Nonhuman Primate Vocalizations Research Articles

STRAIGHTMORPH: A Voice Morphing Tool for Research in Voice Communication Sciences

The purpose of this paper is to make easily available to the scientific community an efficient voice morphing tool called STRAIGHTMORPH and provide a short tutorial on its use with examples. STRAIGHTMORPH consists of a set of Matlab functions allowing the generation of high-quality, parametrically-controlled morphs of an arbitrary number of voice samples. A first step consists in extracting an ‘mObject’ for each voice sample, with accurate tracking of the fundamental frequency contour and manual definition of Time and Frequency anchors corresponding across samples to be morphed. The second step consists in parametrically combining the mObjects to generate novel synthetic stimuli, such as gender, identity or emotion continua, or random combinations. Although STRAIGHTMORPH has been designed for human voices it can work well with other types of sounds such as non-human primate vocalizations.

Transient co-singing of offspring and mothers in non-duetting Javan gibbons (Hylobates moloch)

While the vocalizations of non-human primates were thought to be innate, recent studies have revealed highly flexible vocalizations in immatures. This behavior suggests that social influences have an important role in developing vocalizations. Yet not much is known about how non-human primate vocalization develop and how the vocalizations of immature animals differ between sexes. Here, we analyzed 95 cases of co-singing between mothers and offspring out of 240 female songs from three groups of wild Javan gibbon (Hylobates moloch) in Gunung Halimun-Salak National Park, Indonesia, between 2009 and 2021. Hylobates moloch is one of only two gibbon species with pairs that do not duet. Instead, they produce sex-specific solo songs. We found that both offspring female and male H. moloch follow their mothers’ female-specific songs, similar to other duetting gibbon species. Immatures started co-singing with their mothers from 7 months old, but with an average starting age of about 24 months. As female offspring grew older, they co-sung with mothers more often while male offspring did not. After 7 years of age, both sexes stopped co-singing with their mothers and started singing alone, following their own sex-specific vocalizations. We did not find any relation between male offspring co-singing and territorial functions (e.g., co-singing more during intergroup encounters or closer to home range borders). Our results suggest that mothers’ songs may trigger male offspring and females to practice singing, but not specifically for males to defend territories. We highlight that despite the absence of duets, H. moloch develop their vocalizations from early infancy and throughout their maturation while co-singing with mothers. However, the level of co-singing varies depending on the sexes. Our study is the first to elucidate the sex-specific trajectories of vocal development in H. moloch across years, indicating that offspring in non-duetting gibbons co-sing with mothers like in duetting species.

Rhythm May Be Key to Linking Language and Cognition in Young Infants: Evidence From Machine Learning.

Rhythm is key to language acquisition. Across languages, rhythmic features highlight fundamental linguistic elements of the sound stream and structural relations among them. A sensitivity to rhythmic features, which begins in utero, is evident at birth. What is less clear is whether rhythm supports infants' earliest links between language and cognition. Prior evidence has documented that for infants as young as 3 and 4 months, listening to their native language (English) supports the core cognitive capacity of object categorization. This precocious link is initially part of a broader template: listening to a non-native language from the same rhythmic class as (e.g., German, but not Cantonese) and to vocalizations of non-human primates (e.g., lemur, Eulemur macaco flavifrons, but not birds e.g., zebra-finches, Taeniopygia guttata) provide English-acquiring infants the same cognitive advantage as does listening to their native language. Here, we implement a machine-learning (ML) approach to ask whether there are acoustic properties, available on the surface of these vocalizations, that permit infants' to identify which vocalizations are candidate links to cognition. We provided the model with a robust sample of vocalizations that, from the vantage point of English-acquiring 4-month-olds, either support object categorization (English, German, lemur vocalizations) or fail to do so (Cantonese, zebra-finch vocalizations). We assess (a) whether supervised ML classification models can distinguish those vocalizations that support cognition from those that do not, and (b) which class(es) of acoustic features (including rhythmic, spectral envelope, and pitch features) best support that classification. Our analysis reveals that principal components derived from rhythm-relevant acoustic features were among the most robust in supporting the classification. Classifications performed using temporal envelope components were also robust. These new findings provide in principle evidence that infants' earliest links between vocalizations and cognition may be subserved by their perceptual sensitivity to rhythmic and spectral elements available on the surface of these vocalizations, and that these may guide infants' identification of candidate links to cognition.

The first biolinguist?

Summary In 1930s Germany, Georg Schwidetzky (1875–1952) produced several works attempting to derive modern human languages by reconstruction from the vocalizations of non-human primates. This work was suppressed by other biologists under the Third Reich, not just because both the biology and the linguistics were ridiculously bad, but because Schwidetzky’s views on the origin of races were in conflict with Nazi ideology. While almost comically wrong-headed, there are nonetheless a few parallels between this project and some modern thought about the evolution of language. On the one hand, Schwidetzky stressed the need to think about the evolution of human language in terms of the biological evolution of our species, a branch of Naturwissenschaft, and not a purely humanistic activity, Geisteswissenschaft, as opinion among German linguists of the time saw it. Indeed, he was probably the first to characterize his agenda as the development of Biolinguistik. On the other hand, his attempt to maintain continuity between human language and the communicative vocalizations of non-humans fails to take into account the unique, species-specific character of human language.

Developmental changes in auditory-evoked neural activity underlie infants' links between language and cognition.

The power and precision with which humans link language to cognition is unique to our species. By 3-4months of age, infants have already established this link: simply listening to human language facilitates infants' success in fundamental cognitive processes. Initially, this link to cognition is also engaged by a broader set of acoustic stimuli, including non-human primate vocalizations (but not other sounds, like backwards speech). But by 6months, non-human primate vocalizations no longer confer this cognitive advantage that persists for speech. What remains unknown is the mechanism by which these sounds influence infant cognition, and how this initially broader set of privileged sounds narrows to only human speech between 4 and 6months. Here, we recorded 4- and 6-month-olds' EEG responses to acoustic stimuli whose behavioral effects on infant object categorization have been previously established: infant-directed speech, backwards speech, and non-human primate vocalizations. We document that by 6months, infants' 4-9Hz neural activity is modulated in response to infant-directed speech and non-human primate vocalizations (the two stimuli that initially support categorization), but that 4-9Hz neural activity is not modulated at either age by backward speech (an acoustic stimulus that doesn't support categorization at either age). These results advance the prior behavioral evidence to suggest that by 6months, speech and non-human primate vocalizations elicit distinct changes in infants' cognitive state, influencing performance on foundational cognitive tasks such as object categorization.

Birdsong fails to support object categorization in human infants.

Recent evidence reveals a precocious link between language and cognition in human infants: listening to their native language supports infants’ core cognitive processes, including object categorization, and does so in a way that other acoustic signals (e.g., time-reversed speech; sine-wave tone sequences) do not. Moreover, language is not the only signal that confers this cognitive advantage: listening to vocalizations of non-human primates also supports object categorization in 3- and 4-month-olds. Here, we move beyond primate vocalizations to clarify the breadth of acoustic signals that promote infant cognition. We ask whether listening to birdsong, another naturally produced animal vocalization, also supports object categorization in 3- and 4-month-old infants. We report that listening to zebra finch song failed to confer a cognitive advantage. This outcome brings us closer to identifying a boundary condition on the range of non-linguistic acoustic signals that initially support infant cognition.

Vocal convergence in a multi-level primate society: insights into the evolution of vocal learning.

The extent to which nonhuman primate vocalizations are amenable to modification through experience is relevant for understanding the substrate from which human speech evolved. We examined the vocal behaviour of Guinea baboons, Papio papio, ranging in the Niokolo Koba National Park in Senegal. Guinea baboons live in a multi-level society, with units nested within parties nested within gangs. We investigated whether the acoustic structure of grunts of 27 male baboons of two gangs varied with party/gang membership and genetic relatedness. Males in this species are philopatric, resulting in increased male relatedness within gangs and parties. Grunts of males that were members of the same social levels were more similar than those of males in different social levels (N = 351 dyads for comparison within and between gangs, and N = 169 dyads within and between parties), but the effect sizes were small. Yet, acoustic similarity did not correlate with genetic relatedness, suggesting that higher amounts of social interactions rather than genetic relatedness promote the observed vocal convergence. We consider this convergence a result of sensory–motor integration and suggest this to be an implicit form of vocal learning shared with humans, in contrast to the goal-directed and intentional explicit form of vocal learning unique to human speech acquisition.

Theta Synchronization of Phonatory and Articulatory Systems in Marmoset Monkey Vocal Production

Human speech shares a 3-8-Hz theta rhythm across all languages [1-3]. According to the frame/content theory of speech evolution, this rhythm corresponds to syllabic rates derived from natural mandibular-associated oscillations [4]. The underlying pattern originates from oscillatory movements of articulatory muscles [4, 5] tightly linked to periodic vocal fold vibrations [4, 6, 7]. Such phono-articulatory rhythms have been proposed as one of the crucial preadaptations for human speech evolution [3, 8, 9]. However, the evolutionary link in phono-articulatory rhythmicity between vertebrate vocalization and human speech remains unclear. From the phonatory perspective, theta oscillations might be phylogenetically preserved throughout all vertebrate clades [10-12]. From the articulatory perspective, theta oscillations are present in non-vocal lip smacking [1, 13, 14], teeth chattering [15], vocal lip smacking [16], and clicks and faux-speech [17] in non-human primates, potential evolutionary precursors for speech rhythmicity [1, 13]. Notably, a universal phono-articulatory rhythmicity similar to that in human speech is considered to be absent in non-human primate vocalizations, typically produced with sound modulations lacking concomitant articulatory movements [1, 9, 18]. Here, we challenge this view by investigating the coupling of phonatory and articulatory systems in marmoset vocalizations. Using quantitative measures of acoustic call structure, e.g., amplitude envelope, and call-associated articulatory movements, i.e., inter-lip distance, we show that marmosets display speech-like bi-motor rhythmicity. These oscillations are synchronized and phase locked at theta rhythms. Our findings suggest that oscillatory rhythms underlying speech production evolved early in the primate lineage, identifying marmosets as a suitable animal model to decipher the evolutionary and neural basis of coupled phono-articulatory movements.

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?'

Infants\u2019 advances in speech perception shape their earliest links between language and cognition

The power of human language derives not only from the precision of its signal or the complexity of its grammar, but also from its links to cognition. Infants as young as 3 months have begun to link language and core cognitive capacities. At 3 and 4 months, this link is not exclusive to human language: listening to vocalizations of nonhuman primates also supports infant cognition. By 6 months, infants have tuned this link to human speech alone. Here we provide evidence that infants’ increasing precision in speech perception shapes which signals they will link to cognition. Infants listening to German, a nonnative language that shares key rhythmic and prosodic properties with their own native language (English), successfully formed object categories. In contrast, those listening to Cantonese, a language that differs considerably in these suprasegmental properties, failed. This provides the first evidence that infants’ increasingly precise perceptual tuning to the sounds of their native language sets constraints on the range of human languages they will link to cognition: infants begin to specify which human languages they will link to core cognitive capacities even before they sever the link between nonhuman primate vocalizations and cognition.

Baboon vocal repertoires and the evolution of primate vocal diversity

A remarkable and derived trait of humans is the faculty for language, and considerable research effort has been devoted to understanding the evolution of speech. In contrast to spoken language, which constitutes a (learned) symbolic communication system, the acoustic structure of nonhuman primate vocalizations is largely genetically fixed. Yet, appreciable differences between different genera and species may exist. Environmental conditions, sexual selection, and characteristics of the social system have been invoked to explain these differences. Here, we studied the acoustic variation of call types and vocal repertoires in the genus Papio. Because the genus comprises both stable groups as well as multi-level societies, and reveals striking variation in the degree of aggressiveness from south to north, it constitutes a promising model to assess the link between social system characteristics and vocal communication. We found that, the vocal repertoires of the different species were composed of the same general call types. A quantitative analysis of the acoustic features of the grunts and loud calls of chacma (Papio ursinus), olive (P. anubis), and Guinea (P. papio) baboons showed subtle acoustic differences within call types, however. Social system characteristics did not map onto acoustic variation. We found no correlation between the structure of grunts and geographic distance; the same was true for female loud calls. Only for male loud calls from three populations, call structure varied with geographic distance. Our findings corroborate the view that the structure of nonhuman primate vocalizations is highly conserved, despite the differences in social systems. Apparently, variation in rate and intensity of occurrence of signals, probably due to different behavioral dispositions in species, are sufficient to allow for plasticity at the level of the social relationships, mating patterns, and social organization.

Supervised and unsupervised machine learning approaches to classifying chimpanzee vocalizations

Quantitative tools for classifying vocal repertoires have been constantly evolving with developments in machine learning and speech recognition research as well as increasing computing power. There are two main methodological considerations in classifying vocalizations: (i) choosing the classification technique and (ii) choosing the features for classification. Current state-of-the-art classification techniques are artificial neural networks (ANNs), support vector machines (SVMs), and ensemble methods like random forests (RFs). Current state-of-the-art features from speech recognition research include mel frequency cepstral coefficients (MFCCs). Bioacoustics researchers have applied these tools to problems including individual-, species-, and call-type identification, and vocal repertoire classification. However, researchers studying non-human primate vocalizations have only recently started adopting these approaches and none have applied them to study chimpanzee vocalizations. Here, we analyze vocalizations recorded in Gombe National Park, Tanzania. First, we use supervised classification techniques (ANNs, SVMs, and RFs) that involve training the models based on predefined call-types to evaluate the classification accuracy. Second, we use unsupervised techniques (that do not require prior knowledge of call-types), namely, K-means clustering, and self-organizing neural networks to identify discrete call types. We discuss the results from both supervised and unsupervised techniques and their strengths over traditional methods.

Non-invasive documentation of primate voice production using electroglottography

Electroglottography (EGG) is a low-cost, non-invasive method for documenting laryngeal sound production during vocalization. The EGG signal represents relative vocal-fold contact area and thus delivers physiological evidence of vocal-fold vibration. While the method has received much attention in human voice research over the last five decades, it has seen very little application in other mammals. Here, we give a concise overview of mammalian vocal production principles. We explain how mammalian voice production physiology and the dynamics of vocal-fold vibration can be documented qualitatively and quantitatively with EGG, and we summarize and discuss key issues from research with humans. Finally, we review the limited number of studies applying EGG to non-human mammals, both in vivo and in vitro. The potential of EGG for non-invasive assessment of non-human primate vocalization is demonstrated with novel in vivo data of Cebus albifrons and Ateles chamek vocalization. These examples illustrate the great potential of EGG as a new minimally invasive tool in primate research, which can provide important insight into the ‘black box’ that is vocal production. A better understanding of vocal-fold vibration across a range of taxa can provide us with a deeper understanding of several important elements of speech evolution, such as the universality of vocal production mechanisms, the independence of source and filter, the evolution of vocal control, and the relevance of non-linear phenomena.

Experience is Instrumental in Tuning a Link Between Language and Cognition: Evidence from 6- to 7- Month-Old Infants' Object Categorization.

At birth, infants not only prefer listening to human vocalizations, but also have begun to link these vocalizations to cognition: For infants as young as three months of age, listening to human language supports object categorization, a core cognitive capacity. This precocious link is initially broad: At 3 and 4 months, vocalizations of both humans and nonhuman primates support categorization. But by 6 months, infants have narrowed the link: Only human vocalizations support object categorization. Here we ask what guides infants as they tune their initially broad link to a more precise one, engaged only by the vocalizations of our species. Across three studies, we use a novel exposure paradigm to examine the effects of experience. We document that merely exposing infants to nonhuman primate vocalizations enables infants to preserve the early-established link between this signal and categorization. In contrast, exposing infants to backward speech - a signal that fails to support categorization at any age - offers no such advantage. Our findings reveal the power of early experience as infants specify which signals, from an initially broad set, they will continue to link to cognition.

JoVE Monthly Highlights: April 2017

Here's a look at what's coming up in the April 2017 issue of JoVE: The World's Premier Video Journal The plight of the honeybee holds our first spotlight this month. Pesticides brought back to colonies by workers foraging on contaminated flowers can be spread throughout honeybee colonies, severely impacting health of larvae and adults, and potentially causing colony collapse. In JoVE Environment, our Authors describe feeding methods in which an insect growth regulator and commonly used pesticide - PPN - is fed both to individual honeybees and an entire colony, in a manner that can be applied to any potentially harmful chemicals or pathogens. A technique enabling a better understanding of the challenges facing these critical pollinators leaves us buzzing. From food-producing pollinators to clean water...in JoVE Bioengineering this month, our Authors present methods to prepare low-cost, efficient membranes for water purification. Here, zwitterionic hydrogels are produced using SBMA* crosslinked to polyethylene glycol diacrylate to improve mechanical strength. When impregnated into a highly porous hydrophobic support, the resultant tightly bound layers prevent antifouling of the membranes by physically preventing attachment to the surface. These properties combined allow for production of energy efficient and long lasting filters to meet increasing demand for clean water. Something we can all toast to, cheers! In JoVE Behavior, our Authors demonstrate a procedure of exposure manipulation involving sorting novel and familiar objects paired with an acoustic signal, to reveal the powerful shaping role of experience in recognizing human language. At 3-4 months infants broadly recognize both human and nonhuman primate vocalizations as cues to support object categorization, but by 6-to 7-months only human vocalizations are utilized. This method shows that merely exposing infants to nonhuman primate vocalizations can preserve this early-established link, whereas the same effect is not observed when the child is exposed to backwards speech. Finally, as the first buds of spring emerge, our last video highlight this month gives a fascinating glimpse into the private life of plants. In JoVE Developmental Biology, our Author uses confocal microscopy to show how the intricate inflorescences of the Arabidopsis plant develop in real time. Moreover, the demonstrated procedure allows expression of multiple genes to be visualized at once, aiding in the elucidation of the complex genetic networks, which unravel simultaneously to specify the identities of the different floral organs. Blooming marvelous! You've just had a sneak peek of the April 2017 issue of JoVE. Visit the website to see the full-length articles, plus many more, in JoVE: The World's Premier Video Journal.

Gestural development of chimpanzees in the wild: the impact of interactional experience

To understand the complexity involved in animal signalling, studies have mainly focused on repertoire size and information conveyed in vocalizations of birds and nonhuman primates. However, recent studies on gestural abilities of nonhuman primates have shown that we also need a detailed understanding of other communicative modalities and underlying cognitive skills to grasp this phenomenon in detail. Here, we thus examined gestural signalling of chimpanzees, Pan troglodytes, living in two communities in the wild (Kanyawara, Uganda; Tai South, Cote d'Ivoire) with a special focus on the influence of the social environment on signal development. Specifically, we investigated to what extent specific social factors, namely behavioural context, interaction rates and maternal proximity, affect gestural production (i.e. gesture frequency, sequences and repertoire size). We used a combination of video recordings and focal scans obtained from 11 infants aged between 9 and 69 months during 1145 h of observation throughout two consecutive field periods. Overall, we found that social play was the context in which the highest number of gestures occurred. While gesture frequency and repertoire size increased with higher interaction rates with nonmaternal conspecifics and the number of previous interaction partners, no effect was found for interaction rates with mothers. Our results thus imply that infants of social mothers may have a head start in life. Moreover, we provide hitherto undocumented evidence for sex differences in gestural signalling, which may reflect the differential importance of early socialization for chimpanzee males and females. Gestural development thus relies heavily on interactional experiences with conspecifics, which adds support for gestural acquisition via the learning mechanism of ‘social negotiation’ in great apes.

Primate vocal production and the riddle of language evolution

Trying to uncover the roots of human speech and language has been the premier motivation to study the signalling behaviour of nonhuman primates for several decades. Focussing on the question of whether we find evidence for linguistic reference in the production of nonhuman primate vocalizations, I will first discuss how the criteria used to diagnose referential signalling have changed over time, and will then turn to the paradigmatic case of semantic communication in animals, the alarm calls of vervet monkeys, Chlorocebus pygerythrus. A recent in-depth analysis of the original material revealed that, while the alarm calls could be well distinguished, calls of similar structure were also used in within- and between-group aggression. This finding is difficult to reconcile with the idea that calls denote objects in the environment. Furthermore, nonhuman primates show only minimal signs of vocal production learning, one key prerequisite for conventionalized and symbolic communication. In addition, the structure of calls in different populations or closely related species is highly conserved. In conclusion, any continuity between nonhuman primate and human communication appears to be found at the level of the processing of signals. Why and how the ancestors of our own species one day began to talk to each other continues to be an enigma. Future research should focus on changes in the neural structure supporting volitional control over vocalizations, the gene networks associated with vocal production, and the developmental processes involved in the integration of production and perception of vocalizations.

Listening to the calls of the wild: The role of experience in linking language and cognition in young infants

Well before they understand their first words, infants have begun to link language and cognition. This link is initially broad: At 3months, listening to both human and nonhuman primate vocalizations supports infants’ object categorization, a building block of cognition. But by 6months, the link has narrowed: Only human vocalizations support categorization. What mechanisms underlie this rapid tuning process? Here, we document the crucial role of infants’ experience as infants tune this link to cognition. Merely exposing infants to nonhuman primate vocalizations permits them to preserve, rather than sever, the link between these signals and categorization. Exposing infants to backward speech—a signal that fails to support categorization in the first year of life—does not have this advantage. This new evidence illuminates the central role of early experience as infants specify which signals, from an initially broad set, they will continue to link to core cognitive capacities.

Noise-Induced Frequency Modifications of Tamarin Vocalizations: Implications for Noise Compensation in Nonhuman Primates.

Previous research suggests that nonhuman primates have limited flexibility in the frequency content of their vocalizations, particularly when compared to human speech. Consistent with this notion, several nonhuman primate species have demonstrated noise-induced changes in call amplitude and duration, with no evidence of changes to spectral content. This experiment used broad- and narrow-band noise playbacks to investigate the vocal control of two call types produced by cotton-top tamarins (Saguinus Oedipus). In ‘combination long calls’ (CLCs), peak fundamental frequency and the distribution of energy between low and high frequency harmonics (spectral tilt) changed in response to increased noise amplitude and bandwidth. In chirps, peak and maximum components of the fundamental frequency increased with increasing noise level, with no changes to spectral tilt. Other modifications included the Lombard effect and increases in chirp duration. These results provide the first evidence for noise-induced frequency changes in nonhuman primate vocalizations and suggest that future investigations of vocal plasticity in primates should include spectral parameters.

Modulation-frequency-specific adaptation in awake auditory cortex.

Amplitude modulations are fundamental features of natural signals, including human speech and nonhuman primate vocalizations. Because natural signals frequently occur in the context of other competing signals, we used a forward-masking paradigm to investigate how the modulation context of a prior signal affects cortical responses to subsequent modulated sounds. Psychophysical "modulation masking," in which the presentation of a modulated "masker" signal elevates the threshold for detecting the modulation of a subsequent stimulus, has been interpreted as evidence of a central modulation filterbank and modeled accordingly. Whether cortical modulation tuning is compatible with such models remains unknown. By recording responses to pairs of sinusoidally amplitude modulated (SAM) tones in the auditory cortex of awake squirrel monkeys, we show that the prior presentation of the SAM masker elicited persistent and tuned suppression of the firing rate to subsequent SAM signals. Population averages of these effects are compatible with adaptation in broadly tuned modulation channels. In contrast, modulation context had little effect on the synchrony of the cortical representation of the second SAM stimuli and the tuning of such effects did not match that observed for firing rate. Our results suggest that, although the temporal representation of modulated signals is more robust to changes in stimulus context than representations based on average firing rate, this representation is not fully exploited and psychophysical modulation masking more closely mirrors physiological rate suppression and that rate tuning for a given stimulus feature in a given neuron's signal pathway appears sufficient to engender context-sensitive cortical adaptation.