found in nonhuman primates, we suggest putting the focus on the different mechanisms that may mediate the adjustment of vocal output in response to experience; these mechanisms may include auditory facilitation and learning from success. This article is part of the theme issue 'What can animal communication teach us about human language?'

Differential Song Deficits after Lentivirus-Mediated Knockdown of FoxP1, FoxP2, or FoxP4 in Area X of Juvenile Zebra Finches.

Mutations in the transcription factors FOXP1 and FOXP2 are associated with speech impairments. FOXP1 is additionally linked to cognitive deficits, as is FOXP4. These FoxP proteins are highly conserved in vertebrates and expressed in comparable brain regions, including the striatum. In male zebra finches, experimental manipulation of FoxP2 in Area X, a striatal song nucleus essential for vocal production learning, affects song development, adult song production, dendritic spine density, and dopamine-regulated synaptic transmission of striatal neurons. We previously showed that, in the majority of Area X neurons FoxP1, FoxP2, and FoxP4 are coexpressed, can dimerize and multimerize with each other and differentially regulate the expression of target genes. These findings raise the possibility that FoxP1, FoxP2, and FoxP4 (FoxP1/2/4) affect neural function differently and in turn vocal learning. To address this directly, we downregulated FoxP1 or FoxP4 in Area X of juvenile zebra finches and compared the resulting song phenotypes with the previously described inaccurate and incomplete song learning after FoxP2 knockdown. We found that experimental downregulation of FoxP1 and FoxP4 led to impaired song learning with partly similar features as those reported for FoxP2 knockdowns. However, there were also specific differences between the groups, leading us to suggest that specific features of the song are differentially impacted by developmental manipulations of FoxP1/2/4 expression in Area X.SIGNIFICANCE STATEMENT We compared the effects of experimentally reduced expression of the transcription factors FoxP1, FoxP2, and FoxP4 in a striatal song nucleus, Area X, on vocal production learning in juvenile male zebra finches. We show, for the first time, that these temporally and spatially precise manipulations of the three FoxPs affect spectral and temporal song features differentially. This is important because it raises the possibility that the different FoxPs control different aspects of vocal learning through combinatorial gene expression or by acting in different microcircuits within Area X. These results are consistent with the deleterious effects of human FOXP1 and FOXP2 mutations on speech and language and add FOXP4 as a possible candidate gene for vocal disorders.

Formant Modification through Vocal Production Learning in Gray Seals

Vocal production learning is a rare communication skill and has only been found in selected avian and mammalian species [1-4]. Although humans use learned formants and voiceless sounds to encode most lexical information [5], evidence for vocal learning in other animals tends to focus on the modulation pattern of the fundamental frequency [3, 4]. Attempts to teach mammals to produce human speech sounds have largely been unsuccessful, most notably in extensive studies on great apes [5]. The limited evidence for formant copying in mammals raises the question whether advanced learned control over formant production is uniquely human. We show that gray seals (Halichoerus grypus) have the ability to match modulations in peak frequency patterns of call sequences or melodies by modifying the formants in their own calls, moving outside of their normal repertoire's distribution of frequencies and even copying human vowel sounds. Seals also demonstrated enhanced auditory memory for call sequences by accurately copying sequential changes in peak frequency and the number of calls played to them. Our results demonstrate that formants can be influenced by vocal production learning in non-human vocal learners, providing a mammalian substrate for the evolution of flexible information coding in formants as found in human language.

Comment on "Temporal and spatial variation in harbor seal (Phoca vitulina L.) roar calls from southern Scandinavia" [J. Acoust. Soc. Am. 141, 1824-1834 (2017)

In their recent article, Sabinsky and colleagues investigated heterogeneity in harbor seals' vocalizations. The authors found seasonal and geographical variation in acoustic parameters, warning readers that recording conditions might account for some of their results. This paper expands on the temporal aspect of the encountered heterogeneity in harbor seals' vocalizations. Temporal information is the least susceptible to variable recording conditions. Hence geographical and seasonal variability in roar timing constitutes the most robust finding in the target article. In pinnipeds, evidence of timing and rhythm in the millisecond range-as opposed to circadian and seasonal rhythms-has theoretical and interdisciplinary relevance. In fact, the study of rhythm and timing in harbor seals is particularly decisive to support or confute a cross-species hypothesis, causally linking the evolution of vocal production learning and rhythm. The results by Sabinsky and colleagues can shed light on current scientific questions beyond pinniped bioacoustics, and help formulate empirically testable predictions.

The function and mechanism of vocal accommodation in humans and other primates.

The study of non-human animals, in particular primates, can provide essential insights into language evolution. A critical element of language is vocal production learning, i.e. learning how to produce calls. In contrast to other lineages such as songbirds, vocal production learning of completely new signals is strikingly rare in non-human primates. An increasing body of research, however, suggests that various species of non-human primates engage in vocal accommodation and adjust the structure of their calls in response to environmental noise or conspecific vocalizations. To date it is unclear what role vocal accommodation may have played in language evolution, in particular because it summarizes a variety of heterogeneous phenomena which are potentially achieved by different mechanisms. In contrast to non-human primates, accommodation research in humans has a long tradition in psychology and linguistics. Based on theoretical models from these research traditions, we provide a new framework which allows comparing instances of accommodation across species, and studying them according to their underlying mechanism and ultimate biological function. We found that at the mechanistic level, many cases of accommodation can be explained with an automatic perception-production link, but some instances arguably require higher levels of vocal control. Functionally, both human and non-human primates use social accommodation to signal social closeness or social distance to a partner or social group. Together, this indicates that not only some vocal control, but also the communicative function of vocal accommodation to signal social closeness and distance must have evolved prior to the emergence of language, rather than being the result of it. Vocal accommodation as found in other primates has thus endowed our ancestors with pre-adaptations that may have paved the way for language evolution.

An intra-population analysis of the indris\u2019 song dissimilarity in the light of genetic distance

The increasing interest in the evolution of human language has led several fields of research to focus on primate vocal communication. The ‘singing primates’, which produce elaborated and complex sequences of vocalizations, are of particular interest for this topic. Indris (Indri indri) are the only singing lemurs and emit songs whose most distinctive portions are “descending phrases” consisting of 2-5 units. We examined how the structure of the indris’ phrases varied with genetic relatedness among individuals. We tested whether the acoustic structure could provide conspecifics with information about individual identity and group membership. When analyzing phrase dissimilarity and genetic distance of both sexes, we found significant results for males but not for females. We found that similarity of male song-phrases correlates with kin in both time and frequency parameters, while, for females, this information is encoded only in the frequency of a single type. Song phrases have consistent individual-specific features, but we did not find any potential for advertising group membership. We emphasize the fact that genetic and social factors may play a role in the acoustic plasticity of female indris. Altogether, these findings open a new perspective for future research on the possibility of vocal production learning in these primates.

Evidence for Dialects in Three Captive Populations of Common Marmosets (Callithrix jacchus)

The vocal repertoires of nonhuman primates have long been thought to be invariable across populations and not to result from vocal learning. However, increasing evidence suggests that learning does influence vocal production in nonhuman primates, and that several species modify the structure of their calls in response to social or environmental influences. Vocal usage learning refers to the process whereby an individual learns in which circumstances to produce a certain call type, whereas vocal production learning refers to the process in which signals get modified as the result of individual experiences. Common marmosets (Callithrix jacchus) show socially mediated vocal plasticity as adults and during vocal development. This propensity to engage in simple forms of vocal production learning (accommodation) should produce population-level differences in call structure. To test this prediction, we compared the vocalizations of three captive populations of common marmosets. We analyzed the acoustic structure of 1337 phee calls, 461 trills, and 3611 food calls and compared them with a permutated discriminant function analysis. We found that all call types differed significantly between the three populations, and 76–98% of the calls were correctly classified. As physical differences in body mass and environmental differences between colonies could not explain the call differences, we conclude that vocal accommodation is the most likely explanation for the differences in call structure. This will allow us to further investigate the role and importance of vocal learning in a species increasingly used to study vocal learning and language evolution.

"Bird Song Metronomics": Isochronous Organization of Zebra Finch Song Rhythm.

The human capacity for speech and vocal music depends on vocal imitation. Songbirds, in contrast to non-human primates, share this vocal production learning with humans. The process through which birds and humans learn many of their vocalizations as well as the underlying neural system exhibit a number of striking parallels and have been widely researched. In contrast, rhythm, a key feature of language, and music, has received surprisingly little attention in songbirds. Investigating temporal periodicity in bird song has the potential to inform the relationship between neural mechanisms and behavioral output and can also provide insight into the biology and evolution of musicality. Here we present a method to analyze birdsong for an underlying rhythmic regularity. Using the intervals from one note onset to the next as input, we found for each bird an isochronous sequence of time stamps, a “signal-derived pulse,” or pulseS, of which a subset aligned with all note onsets of the bird's song. Fourier analysis corroborated these results. To determine whether this finding was just a byproduct of the duration of notes and intervals typical for zebra finches but not dependent on the individual duration of elements and the sequence in which they are sung, we compared natural songs to models of artificial songs. Note onsets of natural song deviated from the pulseS significantly less than those of artificial songs with randomized note and gap durations. Thus, male zebra finch song has the regularity required for a listener to extract a perceived pulse (pulseP), as yet untested. Strikingly, in our study, pulsesS that best fit note onsets often also coincided with the transitions between sub-note elements within complex notes, corresponding to neuromuscular gestures. Gesture durations often equaled one or more pulseS periods. This suggests that gesture duration constitutes the basic element of the temporal hierarchy of zebra finch song rhythm, an interesting parallel to the hierarchically structured components of regular rhythms in human music.