Communication In Nonhuman Primates Research Articles

Frontal cortex activity during the production of diverse social communication calls in marmoset monkeys

Vocal communication is essential for social behaviors in humans and non-human primates. While the frontal cortex is crucial to human speech production, its role in vocal production in non-human primates has long been questioned. It is unclear whether activities in the frontal cortex represent diverse vocal signals used in non-human primate communication. Here we studied single neuron activities and local field potentials (LFP) in the frontal cortex of male marmoset monkeys while the animal engaged in vocal exchanges with conspecifics in a social environment. We found that both single neuron activities and LFP were modulated by the production of each of the four major call types. Moreover, neural activities showed distinct patterns for different call types and theta-band LFP oscillations showed phase-locking to the phrases of twitter calls, suggesting a neural representation of vocalization features. Our results suggest important functions of the marmoset frontal cortex in supporting the production of diverse vocalizations in communication.

Pseudoreplication in Primate Communication Research: 10 Years On

Pseudoreplication is the statistical error of collecting numerous datapoints from a single unit (such as an individual), which are not independent, and applying statistical methods that assume independence of data. Importantly, pseudoreplication increases the chances of Type 1 errors (i.e., false positives), bringing findings and conclusions based on pseudoreplicated analyses into question. Ten years ago, Waller et al. (2013) published a paper highlighting the prevalence of statistical pseudoreplication throughout the nonhuman primate communication literature. In this current study, we examined the literature published since the original publication (between 2009 and 2020; 348 papers) to assess whether pseudoreplication is still as widespread as it was, if it has become more problematic, or if the field is beginning to overcome this issue. We find that there has been a significant decrease in pseudoreplication over the past ten years (38.6% then, compared with 23.0% now). This reduction in pseudoreplication appears to be associated with an increase in the use of multilevel models throughout primatology (which allow for nonindependent data to be nested appropriately). Pseudoreplication was historically more prevalent in research using observational (vs. experimental) methods and those working with wild (vs. captive) primates. However, these biases do not seem to exist in more recent literature with a more comparable likelihood of pseudoreplication seen across the field regardless of methods. Although these current findings relate specifically to primate communication research, we think they will translate broadly across nonhuman communication research, and throughout biology. We continue to emphasise the need to monitor these issues, as although now seen at much lower rates, pseudoreplication is still present and therefore potentially impacting the accuracy of findings.

Context-dependent alarm responses in wild vervet monkeys

The alarm calls of nonhuman primates are occasionally cited as functionally equivalent to lexical word meaning in human language. Recently, however, it has become increasingly unlikely that one-to-one relations between alarm call structures and predator categories are the default, mainly because many call types are produced in multiple contexts, requiring more complex notions of meaning. For example, male vervet monkeys produce the same alarm calls during encounters with terrestrial predators and neighbouring groups, suggesting that recipients require additional information to attribute meaning to the calls. We empirically tested the hypothesis that vervet monkeys take contextual information into account when responding to each other's alarm calls. In playback experiments, we exposed subjects to recordings of male alarm barks during actual intergroup encounters (predator unlikely) or when there was no intergroup encounter (predator likely). Subjects responded more strongly in the no intergroup encounter situations, typically associated with discovering a hiding predator, measured in terms of startle responses, vigilance behaviour and gazing towards the presumed caller. We discuss the significance of using contextual information for meaning attribution in nonhuman primate communication.

Revisiting the human 'interaction engine': comparative approaches to social action coordination.

The evolution of language was likely facilitated by a special predisposition for social interaction, involving a set of communicative and cognitive skills summarized as the ‘interaction engine'. This assemblage seems to emerge early in development, to be found universally across cultures, and to enable participation in sophisticated joint action through the addition of spoken language. Yet, new evidence on social action coordination and communication in nonhuman primates warrants an update of the interaction engine hypothesis, particularly with respect to the evolutionary origins of its specific ingredients. However, one enduring problem for comparative research results from a conceptual gulf between disciplines, rendering it difficult to test concepts derived from human interaction research in nonhuman animals. The goal of this theme issue is to make such concepts accessible for comparative research, to promote a fruitful interdisciplinary debate on social action coordination as a new arena of research, and to enable mutual fertilization between human and nonhuman interaction research. In consequence, we here consider relevant theoretical and empirical research within and beyond this theme issue to revisit the interaction engine's shared, convergently derived and uniquely derived ingredients preceding (or perhaps in the last case, succeeding) human language.This article is part of the theme issue ‘Revisiting the human ‘interaction engine’: comparative approaches to social action coordination’.

Sequence organization and embodied mutual orientations: openings of social interactions between baboons.

Human interactions are organized in sequence, which is a key component of Levinson's 'interaction engine.' Referring back to the field where it originated, conversation analysis, we discuss its relevance within the interaction engine, before moving on to show how sequence organization is actually oriented to not only humans in social interaction, but also to non-human animals. On the basis of video-recorded encounters between baboons (Papio anubis), we study canonical sequences constituting openings and, within them, greetings. Openings are the locus where future interactants adjust to each other to coordinately enter in interaction, thus achieving a common definition of their context, activity, and relationships. The analysis shows that the ways individuals spatially approach each other provide systematic interactional affordances for how the first sequences of actions in the opening are formatted, initiated, and responded to. Adopting sequential multimodal analysis, we demonstrate how participants orient to central features of sequence organization-its sequential implicativeness and the expectations it produces-building on them their interpretations of others' actions, their responsivity, and their mutual understanding of the ongoing course of action as it unfolds. This paves the way for further reflections on the pervasiveness of the interactional engine in human and non-human primate communication. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

Individual variation and plasticity in the infant-directed communication of orang-utan mothers.

Between-individual variation in behavioural expression, such as social responsiveness, has been shown to have important eco-evolutionary consequences. However, most comparative research on non-human primate communication has focused on species- or population-level variation, while among- and within-individual variation has been largely ignored or considered as noise. Here, we apply a behavioural reaction norm framework to repeated observations of mother–offspring interactions in wild and zoo-housed orang-utans (Pongo abelii, P. pygmaeus) to tease apart variation on the individual level from population-level and species-level differences. Our results showed that mothers not only differed in the composition of their infant-directed gestural repertoires, but also in communicative tactics, such as gestural redoings (i.e. persistence) and responsiveness to infants' requests. These differences remained after controlling for essential moderators, including species, setting, parity and infant age. Importantly, mothers differed in how they adjusted their behaviour across social contexts, making a strong case for investigating within-individual variation. Our findings highlight that partitioning behavioural variation into its within-individual, between-individual and environmental sources allows us to estimate the extent of plastic responses to the immediate environment in great ape communication.

Dialogic Book-Sharing as a Privileged Intersubjective Space.

Parental reading to young children is well-established as being positively associated with child cognitive development, particularly their language development. Research indicates that a particular, “intersubjective,” form of using books with children, “Dialogic Book-sharing” (DBS), is especially beneficial to infants and pre-school aged children, particularly when using picture books. The work on DBS to date has paid little attention to the theoretical and empirical underpinnings of the approach. Here, we address the question of what processes taking place during DBS confer benefits to child development, and why these processes are beneficial. In a novel integration of evidence, ranging from non-human primate communication through iconic gestures and pointing, archaeological data on Pre-hominid and early human art, to experimental and naturalistic studies of infant attention, cognitive processing, and language, we argue that DBS entails core characteristics that make it a privileged intersubjective space for the promotion of child cognitive and language development. This analysis, together with the findings of DBS intervention studies, provides a powerful intellectual basis for the wide-scale promotion of DBS, especially in disadvantaged populations.

Inferential Communication: Bridging the Gap Between Intentional and Ostensive Communication in Non-human Primates.

Communication, when defined as an act intended to affect the psychological state of another individual, demands the use of inference. Either the signaler, the recipient, or both must make leaps of understanding which surpass the semantic information available and draw from pragmatic clues to fully imbue and interpret meaning. While research into human communication and the evolution of language has long been comfortable with mentalistic interpretations of communicative exchanges, including rich attributions of mental state, research into animal communication has balked at theoretical models which describe mentalized cognitive mechanisms. We submit a new theoretical perspective on animal communication: the model of inferential communication. For use when existing proximate models of animal communication are not sufficient to fully explain the complex, flexible, and intentional communication documented in certain species, specifically non-human primates, we present our model as a bridge between shallower, less cognitive descriptions of communicative behavior and the perhaps otherwise inaccessible mentalistic interpretations of communication found in theoretical considerations of human language. Inferential communication is a framework that builds on existing evidence of referentiality, intentionality, and social inference in primates. It allows that they might be capable of applying social inferences to a communicative setting, which could explain some of the cognitive processes that enable the complexity and flexibility of primate communication systems. While historical models of animal communication focus on the means-ends process of behavior and apparent cognitive outcomes, inferential communication invites consideration of the mentalistic processes that must underlie those outcomes. We propose a mentalized approach to questions, investigations, and interpretations of non-human primate communication. We include an overview of both ultimate and proximate models of animal communication, which contextualize the role and utility of our inferential communication model, and provide a detailed breakdown of the possible levels of cognitive complexity which could be investigated using this framework. Finally, we present some possible applications of inferential communication in the field of non-human primate communication and highlight the role it could play in advancing progress toward an increasingly precise understanding of the cognitive capabilities of our closest living relatives.

Connecting primate gesture to the evolutionary roots of language: A systematic review.

Comparative psychology provides important contributions to our understanding of the origins of human language. The presence of common features in human and nonhuman primate communication can be used to suggest the evolutionary trajectories of potential precursors to language. However, to do so effectively, our findings must be comparable across diverse species. This systematic review describes the current landscape of data available from studies of gestural communication in human and nonhuman primates that make an explicit connection to language evolution. We found a similar number of studies on human and nonhuman primates, but that very few studies included data from more than one species. As a result, evolutionary inferences remain restricted to comparison across studies. We identify areas of focus, bias, and apparent gaps within the field. Different domains have been studied in human and nonhuman primates, with relatively few nonhuman primate studies of ontogeny and relatively few human studies of gesture form. Diversity in focus, methods, and socio-ecological context fill important gaps and provide nuanced understanding, but only where the source of any difference between studies is transparent. Many studies provide some definition for their use of gesture; but definitions of gesture, and in particular, criteria for intentional use, are absent in the majority of human studies. We find systematic differences between human and nonhuman primate studies in the research scope, incorporation of other modalities, research setting, and study design. We highlight eight particular areas in a call to action through which we can strengthen our ability to investigate gestural communication's contribution within the evolutionary roots of human language.

Distinct neuron populations for simple and compound calls in the primary auditory cortex of awake marmosets.

Marmosets are highly social non-human primates that live in families. They exhibit rich vocalization, but the neural basis underlying this complex vocal communication is largely unknown. Here we report the existence of specific neuron populations in marmoset A1 that respond selectively to distinct simple or compound calls made by conspecific marmosets. These neurons were spatially dispersed within A1 but distinct from those responsive to pure tones. Call-selective responses were markedly diminished when individual domains of the call were deleted or the domain sequence was altered, indicating the importance of the global rather than local spectral-temporal properties of the sound. Compound call-selective responses also disappeared when the sequence of the two simple-call components was reversed or their interval was extended beyond 1 s. Light anesthesia largely abolished call-selective responses. Our findings demonstrate extensive inhibitory and facilitatory interactions among call-evoked responses, and provide the basis for further study of circuit mechanisms underlying vocal communication in awake non-human primates.

Primate Vocal Communication and the Evolution of Speech

Studies of nonhuman primate communication are often motivated by the desire to shed light on the evolution of speech. In contrast to human speech, the vocal repertoires of nonhuman primates are evolutionarily highly conserved. Within species-specific constraints, calls may vary in relation to the internal state of the caller or social experience. Receivers can use signalers’ calls to predict upcoming events or behavioral dispositions. Yet nonhuman primates do not appear to express or comprehend communicative or informative intent. Signalers are sensitive to the relation between their own actions and receivers’ responses, and thus, signaling behavior can be conceived as goal directed. Receivers’ ability to integrate information from multiple sources renders the system flexible and powerful. Researchers who take a linguistic or biological perspective on nonhuman primate communication should be aware of the strengths and limitations of their approaches. Both benefit from a focus on the mechanisms that underpin signaling and responses to signals.

Dwarf mongoose alarm calls: investigating a complex non-human animal call.

Communication plays a vital role in the social lives of many species and varies greatly in complexity. One possible way to increase communicative complexity is by combining signals into longer sequences, which has been proposed as a mechanism allowing species with a limited repertoire to increase their communicative output. In mammals, most studies on combinatoriality have focused on vocal communication in non-human primates. Here, we investigated a potential combination of alarm calls in the dwarf mongoose (Helogale parvula), a non-primate mammal. Acoustic analyses and playback experiments with a wild population suggest: (i) that dwarf mongooses produce a complex call type (T3) which, at least at the surface level, seems to comprise units that are not functionally different to two meaningful alarm calls (aerial and terrestrial); and (ii) that this T3 call functions as a general alarm, produced in response to a wide range of threats. Using a novel approach, we further explored multiple interpretations of the T3 call based on the information content of the apparent comprising calls and how they are combined. We also considered an alternative, non-combinatorial interpretation that frames T3 as the origin, rather than the product, of the individual alarm calls. This study complements previous knowledge of vocal combinatoriality in non-primate mammals and introduces an approach that could facilitate comparisons between different animal and human communication systems.

Male gibbon loud morning calls conform to Zipf's law of brevity and Menzerath's law: insights into the origin of human language

The study of vocal communication in nonhuman primates, especially apes, offers critical insight into the origins of human language. Although human language represents a highly derived and complex form of communication, researchers have found that the organization of language follows a series of common statistical patterns, known as ‘linguistic laws’. Zipf's law of brevity and Menzerath's law are pervasive across human languages, and these laws have been identified in the communication of a small number of primate species. What remains less clear is whether these two laws also affect long-distance vocal communication in primates. Here, we provide evidence that the long-distance morning calls of male gibbons (cao vit gibbon, Nomascus nasutus, and western black-crested gibbon, Nomascus concolor ) follow both Zipf's law of brevity and Menzerath's law. We found that notes of male gibbon calls conform to Zipf's law of brevity, with the most common notes being shortest in duration. Similarly, longer sequences are made up of shorter calls on average, consistent with Menzerath's law; we also found a shortening of specific note type duration and an increase in proportion of shorter call types in longer sequences, which may underpin the emergence of this law. Our findings support the generality of these two linguistic laws beyond human language and provide evidence for compression at two levels of organizations (how frequently different note types are used, and how vocal sequences are constructed) in a long-range communication system. • Male gibbon morning calls conform to Zipf's law of brevity and Menzerath's law. • The most common notes being shortest in duration. • Longer sequences are made up of shorter calls on average.

Multimodal communication and language origins: integrating gestures and vocalizations.

The presence of divergent and independent research traditions in the gestural and vocal domains of primate communication has resulted in major discrepancies in the definition and operationalization of cognitive concepts. However, in recent years, accumulating evidence from behavioural and neurobiological research has shown that both human and non-human primate communication is inherently multimodal. It is therefore timely to integrate the study of gestural and vocal communication. Herein, we review evidence demonstrating that there is no clear difference between primate gestures and vocalizations in the extent to which they show evidence for the presence of key language properties: intentionality, reference, iconicity and turn-taking. We also find high overlap in the neurobiological mechanisms producing primate gestures and vocalizations, as well as in ontogenetic flexibility. These findings confirm that human language had multimodal origins. Nonetheless, we note that in great apes, gestures seem to fulfil a carrying (i.e. predominantly informative) role in close-range communication, whereas the opposite holds for face-to-face interactions of humans. This suggests an evolutionary shift in the carrying role from the gestural to the vocal stream, and we explore this transition in the carrying modality. Finally, we suggest that future studies should focus on the links between complex communication, sociality and cooperative tendency to strengthen the study of language origins.

The role of the motor system in action understanding and communication: Evidence from human infants and non-human primates.

There is growing evidence that activation of the motor system during observation of actions, a phenomenon first observed in non-human primates, underlies action understanding and even communication. This review (a) examines the evidence on motor system activity as an underlying neural correlate of action understanding; (b) reviews the theoretical and empirical work linking action understanding and the development of communication, with a specific focus on the role that gestures play as an intermediary; and (c) discusses the research on and existing opportunities for understanding the link between the motor system and communication in both humans and non-human primates, through the lens of action perception. Bringing together findings and perspectives from developmental social cognition in both humans and non-human primates and applying recent neuroscientific perspectives will help to elucidate the processes underlying the ability to understand and communicate with others.

The function of primate multimodal communication.

Language is commonly narrowed down to speech, but human face-to-face communication is in fact an intrinsically multimodal phenomenon. Despite growing evidence that the communication of non-human primates, our main model for the evolution of language, is also inherently multimodal, most studies on primate communication have focused on either gestures or vocalizations in isolation. Accordingly, the biological function of multimodal signalling remains poorly understood. In this paper, we aim to merge the perspectives of comparative psychology and behavioural ecology on multimodal communication, and review existing studies in great apes for evidence of multimodal signal function based on content-based, efficacy-based and inter-signal interaction hypotheses. We suggest that cross-species comparisons of great ape interactions in both captive and wild settings will allow us to test the conditions in which these hypotheses apply. We expect such studies to provide novel insights into the function of speech-accompanying signals and cues, such as gestures, facial expressions, and eye gaze.

Are olfactory traits in a pair-bonded primate under sexual selection? An evaluation of sexual dimorphism in Aotus nancymaae.

Sexual selection has seemingly influenced chemical communication in numerous non-human primates, although it is unclear whether it has influenced strictly pair-living and pair-bonded taxa. The physical similarities between male and female owl monkeys suggest that disruptive selection has not played a role in this taxon. However, given their nocturnality, olfactory traits may show differing patterns of sexual selection than visual traits. If sexual selection has influenced chemical communication in owl monkeys, we expect larger scent glands and greater scent-marking in females given the high degree of paternal care, as has been proposed for callitrichines. We evaluated sex differences in the qualitative and quantitative descriptions of the subcaudal and perianal glandular regions of captive male (n = 39) and female (n = 36) owl monkeys (A. nancymaae), and in the olfactory behaviors performed within breeding pairs (n = 16). Males had larger areas of secretion retained in the hairs covering the subcaudal gland, and females had more and darker secretion than males covering the perianal region. Males inspected the genital region of their partners more frequently than females did, but the sexes did not differ much in other investigative and marking behaviors. The observed sex differences and variation in olfactory traits are consistent with the hypothesis that sexual selection has influenced chemical communication in owl monkeys, with males having larger subcaudal glands and spending more time investigating odors. Still, sex differences in monogamous owl monkeys were less extreme than those in other, non-monogamous, taxa.

Different Approaches to Meaning in Primate Gestural and Vocal Communication.

In searching for the roots of human language, comparative researchers investigate whether precursors to language are already present in our closest relatives, the non-human primates. As the majority of studies into primates’ communication use a unimodal approach with focus on one signal type only, researchers investigate very different aspects depending on whether they are interested in vocal, gestural, or facial communication. Here, we focus on two signal types and discuss how meaning is created in the gestural (visual, tactile/auditory) as compared to the vocal modality in non-human primates, to highlight the different research foci across these modalities. First, we briefly describe the defining features of meaning in human language and introduce some debates concerning meaning in non-human communication. Second, with focus on these features, we summarize the current evidence for meaningful communication in gestural as compared to vocal communication and demonstrate that meaning is operationalized very differently by researchers in these two fields. As a result, it is currently not possible to generalize findings across these modalities. Rather than arguing for or against the occurrence of semantic communication in non-human primates, we aim at pointing to gaps of knowledge in studying meaning in our closest relatives, and these gaps might be closed.

Profile of Dorothy L. Cheney and Robert M. Seyfarth

Field studies in Africa over the past four decades by ethologists Dorothy Cheney and Robert Seyfarth have uncovered a trove of insights into the behavior, communication, and social cognition of nonhuman primates. The pair’s research further reveals evolutionary antecedents of the human mind. University of Pennsylvania professors emeriti, Cheney and Seyfarth are both elected members of the National Academy of Sciences. For her Inaugural Article cowritten with Seyfarth, Cheney strengthens the hypothesis that many primate vocalizations shape social interactions. Factors driving the early stages of language evolution may therefore be associated with primate social challenges. Dorothy Cheney and baboons. Image courtesy of Keena Roberts (photographer). Robert Seyfarth and baboons crossing water. Image courtesy of Dorothy L. Cheney. As youths, Cheney and Seyfarth enjoyed travel and nature. Cheney’s father was in the US Foreign Service, so her family moved to a different place every few years before returning to Washington, DC. “My parents’ rather laissez faire approach to child-rearing allowed my sister and me to travel alone around India in our teenage years,” says Cheney. “We were given complete independence, for which I’ve always been grateful.” Seyfarth’s father was a Chicago-based businessman. “He also loved the outdoors, and on fishing trips to Canada and the Caribbean, taught me how to enjoy the wilderness even when we didn’t catch fish,” Seyfarth says. Cheney and Seyfarth were not initially drawn to science. Cheney preferred history at her preparatory school in Massachusetts, Abbot Academy, and Seyfarth at first struggled with science. He says, “I found science courses difficult and unappealing until, in my senior year at Phillips Exeter Academy in New Hampshire, I took a course on Darwin. The theory of evolution brought everything into focus and made all that memorization seem worthwhile.” Cheney’s “Darwin moment” happened in the spring term of her Wellesley …

Emergence of living language: ontogeny–phylogeny framework and other parallels of linguistics and biology

Abstract Although language is something deeply embedded in our nature, the question of its origin is of the same order as the misty question of the origin of life. I point out that the core of the problem can be rooted in the dichotomy between language and speech, similar to the dichotomy of genotype and phenotype in biology. Following the ontogeny–phylogeny framework, I propose that studies of language ontogeny, especially its early stages, can bring a new understanding to language, same as the study of communication in non-human primates.