The postnatal ontogeny of the sexually dimorphic vocal apparatus in goitred gazelles (Gazella subgutturosa)

This study quantitatively documents the progressive development of sexual dimorphism of the vocal organs along the ontogeny of the goitred gazelle (Gazella subgutturosa). The major, male‐specific secondary sexual features, of vocal anatomy in goitred gazelle are an enlarged larynx and a marked laryngeal descent. These features appear to have evolved by sexual selection and may serve as a model for similar events in male humans. Sexual dimorphism of larynx size and larynx position in adult goitred gazelles is more pronounced than in humans, whereas the vocal anatomy of neonate goitred gazelles does not differ between sexes. This study examines the vocal anatomy of 19 (11 male, 8 female) goitred gazelle specimens across three age‐classes, that is, neonates, subadults and mature adults. The postnatal ontogenetic development of the vocal organs up to their respective end states takes considerably longer in males than in females. Both sexes share the same features of vocal morphology but differences emerge in the course of ontogeny, ultimately resulting in the pronounced sexual dimorphism of the vocal apparatus in adults. The main differences comprise larynx size, vocal fold length, vocal tract length, and mobility of the larynx. The resilience of the thyrohyoid ligament and the pharynx, including the soft palate, and the length changes during contraction and relaxation of the extrinsic laryngeal muscles play a decisive role in the mobility of the larynx in both sexes but to substantially different degrees in adult females and males. Goitred gazelles are born with an undescended larynx and, therefore, larynx descent has to develop in the course of ontogeny. This might result from a trade‐off between natural selection and sexual selection requiring a temporal separation of different laryngeal functions at birth and shortly after from those later in life. J. Morphol. 277:826–844, 2016. © 2016 Wiley Periodicals, Inc.     

The gradual vocal responses to human-provoked discomfort in farmed silver foxes

Vocal indicators of welfare have proven their use for many farmed and zoo animals and may be applied to farmed silver foxes as these animals display high vocal activity toward humans. Farmed silver foxes were selected mainly for fur, size, and litter sizes, but not for attitudes to people, so they are fearful of humans and have short-term welfare problems in their proximity. With a human approach test, we designed here the steady increase and decrease of fox–human distance and registered vocal responses of 25 farmed silver foxes. We analyzed the features of vocalizations produced by the foxes at different fox–human distances, assuming that changes in vocal responses reflect the degrees of human-related discomfort. For revealing the discomfort-related vocal traits in farmed silver foxes, we proposed and tested the algorithm of “joint calls,” equally applicable for analysis of all calls independently on their structure, either tonal or noisy. We discuss that the increase in proportion of time spent vocalizing and the shift of call energy toward higher frequencies may be integral vocal characteristics of short-term welfare problems in farmed silver foxes and probably in other captive mammals.     

Development of Auditory-Vocal Perceptual Skills in Songbirds

Songbirds are one of the few groups of animals that learn the sounds used for vocal communication during development. Like humans, songbirds memorize vocal sounds based on auditory experience with vocalizations of adult “tutors”, and then use auditory feedback of self-produced vocalizations to gradually match their motor output to the memory of tutor sounds. In humans, investigations of early vocal learning have focused mainly on perceptual skills of infants, whereas studies of songbirds have focused on measures of vocal production. In order to fully exploit songbirds as a model for human speech, understand the neural basis of learned vocal behavior, and investigate links between vocal perception and production, studies of songbirds must examine both behavioral measures of perception and neural measures of discrimination during development. Here we used behavioral and electrophysiological assays of the ability of songbirds to distinguish vocal calls of varying frequencies at different stages of vocal learning. The results show that neural tuning in auditory cortex mirrors behavioral improvements in the ability to make perceptual distinctions of vocal calls as birds are engaged in vocal learning. Thus, separate measures of neural discrimination and behavioral perception yielded highly similar trends during the course of vocal development. The timing of this improvement in the ability to distinguish vocal sounds correlates with our previous work showing substantial refinement of axonal connectivity in cortico-basal ganglia pathways necessary for vocal learning.     

Auditory–vocal mirroring in songbirds

Mirror neurons are theorized to serve as a neural substrate for spoken language in humans, but the existence and functions of auditory–vocal mirror neurons in the human brain remain largely matters of speculation. Songbirds resemble humans in their capacity for vocal learning and depend on their learned songs to facilitate courtship and individual recognition. Recent neurophysiological studies have detected putative auditory–vocal mirror neurons in a sensorimotor region of the songbird''s brain that plays an important role in expressive and receptive aspects of vocal communication. This review discusses the auditory and motor-related properties of these cells, considers their potential role on song learning and communication in relation to classical studies of birdsong, and points to the circuit and developmental mechanisms that may give rise to auditory–vocal mirroring in the songbird''s brain.     

Songbird: a unique animal model for studying the molecular basis of disorders of vocal development and communication

Like humans, songbirds are one of the few animal groups that learn vocalization. Vocal learning requires coordination of auditory input and vocal output using auditory feedback to guide one’s own vocalizations during a specific developmental stage known as the critical period. Songbirds are good animal models for understand the neural basis of vocal learning, a complex form of imitation, because they have many parallels to humans with regard to the features of vocal behavior and neural circuits dedicated to vocal learning. In this review, we will summarize the behavioral, neural, and genetic traits of birdsong. We will also discuss how studies of birdsong can help us understand how the development of neural circuits for vocal learning and production is driven by sensory input (auditory information) and motor output (vocalization).     

The role of auditory feedback in vocal learning and maintenance

Auditory experience is critical for the acquisition and maintenance of learned vocalizations in both humans and songbirds. Despite the central role of auditory feedback in vocal learning and maintenance, where and how auditory feedback affects neural circuits important to vocal control remain poorly understood. Recent studies of singing birds have uncovered neural mechanisms by which feedback perturbations affect vocal plasticity and also have identified feedback-sensitive neurons at or near sites of auditory and vocal motor interaction. Additionally, recent studies in marmosets have underscored that even in the absence of vocal learning, vocalization remains flexible in the face of changing acoustical environments, pointing to rapid interactions between auditory and vocal motor systems. Finally, recent studies show that a juvenile songbird's initial auditory experience of a song model has long-lasting effects on sensorimotor neurons important to vocalization, shedding light on how auditory memories and feedback interact to guide vocal learning.     

Convergent differential regulation of parvalbumin in the brains of vocal learners

Spoken language and learned song are complex communication behaviors found in only a few species, including humans and three groups of distantly related birds--songbirds, parrots, and hummingbirds. Despite their large phylogenetic distances, these vocal learners show convergent behaviors and associated brain pathways for vocal communication. However, it is not clear whether this behavioral and anatomical convergence is associated with molecular convergence. Here we used oligo microarrays to screen for genes differentially regulated in brain nuclei necessary for producing learned vocalizations relative to adjacent brain areas that control other behaviors in avian vocal learners versus vocal non-learners. A top candidate gene in our screen was a calcium-binding protein, parvalbumin (PV). In situ hybridization verification revealed that PV was expressed significantly higher throughout the song motor pathway, including brainstem vocal motor neurons relative to the surrounding brain regions of all distantly related avian vocal learners. This differential expression was specific to PV and vocal learners, as it was not found in avian vocal non-learners nor for control genes in learners and non-learners. Similar to the vocal learning birds, higher PV up-regulation was found in the brainstem tongue motor neurons used for speech production in humans relative to a non-human primate, macaques. These results suggest repeated convergent evolution of differential PV up-regulation in the brains of vocal learners separated by more than 65-300 million years from a common ancestor and that the specialized behaviors of learned song and speech may require extra calcium buffering and signaling.     

Of Mice,Birds, and Men: The Mouse Ultrasonic Song System Has Some Features Similar to Humans and Song-Learning Birds

Humans and song-learning birds communicate acoustically using learned vocalizations. The characteristic features of this social communication behavior include vocal control by forebrain motor areas, a direct cortical projection to brainstem vocal motor neurons, and dependence on auditory feedback to develop and maintain learned vocalizations. These features have so far not been found in closely related primate and avian species that do not learn vocalizations. Male mice produce courtship ultrasonic vocalizations with acoustic features similar to songs of song-learning birds. However, it is assumed that mice lack a forebrain system for vocal modification and that their ultrasonic vocalizations are innate. Here we investigated the mouse song system and discovered that it includes a motor cortex region active during singing, that projects directly to brainstem vocal motor neurons and is necessary for keeping song more stereotyped and on pitch. We also discovered that male mice depend on auditory feedback to maintain some ultrasonic song features, and that sub-strains with differences in their songs can match each other''s pitch when cross-housed under competitive social conditions. We conclude that male mice have some limited vocal modification abilities with at least some neuroanatomical features thought to be unique to humans and song-learning birds. To explain our findings, we propose a continuum hypothesis of vocal learning.     

In reference to phonation larynx fixation: computer graphic record

The vocal apparatus serves phonation. It represents a biocybernetic self-regulating system, disposing of a feedback network of the central nervous system. The larynx is a self-induced vibrating system. The larynx, functioning as the phonation apparatus of the vocal apparatus, is a source of human voice. In every individual its frequency range corresponds to about eight semitones in speech and about two octaves of the so-called chest register in singing, denoted also as a thoracic or modal voice. This is followed by one more octave of the so-called cranial register or falsetto voice. We were interested in changes of the larynx positions at intonation in the fundamental singing registers, both modal and falsetto, in professional male singers. At our disposal were 11 professional male singers. We investigated changes in the position of the laryngeal structures simultaneously with the aid of an X-ray apparatus, the acoustic and mechanical signals registered by means of the B & K 4369 acceleration recorder. It has been found that at phonation with the modal voice a change in the position of the laryngeal structures takes place in two different ways, whereas the larynx movements at falsetto remain the same. It has been suggested that a complex fixation apparatus participates in the phonation larynx movements. Of the same complex character are also the problems connected with the examination of the entire vocal apparatus. For the purpose of compiling the present pieces of knowledge in the field of human voice studies, we have made the most advantageous use of the presently most complex system Authorware for the production of some interactive multimedial programmes on personal computers.     

Bird speech perception and vocal production: a comparison with humans

Research into speech perception by nonhuman animals can be crucially informative in assessing whether specific perceptual phenomena in humans have evolved to decode speech, or reflect more general traits. Birds share with humans not only the capacity to use complex vocalizations for communication but also many characteristics of its underlying developmental and mechanistic processes; thus, birds are a particularly interesting group for comparative study. This review first discusses commonalities between birds and humans in perception of speech sounds. Several psychoacoustic studies have shown striking parallels in seemingly speech-specific perceptual phenomena, such as categorical perception of voice-onset-time variation, categorization of consonants that lack phonetic invariance, and compensation for coarticulation. Such findings are often regarded as evidence for the idea that the objects of human speech perception are auditory or acoustic events rather than articulations. Next, I highlight recent research on the production side of avian communication that has revealed the existence of vocal tract filtering and articulation in bird species-specific vocalization, which has traditionally been considered a hallmark of human speech production. Together, findings in birds show that many of characteristics of human speech perception are not uniquely human but also that a comparative approach to the question of what are the objects of perception--articulatory or auditory events--requires careful consideration of species-specific vocal production mechanisms.     

The ontogeny of cranial base angulation in humans and chimpanzees and its implications for reconstructing pharyngeal dimensions

This paper examines differences in the processes by which the cranial base flexes in humans and extends in chimpanzees. In addition, we test the extent to which one can use comparisons of cranial base angles in humans and non-human primates to predict vocal tract dimensions. Four internal cranial base angles and one external cranial base angle were measured in a longitudinal sample of Homo sapiens and a cross-sectional sample of Pan troglodytes. These data show that the processes of cranial base angulation differ substantially in these species. While the human cranial base flexes postnatally in a rapid growth trajectory that is complete by two years, the cranial base in P. troglodytes extends postnatally in a more prolonged skeletal growth trajectory. These comparisons also demonstrate that the rate of cranial base angulation is comparable for different measures, but that angles which incorporate different anterior cranial base measurements correlate poorly. We also examined ontogenetic relationships between internal and external cranial base angles and vocal tract growth in humans to test the hypothesis that cranial base angulation influences pharyngeal dimensions and can, therefore, be used to estimate vocal tract proportions in fossil hominids. Our results indicate that internal and external cranial base angles are independent of the horizontal and vertical dimensions of the vocal tract. Instead, a combination of mandibular and palatal landmarks can be used to predict dimensions of the vocal tract in H. sapiens. The developmental contrasts in cranial base angulation between humans and non-human primates may have important implications for testing hypotheses about the relationship between cranial base flexion and other craniofacial dimensions in hominid evolution.     

Elasticity and stress relaxation of a very small vocal fold

Across mammals many vocal sounds are produced by airflow induced vocal fold oscillation. We tested the hypothesis that stress-strain and stress-relaxation behavior of rat vocal folds can be used to predict the fundamental frequency range of the species' vocal repertoire. In a first approximation vocal fold oscillation has been modeled by the string model but it is not known whether this concept equally applies to large and small species. The shorter the vocal fold, the more the ideal string law may underestimate normal mode frequencies. To accommodate the very small size of the tissue specimen, a custom-built miniaturized tensile test apparatus was developed. Tissue properties of 6 male rat vocal folds were measured. Rat vocal folds demonstrated the typical linear stress-strain behavior in the low strain region and an exponential stress response at strains larger than about 40%. Approximating the rat's vocal fold oscillation with the string model suggests that fundamental frequencies up to about 6 kHz can be produced, which agrees with frequencies reported for audible rat vocalization. Individual differences and time-dependent changes in the tissue properties parallel findings in other species, and are interpreted as universal features of the laryngeal sound source.     

Predicting Achievable Fundamental Frequency Ranges in Vocalization Across Species

Vocal folds are used as sound sources in various species, but it is unknown how vocal fold morphologies are optimized for different acoustic objectives. Here we identify two main variables affecting range of vocal fold vibration frequency, namely vocal fold elongation and tissue fiber stress. A simple vibrating string model is used to predict fundamental frequency ranges across species of different vocal fold sizes. While average fundamental frequency is predominantly determined by vocal fold length (larynx size), range of fundamental frequency is facilitated by (1) laryngeal muscles that control elongation and by (2) nonlinearity in tissue fiber tension. One adaptation that would increase fundamental frequency range is greater freedom in joint rotation or gliding of two cartilages (thyroid and cricoid), so that vocal fold length change is maximized. Alternatively, tissue layers can develop to bear a disproportionate fiber tension (i.e., a ligament with high density collagen fibers), increasing the fundamental frequency range and thereby vocal versatility. The range of fundamental frequency across species is thus not simply one-dimensional, but can be conceptualized as the dependent variable in a multi-dimensional morphospace. In humans, this could allow for variations that could be clinically important for voice therapy and vocal fold repair. Alternative solutions could also have importance in vocal training for singing and other highly-skilled vocalizations.     

Humans rely on the same rules to assess emotional valence and intensity in conspecific and dog vocalizations

Humans excel at assessing conspecific emotional valence and intensity, based solely on non-verbal vocal bursts that are also common in other mammals. It is not known, however, whether human listeners rely on similar acoustic cues to assess emotional content in conspecific and heterospecific vocalizations, and which acoustical parameters affect their performance. Here, for the first time, we directly compared the emotional valence and intensity perception of dog and human non-verbal vocalizations. We revealed similar relationships between acoustic features and emotional valence and intensity ratings of human and dog vocalizations: those with shorter call lengths were rated as more positive, whereas those with a higher pitch were rated as more intense. Our findings demonstrate that humans rate conspecific emotional vocalizations along basic acoustic rules, and that they apply similar rules when processing dog vocal expressions. This suggests that humans may utilize similar mental mechanisms for recognizing human and heterospecific vocal emotions.     

Structure, occurrence and functional significance of nonlinear phenomena in sounds of terrestrial mammals

Subharmonics, deterministic chaos, biphonations, sidebands and frequency jumps, known under joining name nonlinear phenomena, represent acoustical appearances that occur in calls of various mammals, from insectivorous to humans. Although the physical basis for appearances of the nonlinear phenomen is known in principle, such aspects as occurrence and functional significance of nonlinear phenomena, are poorly understood. We described here the structural peculiarities of these appearances based on domestic dogs' whines demonstrating all kinds of the nonlinear phenomena. The nonlinear phenomena result directly from the work of mammalian vocal apparatus--lunges, vocal folds, and vocal tract, which are responsible for its inherent functional characteristics. The mammalian vocal folds represent a system of two coupled oscillators functioning in different vibratory regimes depending on degree of synchronization in their vibrations and occurrence of coupling between the vocal folds. This functioning does not need in direct neural control for turning on the complex regimes of vocal folds' vibration and switching from one regime to another. Besides, many mammals possess anatomical structures, such as vocal membranes, pads on vocal folds, or laryngeal air sacs, that are to participate in sound production as additional oscillators extend the range of possibilities for arising of nonlinear phenomena in vocalization. On the basis of published and own data, we provide and overview of the occurrence of nonlinear phenomena in sounds of humans, nonhuman primates, canids, and rodents, and discuss the supposed functional significance of these acoustical appearances in mammalian vocal communication systems. From one side, nonlinear phenomena may be related to various physiological disorders in humans and animals. In such cases, their appearance in calls may be nonadaptive, because they permit conspecifics' to avoid owners of such "ill" voices, and points easy prey to predators. From another side, in some cases the nonlinear phenomena may arise especially for performing of some signal functions in species communication system: to enhance reliability of individual recognition, to transmit information about size of a caller over the large distance, to permit individuals of not great size mimicry acoustically under more larger animal, to introduce variety into monotonous vocal sequences in order to force other group members to pay attention to a caller, and to facilitate distance estimation to a caller and direction of its movement.     

Vocal Production by a Language-Competent Pan paniscus

Human spoken language and nonhuman primate vocalization systems have traditionally been regarded as qualitatively different from one another with respect to their semanticity and the way in which individuals acquire and utilize these signals. However, recent studies of the vocal behaviors of both captive and free-ranging monkeys and apes suggest that this dichotomy may not be unequivocal. We examined the vocalizations produced by a linguistically-competent adult male bonobo (Pan paniscus) named Kanzi. We analyzed his vocalizations during communicative interactions with humans in order to determine whether they vary systematically according to the semantic context in which they are produced. We determined semantic contexts based upon a vocalization's co-occurrence with predefined behavioral correlates. Spectrographic and statistical analyses revealed that acoustic structure is similar among the vocalizations that occurred within a specific semantic context and structural differences are evident between the vocalizations produced in different contexts. The results provide evidence that, during communicative interactions with humans, Kanzi modulates his vocal output on both the temporal and spectral levels.     

Primate vocal communication: a useful tool for understanding human speech and language evolution?

Language is a uniquely human trait, and questions of how and why it evolved have been intriguing scientists for years. Nonhuman primates (primates) are our closest living relatives, and their behavior can be used to estimate the capacities of our extinct ancestors. As humans and many primate species rely on vocalizations as their primary mode of communication, the vocal behavior of primates has been an obvious target for studies investigating the evolutionary roots of human speech and language. By studying the similarities and differences between human and primate vocalizations, comparative research has the potential to clarify the evolutionary processes that shaped human speech and language. This review examines some of the seminal and recent studies that contribute to our knowledge regarding the link between primate calls and human language and speech. We focus on three main aspects of primate vocal behavior: functional reference, call combinations, and vocal learning. Studies in these areas indicate that despite important differences, primate vocal communication exhibits some key features characterizing human language. They also indicate, however, that some critical aspects of speech, such as vocal plasticity, are not shared with our primate cousins. We conclude that comparative research on primate vocal behavior is a very promising tool for deepening our understanding of the evolution of human speech and language, but much is still to be done as many aspects of monkey and ape vocalizations remain largely unexplored.     

Vocal communication as a function of differential rearing experiences inPan paniscus: A preliminary report

There is little evidence of vocal learning in nonhuman primates despite the well-documented abilities found in avian species. We describe the vocal repertoire of five bonobos (Pan paniscus), four of which live in a seminatural environment. The fifth subject, Kanzi, has been reared with humans during the course of language training. The data indicated that the four bonobos living in a seminatural environment exhibit a variety of species-typical vocalizations. In addition to producing all the species-typical vocalization, Kanzi produced four structurally unique vocalizations that were not heard among the other subjects. These data suggest that Kanzi has learned vocalizations that are novel due to his unique rearing experience. Discussion is focused on the flexibility of vocal communication and vocal comprehension inPan paniscus.     

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.     

Auditory plasticity: vocal output shapes auditory cortex

Studies in humans and songbirds have revealed a close link between vocal output and hearing. Now experiments in marmosets have shown that self-generated vocalizations can modulate the activity of neurons in the auditory cortex and even remodel their response properties.