Nonhuman Primate Vocalizations Research Articles

Very young infants' responses to human and nonhuman primate vocalizations.

Recent evidence from very young human infants' responses to human and nonhuman primate vocalizations offers new insights - and brings new questions - to the forefront for those who seek to integrate primate-general and human-specific mechanisms of acoustic communication with theories of language acquisition.

Single neurons in monkey prefrontal cortex encode volitional initiation of vocalizations

Broca's area in the ventrolateral prefrontal cortex (vlPFC) has a crucial role in human volitional speech production; damage to this area causes severe impairment of speech production. Lesions in PFC of monkeys, however, have only mild effects on spontaneous vocal behaviour. Non-human primate vocalizations are thus believed to constitute affective utterances processed by a subcortical network. Here in contrast to this assumption, we show that rhesus monkeys can control their vocalizations in a goal-directed way. During single-cell recordings in the vlPFC of monkeys trained to vocalize in response to visual cues, we find call-related neurons that specifically predict the preparation of instructed vocalizations. The activity of many call-related neurons before vocal output correlates with call parameters of instructed vocalizations. These findings suggest a cardinal role of the monkey homologue of Broca's area in vocal planning and call initiation, a putative phylogenetic precursor in non-human primates for speech control in linguistic humans.

Nonhuman primate vocalizations support categorization in very young human infants.

Language is a signature of our species and our primary conduit for conveying the contents of our minds. The power of language derives not only from the exquisite detail of the signal itself but also from its intricate link to human cognition. To acquire a language, infants must identify which signals are part of their language and discover how these signals are linked to meaning. At birth, infants prefer listening to vocalizations of human and nonhuman primates; within 3 mo, this initially broad listening preference is tuned specifically to human vocalizations. Moreover, even at this early developmental point, human vocalizations evoke more than listening preferences alone: they engender in infants a heightened focus on the objects in their visual environment and promote the formation of object categories, a fundamental cognitive capacity. Here, we illuminate the developmental origin of this early link between human vocalizations and cognition. We document that this link emerges from a broad biological template that initially encompasses vocalizations of human and nonhuman primates (but not backward speech) and that within 6 mo this link to cognition is tuned specifically to human vocalizations. At 3 and 4 mo, nonhuman primate vocalizations promote object categorization, mirroring precisely the advantages conferred by human vocalizations, but by 6 mo, nonhuman primate vocalizations no longer exert this advantageous effect. This striking developmental shift illuminates a path of specialization that supports infants as they forge the foundational links between human language and the core cognitive processes that will serve as the foundations of meaning.

The use of Artificial Neural Networks to classify primate vocalizations: a pilot study on black lemurs

The identification of the vocal repertoire of a species represents a crucial prerequisite for a correct interpretation of animal behavior. Artificial Neural Networks (ANNs) have been widely used in behavioral sciences, and today are considered a valuable classification tool for reducing the level of subjectivity and allowing replicable results across different studies. However, to date, no studies have applied this tool to nonhuman primate vocalizations. Here, we apply for the first time ANNs, to discriminate the vocal repertoire in a primate species, Eulemur macaco macaco. We designed an automatic procedure to extract both spectral and temporal features from signals, and performed a comparative analysis between a supervised Multilayer Perceptron and two statistical approaches commonly used in primatology (Discriminant Function Analysis and Cluster Analysis), in order to explore pros and cons of these methods in bioacoustic classification. Our results show that ANNs were able to recognize all seven vocal categories previously described (92.5-95.6%) and perform better than either statistical analysis (76.1-88.4%). The results show that ANNs can provide an effective and robust method for automatic classification also in primates, suggesting that neural models can represent a valuable tool to contribute to a better understanding of primate vocal communication. The use of neural networks to identify primate vocalizations and the further development of this approach in studying primate communication are discussed.

Primate Vocalization, Gesture, and the Evolution of Human Language

The performance of language is multimodal, not confined to speech. Review of monkey and ape communication demonstrates greater flexibility in the use of hands and body than for vocalization. Nonetheless, the gestural repertoire of any group of nonhuman primates is small compared with the vocabulary of any human language and thus, presumably, of the transitional form called protolanguage. We argue that it was the coupling of gestural communication with enhanced capacities for imitation that made possible the emergence of protosign to provide essential scaffolding for protospeech in the evolution of protolanguage. Similarly, we argue against a direct evolutionary path from nonhuman primate vocalization to human speech. The analysis refines aspects of the mirror system hypothesis on the role of the primate brain's mirror system for manual action in evolution of the human language-ready brain.

Do age- and sex-related variations reliably reflect body size in non-human primate vocalizations? A review

In vocal communication, the mechanisms of sound production are well understood. The length of the vocal folds determines the minimum fundamental frequency, while the size and the shape of the vocal tract affect its filtering characteristics and hence, the resonant frequencies. Both measures-vocal fold length and vocal tract length-are related to body size and therefore, acoustic features are expected to vary with body size. Because direct measures of body size are difficult to obtain from free-ranging animals, age and sex have often been used as proxies. We surveyed studies which included direct measures of size or weight, and also studies in which only age and/or sex differences were examined. The main purpose was to examine whether age- and sex-related variations in acoustic features meet the predictions generated from our knowledge about sound production. Our survey revealed that compared to smaller animals, larger animals utter longer calls, with a lower fundamental frequency, with smaller formant dispersion, and with the energy concentrated in lower frequencies. Age and sex reliably reflect the influence of body size on acoustic features when gross size differences are examined. However, within age- and sex classes, this relationship may break down. In addition to body size, other factors such as internal state or social context may also influence the structure of vocal signals and highlight the richness of information in calls that is potentially available to listeners.

Language Evolution: What Do Chimpanzees Have to Say?

Although unique in important ways, language shares some properties with other animal communication systems. Comparative analyses of nonhuman primate vocalizations can shed light on the evolution of language's special features.

Human laughter, social play, and play vocalizations of non-human primates: an evolutionary approach

It has been hypothesized that the evolutionary origin of human laughter lies in the facial play signals of non-human primates. Recent studies dealing with human laughter have stressed the importance of the acoustic component of this nonverbal behaviour. In this study, we analysed the occurrence and some acoustic parameters, such as interval durations and fundamental frequency, of Barbary macaque and chimpanzee play vocalizations and human laughter during tickling. Play vocalizations occurred most often during play with close bodily contact, i.e. wrestling and tickling. In both Barbary macaques and chimpanzees, they were serially organized and had a high intra-bout variability in their acoustic parameters. These are characteristic features of human laughter which are crucial for deciding whether a given utterance will be classified as laughter in humans. Besides intra-bout variability, there was substantial intraindividual variability which was as high or higher than the interindividual variability in all three species. Interval durations of Barbary macaque and chimpanzee play vocalizations and human laughter during tickling lay in a similar range. These results provide further evidence for the hypothesis that human laughter evolved from a play signal of non-human primates and raise questions about the importance of and the relationship between facial and vocal play signals in the evolution of human laughter.

Aspects of human language: Where motherese?

Human language is a peculiar primate communication tool because of its large neocortical substrate, comparable to the structural substrates of cognitive systems. Although monkey calls and human language rely on different structures, neural substrate for human language emotional coding, prosody, and intonation is already part of nonhuman primate vocalization circuitry. Motherese could be an aspect of language at the crossing or at the origin of communicative and cognitive content.

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.

The evolution of human speech: the role of enhanced breathing control.

Many cognitive and physical features must have undergone change for the evolution of fully modern human language. One neglected aspect is the evolution of increased breathing control. Evidence presented herein shows that modern humans and Neanderthals have an expanded thoracic vertebral canal compared with australopithecines and Homo ergaster, who had canals of the same relative size as extant nonhuman primates. Based on previously published analyses, these results demonstrate that there was an increase in thoracic innervation during human evolution. Possible explanations for this increase include postural control for bipedalism, increased difficulty of parturition, respiration for endurance running, an aquatic phase, and choking avoidance. These can all be ruled out, either because of their evolutionary timing, or because they are insufficiently demanding neurologically. The remaining possible functional cause is increased control of breathing for speech. The main muscles involved in the fine control of human speech breathing are the intercostals and a set of abdominal muscles which are all thoracically innervated. Modifications to quiet breathing are essential for modern human speech, enabling the production of long phrases on single expirations punctuated with quick inspirations at meaningful linguistic breaks. Other linguistically important features affected by variation in subglottal air pressure include emphasis of particular sound units, and control of pitch and intonation. Subtle, complex muscle movements, integrated with cognitive factors, are involved. The vocalizations of nonhuman primates involve markedly less respiratory control. Without sophisticated breath control, early hominids would only have been capable of short, unmodulated utterances, like those of extant nonhuman primates. Fine respiratory control, a necessary component for fully modern language, evolved sometime between 1.6 Mya and 100,000 ya.

Matching of acoustic features during the vocal exchange of coo calls by Japanese macaques

A central issue in studies of vocalizations of non-human primates is the extent of their plasticity. Japanese macaques,Macaca fuscata, frequently utter coo calls and exchange these calls with other group members to maintain contact vocally. I conducted a playback experiment to examine whether monkeys that respond vocally match the acoustic features of their reply to those of the calls they have heard. Six to eight stimulus calls with different acoustic properties in terms of fundamental frequency components were played back to each of seven females, in an attempt to elicit replies from the subjects. There were significant positive regressions of the frequency range of stimuli with that of the replies. Japanese macaques thus matched some of the acoustic features of their replies to those of the preceding calls, suggesting that they might be able to modify the acoustic features of their calls according to the features of the prior calls of another group member.

Indexical cuing in laughter

Laughter is a frequently produced yet poorly understood vocal signal. Despite the lack of basic knowledge regarding this species-typical vocalization, this signal may be advantageous to study as it provides an opportunity to examine indexical cueing in the absence of linguistic content. The source-filter model of vowel production guided acoustic analysis of laughter recorded from experimentally naive subjects as they watched emotion-inducing film clips in a laboratory setting. Subjects were 48 males and 48 females tested either alone or with a same- or opposite-sex friend or stranger. Laugh acoustics were found to vary by gender, talker, and social context. Males produced predominantly unvoiced, ‘‘grunt’’ laughs, whereas female laughter was more variable and included more voiced, long duration ‘‘song’’ laughs. Discriminant function analyses revealed that source and filter-related cues were differentially associated with social context and talker identity. Variability in source-related cues, particularly F0, more successfully discriminated social context, whereas cues related to the vocal tract transfer function better discriminated among individuals. Females, but not males, had significantly higher formant frequencies when tested with opposite-sex strangers. The overall pattern of results is consistent with recent examinations of indexical cuing in human speech and nonhuman primate vocalizations. [Work supported by NIMH.]

Behavioral mechanisms underlying vocal communication in nonhuman primates

In the wild, nonhuman primate vocalizations signal the presence of different predators, provide information about the group’s location and movement, facilitate friendly interactions, and lead to reconciliation between individuals who have recently exchanged aggression. Current research examines the mechanisms that underlie such communication. Playback experiments demonstrate that subjects treat vocalizations as semantic signals, in the sense that they compare signals according to their referents and not just their acoustic properties. Results provide no evidence, however, that subjects recognize one another’s mental states. Calls that provide information about the group’s location or movement are given by baboons only when they themselves are lost; individuals at the group’s center apparently do not call to inform peripheral animals of their location. Calls that lead to reconciliation are best explained by assuming that callers and recipients have learned, through experience, that a vocalization is rarely followed by aggression and often followed by friendly behavior. The inability of animals to recognize what other individuals know, believe, or desire constitutes a fundamental difference between nonhuman primate vocal communication and human language.

Cortical Field Potentials Preceding Vocalization in Monkeys

Field potentials before vocalization were studied with electrodes chronically implanted on the surface and at a 2.0–3.0 mm depth in various cortical areas in three monkeys. Surface-negative, depth-positive (s-N, d-P) slow potentials prior to vocalization were recorded in the premotor (including the Broca's homolog), motor and somatosensory cortices, and the supplementary motor area (SMA). Such premovement potentials were recorded also in the cingulate and prefrontal cortices when a monkey uttered a sound with intense motivation for reward. Cerebellar hemispherectomy on the right side eliminated the s-N, d-P premovement potentials in the motor cortex and in the posterior bank of inferior limb of the arcuate sulcus (homolog of Broca's area) in the left hemisphere. After the operation, the tone came to have less components of different frequencies, and its duration varied much more than before. These facts suggest that the neocortical area homologous to the human speech area takes part in the generation and control of monkey vocalization together with the cerebellum possibly through cerebro-cerebellar interactions. This is against ideas so far proposed on nonhuman primate vocalization, i.e., it is generally considered that animal vocalization differs fundamentally from human speech.

Young children's post tantrum affiliation with their parents

In our database of 331 parental narratives of tantrums had by children 18–60 months old, 29% of the tantrums were followed by child-initiated affiliation with parents. Four variables increased the probability of children's post tantrum affiliation (PTA): age, prolonged screaming, physiological stress, and parent-initiated separation from the child during the tantrum. The age effect may be due to increasing post tantrum persistence of negative affect, to the emergence of shame, guilt, and embarrassment over this developmental period, and/or to increasing cognitive ability, empathic capacity, or socialization. Screaming, which may be analogous to the defensive vocalizations of nonhuman primates, increases PTA when prolonged for 6 min or more. Physiological stress (indicated by autonomic activation or respiratory distress) appears linked to prolonged screaming and may mediate its effects by increasing the child's dysphoria and need for consolation. Separation (parents' departure from the scene of the tantrum or their imposition of a time out) also appears linked to prolonged screaming and may reflect parents' response to an aversive auditory stimulus. There was no evidence that PTA was associated with the presence or degree of physically expressed anger in the tantrum. PTA may be associated with distress during the tantrum. The post conflict reconciliation which occurs in several domains of human social life may be first experienced by children in the aftermath of their tantrums. Aggr. Behav. 23:329–341, 1997. © 1997 Wiley-Liss, Inc.

Young children's post tantrum affiliation with their parents

In our database of 331 parental narratives of tantrums had by children 18-60 months old, 29% of the tantrums were followed by child-initiated affiliation with parents. Four variables increased the probability of children's post tantrum affiliation (PTA): age, prolonged screaming, physiological stress, and parent-initiated separation from the child during the tantrum. The age effect may he due to increasing post tantrum persistence of negative affect, to the emergence of shame, guilt, and embarrassment over this developmental period, and/or to increasing cognitive ability, empathic capacity, or socialization. Screaming, which may be analogous to the defensive vocalizations of nonhuman primates, increases PTA when prolonged for 6 min or more. Physiological stress (indicated by autonomic activation or respiratory distress) appears linked to prolonged screaming and may mediate its effects by increasing the child's dysphoria and need for consolation. Separation (parents' departure from the scene of the tantrum or their imposition of a time out) also appears linked to prolonged screaming and may reflect parents' response to an aversive auditory stimulus. There was no evidence that PTA was associated with the presence or degree of physically expressed anger in the tantrum. PTA may be associated with distress during the tantrum. The post conflict reconciliation which occurs in several domains of human social life may be first experienced by children in the aftermath of their tantrums.

Cortical field potentials preceding vocalization and influences of cerebellar hemispherectomy upon them in monkeys

Field potentials preceding vocalization were recorded with electrodes chronically implanted on the surface and at 2.0–3.0 mm depth in various cortical areas in three monkeys. Surface-negative, depth-positive (s-N, d-P) slow potentials prior to vocalization were recorded in the premotor (including the Broca's homolog), motor and somatosensory cortices in both hemispheres, and the supplementary motor area in the cerebral hemisphere. Such premovement potentials were recorded also in the cingulate and prefrontal cortices when a monkey uttered with intense motivation for reward. Cerebellar hemispherectomy on the right side eliminated the s-N, d-P premovement potentials in the motor cortex and in the posterior bank of inferior limb of the arcuate sulcus (homolog of Broca's area) in the left hemisphere. Vocal tone contained less components in different frequencies, and its duration became more variable than before the operation. These facts suggest that the neocortical area homologous to the human speech area takes part in generation and control of monkey vocalization together with the cerebellum, possibly through cerebro-cerebellar interactions, against ideas so far offered on nonhuman primate vocalization.

The Evolution of Nonhuman Primate Vocalizations: Effects of Phylogeny, Body Weight, and Social Context

E. S. Morton proposed that, in birds and mammals, individuals tend to produce low-frequency atonal vocalizations in highly aggressive situations, whereas they typically produce high-frequency tonal vocalizations during nonaggressive or fearful situations. This hypothesis, referred to as the "motivation-structural (MS) rules," is based on two assumptions: the frequency of a vocalization is negatively correlated with body weight, and large animals are dominant over smaller animals, and thus aggressive vocalizations tend to have a lower pitch than fearful vocalizations. The relationship between body weight and frequency is examined using data on 36 nonhuman primate species representing 23 genera and 474 vocalizations. Results show that there is a statistically significant negative correlation between body weight and frequency: larger species produce relatively lower-pitched vocalizations than smaller species. A test of Morton's MS rules provided overall support for the predicted relationship between motivational state and frequency (i.e., high-frequency calls were produced by fearful individuals, and low-frequency calls were produced by aggressive individuals) but no support for the expected relationship between motivational state and tonality. However, the motivational state-frequency pairing was confounded by the fact that some taxonomic groups (Platyrrhini and Catarrhini) showed a much stronger level of association than other groups (Prosimii and Hominoidea). In summary, therefore, the nonhuman primate data provide only partial support for MS rules. At least three factors may have influenced the outcome of the current test. First, in some species, motivational state may be more closely associated with other acoustic parameters than absolute frequency and tonality. Second, the acoustic structure of nonhuman primate vocalizations is, at least in some cases, more closely associated with an external referent than with the caller's internal state. And third, features of the species-typical habitat have had direct selective effects on signal structure, optimizing for effective propagation through the environment.

Neuroethological approaches to the study of vocal production in nonhuman primates.

The vocalizations of nonhuman primates are potentially important probes for studying the neural and neurochemical substrates of behavior. These studies have focused on one category of vocalization, the isolation call, due to its relatively stereotyped acoustic structure and ease of elicitation and attribution in captive animals. Experimental brain lesions reveal an important role for the thalamic tegmentum and anterior cingulate gyrus in mediating normal acoustic structure and motivation to vocalize, respectively. The amygdala plays a role in determining the development of normal levels of emotional expression, as shown in the effects of neonatal ablations of this limbic structure and its cortical afferents on vocal behavior during development. Neurochemical control of the isolation call arises from several disparate endogenous neurochemical systems, including opiatergic and monoaminergic pathways.