Two organizing principles of vocal production: Implications for nonhuman and human primates

Human language is largely a vocal behavior, but its evolutionary origins remain elusive. Although vocalizations are also the main way by which nonhuman primates communicate and interact socially, it has been difficult to demonstrate direct transitions from nonlinguistic primate vocal communication to human language. Nonhuman primates produce and perceive sounds by specialized anatomical and neural structures also present in humans. Compared to humans, however, nonhuman primates are severely limited in the control they have over vocal production, which restricts their ability to produce rapid sound combinations and limits vocal learning. But language is also a cognitive capacity, and there is good evidence that nonhuman primates understand others’ calls as given by specific individuals to specific events or as part of specific social interactions. In great apes, callers can take the past history with their audience into account by suppressing, exaggerating, and socially directing their calls in seemingly strategic ways. But there is no clear evidence that primates, apart from humans, perceive others as governed by complex mental states, especially knowledge, during acts of communication, nor is there evidence that they are motivated to seek common ground and actively inform their audience accordingly. There is also no clear indication that nonhuman primates use vocalizations for the sole purpose of social bonding. One hypothesis is that these differences in cognitive ability and social motivation may have prevented the evolution of flexible and combinatorial vocal communication in nonhuman primates.

The present article offers a condensed overview, of why a comparative view on gestures in human and nonhuman primates may offer important insights to both: researchers of human as well as of nonhuman primates. It is argued that a comparative view may further contribute to the debate over the evolution of language but that in addition it may also enhance understanding of the relation of language and gesture in humans. The article sketches programmatic issues, which are summarized in the list of framing questions for the workshop and this special issue on “Gestural communication in nonhuman and human primates”; it is aimed to clarify conceptual and methodological prerequisites and to offer points of departure for future comparative research.

The present article offers a condensed overview, of why a comparative view on gestures in human and nonhuman primates may offer important insights to both: researchers of human as well as of nonhuman primates. It is argued that a comparative view may further contribute to the debate over the evolution of language but that in addition it may also enhance understanding of the relation of language and gesture in humans. The article sketches programmatic issues, which are summarized in the list of framing questions for the workshop and this special issue on “Gestural communication in nonhuman and human primates”; it is aimed to clarify conceptual and methodological prerequisites and to offer points of departure for future comparative research.

The present article offers a condensed overview, of why a comparative view on gestures in human and nonhuman primates may offer important insights to both: researchers of human as well as of nonhuman primates. It is argued that a comparative view may further contribute to the debate over the evolution of language but that in addition it may also enhance understanding of the relation of language and gesture in humans. The article sketches programmatic issues, which are summarized in the list of framing questions for the workshop and this special issue on “Gestural communication in nonhuman and human primates”; it is aimed to clarify conceptual and methodological prerequisites and to offer points of departure for future comparative research.

Vocal communication is common in the animal kingdom. Researchers often examine vocal communication in nonhuman primates (primates) with the aim of identifying similarities and differences with human language and speech, in order to trace the evolutionary origins of our complex communication system. Primates can produce distinct calls in response to specific events, such as the discovery of a certain predator, and listeners seem to understand what these calls refer to. Although on the surface there are similarities between this type of communication and human referential words, the mental processes that underlie them may be very different. While in general the flexibility shown by primate receivers may demonstrate some commonalities with humans, there is much more controversy over whether there are similarities between the production of primate vocalizations and language. It is widely accepted that primates, unlike humans, lack the ability to generate new vocalizations. Although this means primates have a closed repertoire of calls that cannot be expanded, primates are capable of combining their existing calls to generate new messages. The degree of voluntary control and intentionality involved in the use of calls is also a matter of debate, with recent evidence on both a neural and behavioral level challenging traditional assumptions that primate vocalizations are used in an automatic, reflexive manner. More research is needed to examine the mental processes underlying communicative behavior in both the producer and the receiver. In the future adopting a more holistic, multimodal approach to studying primate communication is likely to challenge and ultimately improve our understanding of primate communication and the evolution of human language.

If we accept the view that language first evolved from the conceptual structure of our pre-linguistic ancestors, several questions arise, including: What kind of structure? Concepts about what? Here we review research on the vocal communication and cognition of nonhuman primates, focusing on results that may be relevant to the earliest stages of language evolution. From these data we conclude, first, that nonhuman primates’ inability to represent the mental states of others makes their communication fundamentally different from human language. Second, while nonhuman primates’ production of vocalizations is highly constrained, their ability to extract complex information from sounds is not. Upon hearing vocalizations, listeners acquire information about their social companions that is referential, discretely coded, hierarchically structured, rule-governed, and propositional. We therefore suggest that, in the earliest stages of language evolution, communication had a formal structure that grew out of its speakers’ knowledge of social relations.

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.

Research into gestures represents a multifaceted field comprising a wide range of disciplines and research topics, varying methods and approaches, and even different species such as humans, apes and monkeys. The aim of this volume (originally published as a Special Issue of Gesture 5:1/2 (2005)) is to bring together the research in gestural communication in both nonhuman and human primates and to explore the potential of a comparative approach and its contribution to the question of an evolutionary scenario in which gestures play a significant role. The topics covered include the spontaneous natural gesture use in social groups of apes and monkeys, but also during interactions with humans, gestures of preverbal children and their interaction with language, speech-accompanying gestures in humans as well as the use of sign-language in human and nonhuman great apes. It addresses researchers with a background in Psychology, Primatology, Linguistics, and Anthropology, but it might also function as an introduction and a documentation state of the art for a wider less specialised audience which is fascinated by the role gestures might have played in the evolution of human language.

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.

In the last two decades, the study of language parallels in nonhuman animals has generated considerable controversy and excitement. Many have perceived demonstrations of linguistic skills in nonhuman animals as a threat to human uniqueness, whereas others have been uncritical of claims for complex cognitive skills in animals. Two different paradigms for studying linguistic parallels have appeared. One approach teaches great apes linguistic analogues of human language using signs or arbitrary symbol systems; the other seeks to decode communicative complexity in the natural languages of nonhuman animals. This paper reviews the language analogue studies with great apes and cetaceans, examining the utility of the different methods and reviewing the animals' accomplishments. Studies of ontogeny, syntax, referential communication, audience effects, and perception of vocalizations in the natural communication of birds, squirrels, and primates are evaluated. Finally, the brain mechanisms underlying human speech and language are compared with those involved in vocal communication in nonhuman primates. Although chimpanzees and bonobos have accomplished much, they do not threaten human uniqueness with respect to speech and language. Many of the claims for language paralleles in natural communication systems of nonhuman animals are weak, and many can be interpreted without recourse to cognitive constructs. Whereas there exist many similarities between subcortical controls of language and of animal vocalizations, there are no parallels to Broca's and Wernicke's areas in monkeys. However, the critical studies have not been done.

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

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.

Human language is probably the most complex communication system in the living world. It is investigated by various scientific disciplines, including linguistics, neuroscience, or cultural studies. However, despite this large and interdisciplinary effort, one key question has remained open and continues to perplex the scientific community; how could such an intricate system evolve? Comparative research on our extant evolutionary neighbours—the non-human primates—is often considered a good starting point to investigate the origins and evolution of human language. As humans communicate mainly with speech, primate vocal behaviour is the natural target of investigation, although this approach is not uniformly accepted. Behaviourist theories, in particular, characterise primate vocal behaviour as a predominantly hard-wired system, arguing that not much can be learned from it regarding language evolution. On the other hand, there is growing evidence for a considerable cognitive component in non-human primate communication, which often points to early signs of flexibility and indications of gradual evolutionary patterns more generally. In this thesis, I ventured to further our understanding of the flexibility in non-human primate communication systems through series of field experiments on wild South African vervet monkeys. First, I assessed the capacity of vervet monkeys to socially learn novel call-context associations. Using unfamiliar animal models in conjunction with alarm call playbacks, I showed that monkeys rapidly associated alarm calls with these models, evidenced by high vigilance towards them in the subsequent encounter. Furthermore, some juveniles also produced alarm calls similar to the playbacks they heard during the first encounter, showing how rapid social learning could influence call comprehension and usage in this species. In a second experiment, I tested the functional flexibility of vocalisations by providing wild vervet monkeys with opportunities to socially learn a novel usage of move-grunts to obtain food rewards. I worked with two groups that differed in the complexity of the learning stimuli provided during the experiments. For the first group of monkeys, I paired playback of movegrunt with a food dispenser providing a reward, such that the call predicted food as a simple conditioning stimulus. In the second group, I provided subjects with a demonstration video of a conspecific producing a move-grunt in order to activate the food dispenser and obtain a reward. While I did not find any evidence for relevant learning in the first group, a juvenile female from the second group started to produce her own move-grunts to obtain food rewards, suggesting that primates can learn to produce calls in completely novel circumstances if provided with the right social input. The focus of the third experiment was on flexibility in call perception. I examined whether vervet monkeys, when confronted with referentially ambiguous calls, use contextual information to respond to them. I addressed this by probing them with male 'leopard' alarm calls, which can naturally be given to terrestrial predators or during intergroup encounters. In the experiment, I played back leopard alarms either during natural between-group encounters or in a control situation. The subjects showed anti-predator responses and looked for additional information in control but not inter-group situations, suggesting that call meaning in primate communication is subject to simple forms of pragmatic inference. The results of these experiments indicate that non-human primate vocal communication rests on a primitive cognitive infrastructure that, within the human lineage, could have gradually evolved into the complex communication system seen in today's human languages. Finally, I conclude the thesis by proposing a classification scheme for non-human primate vocalisations, based on differences in underlying cognitive complexity, and briefly speculate about the future of primate research in light of emerging technologies that have the potential to revolutionise our understanding of the evolution of human and non-human communication.

Locomotor behavior and control in human and non-human primates: Comparisons with cats and dogs

The evolution of human language has been discussed for centuries from different perspectives. Linguistic theory has proposed grammar as a core part of human language that has to be considered in this context. Recent advances in neurosciences have allowed us to take a new neurobiological look on the similarities and dissimilarities of cognitive capacities and their neural basis across both closely and distantly related species. A couple of decades ago, the comparisons were mainly drawn between human and non-human primates, investigating the cytoarchitecture of particular brain areas and their structural connectivity. Moreover, comparative studies were conducted with respect to their ability to process grammars of different complexity. So far the available data suggest that non-human primates are able to learn simple probabilistic grammars, but not hierarchically structured complex grammars. The human brain, which easily learns both grammars, differs from the non-human brain (among others) in how two language-relevant brain regions (Broca's area in the inferior frontal cortex and the superior temporal cortex) are connected structurally by fiber tracts which run dorsally and ventrally in the primate brain. Whether the more dominant dorsal pathway in humans compared to non-human primates is causally related to this behavioral difference is an issue of current debate. Ontogenetic findings suggest at least a correlation between the maturation of the dorsal pathway and the behavior to process syntactically complex structures, although the ultimate causal prove is still not available. Thus, the neural basis of complex grammar processing in humans remains to be defined. More recently it has been reported that songbirds are also able to distinguish between sound sequences reflecting complex grammar. Interestingly, songbirds learn to sing by imitating adult song in a process not unlike language development in children. Moreover, the neural circuits supporting this behavior in songbirds bear anatomical and functional similarities to those in humans. In adult humans the fiber tract connecting the auditory cortex and motor cortex dorsally is known to be involved in the repetition of spoken language. This pathway is present already at birth and is taken to play a major role during language acquisition. In songbirds, detailed information exist concerning the interaction of auditory, motor, and cortical-basal ganglia processing during song learning, and present a rich substrate for comparative studies. The scope of the Research Topic was to bring together contributions of researchers from different fields, who investigate grammar processing in humans, non-human primates, and songbirds with the aim to find answers to the question of what constitutes the neurobiological basis of language and language learning. A number of contributions discuss the ventral and dorsal pathways in human and non-human primates considering their functional roles in speech and language. Some of these take an evolutionary perspective comparing non-human and human primates (Rauschecker, 2012; Rilling et al., 2012), whereas other takes an ontogenetic perspective (Friederici, 2012). The functional roles of the ventral and dorsal pathways in language and other modalities in particular action including articulatory and hand gestures are discussed in further articles (Fitch, 2011; Aboitiz, 2012; Rijntjes et al., 2012). Two articles consider the language system at the interface of two other human specific abilities, namely number processing (Heim et al., 2012) and reading (Lachmann et al., 2012). A couple of contributions take the evolutionary perspective even further by including song birds into their comparative approach (Berwick et al., 2012; Kiggins et al., 2012; Petkov and Jarvis, 2012). The selection of the articles provides a picture of the current views on the evolutionary and neurobiological basis of the language and language learning.