Social learning of a communicative signal in captive chimpanzees

The acquisition of linguistic competency from more experienced social partners is a fundamental aspect of human language. However, there is little evidence that non-human primates learn to use their vocalizations from social partners. Captive chimpanzees (Pan troglodytes) produce idiosyncratic vocal signals that are used intentionally to capture the attention of a human experimenter. Interestingly, not all apes produce these sounds, and it is unclear what factors explain this difference. We tested the hypothesis that these attention-getting (AG) sounds are socially learned via transmission between mothers and their offspring. We assessed 158 chimpanzees to determine if they produced AG sounds. A significant association was found between mother and offspring sound production. This association was attributable to individuals who were raised by their biological mother-as opposed to those raised by humans in a nursery environment. These data support the hypothesis that social learning plays a role in the acquisition and use of communicative vocal signals in chimpanzees.     

Communicative signaling activates 'Broca's' homolog in chimpanzees

Broca's area, a cerebral cortical area located in the inferior frontal gyrus (IFG) of the human brain, has been identified as one of several critical regions associated with the motor planning and execution of language. Anatomically, Broca's area is most often larger in the left hemisphere, and functional imaging studies in humans indicate significant left-lateralized patterns of activation during language-related tasks. If, and to what extent, nonhuman primates, particularly chimpanzees, possess a homologous region that is involved in the production of their own communicative signals remains unknown. Here, we show that portions of the IFG as well as other cortical and subcortical regions in chimpanzees are active during the production of communicative signals. These findings are the first to provide direct evidence of the neuroanatomical structures associated with the production of communicative behaviors in chimpanzees. Significant activation in the left IFG in conjunction with other cortical and subcortical brain areas during the production of communicative signals in chimpanzees suggests that the neurological substrates underlying language production in the human brain may have been present in the common ancestor of humans and chimpanzees.     

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.     

Chimpanzee Alarm Call Production Meets Key Criteria for Intentionality

Determining the intentionality of primate communication is critical to understanding the evolution of human language. Although intentional signalling has been claimed for some great ape gestural signals, comparable evidence is currently lacking for their vocal signals. We presented wild chimpanzees with a python model and found that two of three alarm call types exhibited characteristics previously used to argue for intentionality in gestural communication. These alarm calls were: (i) socially directed and given to the arrival of friends, (ii) associated with visual monitoring of the audience and gaze alternations, and (iii) goal directed, as calling only stopped when recipients were safe from the predator. Our results demonstrate that certain vocalisations of our closest living relatives qualify as intentional signals, in a directly comparable way to many great ape gestures. We conclude that our results undermine a central argument of gestural theories of language evolution and instead support a multimodal origin of human language.     

Chimpanzees (Pan troglodytes) Produce the Same Types of ‘Laugh Faces’ when They Emit Laughter and when They Are Silent

The ability to flexibly produce facial expressions and vocalizations has a strong impact on the way humans communicate, as it promotes more explicit and versatile forms of communication. Whereas facial expressions and vocalizations are unarguably closely linked in primates, the extent to which these expressions can be produced independently in nonhuman primates is unknown. The present work, thus, examined if chimpanzees produce the same types of facial expressions with and without accompanying vocalizations, as do humans. Forty-six chimpanzees (Pan troglodytes) were video-recorded during spontaneous play with conspecifics at the Chimfunshi Wildlife Orphanage. ChimpFACS was applied, a standardized coding system to measure chimpanzee facial movements, based on FACS developed for humans. Data showed that the chimpanzees produced the same 14 configurations of open-mouth faces when laugh sounds were present and when they were absent. Chimpanzees, thus, produce these facial expressions flexibly without being morphologically constrained by the accompanying vocalizations. Furthermore, the data indicated that the facial expression plus vocalization and the facial expression alone were used differently in social play, i.e., when in physical contact with the playmates and when matching the playmates’ open-mouth faces. These findings provide empirical evidence that chimpanzees produce distinctive facial expressions independently from a vocalization, and that their multimodal use affects communicative meaning, important traits for a more explicit and versatile way of communication. As it is still uncertain how human laugh faces evolved, the ChimpFACS data were also used to empirically examine the evolutionary relation between open-mouth faces with laugh sounds of chimpanzees and laugh faces of humans. The ChimpFACS results revealed that laugh faces of humans must have gradually emerged from laughing open-mouth faces of ancestral apes. This work examines the main evolutionary changes of laugh faces since the last common ancestor of chimpanzees and humans.     

Vocal responsiveness in male wild chimpanzees: implications for the evolution of language

Several captive chimpanzees and bonobos have learned to use symbols and to comprehend syntax. Thus, compared with other nonhumans, these animals appear to have unusual cognitive powers that can be recruited for communicative behavior. This raises the possibility that wild chimpanzee vocal communication is more complex than heretofore demonstrated. To examine this possibility, I investigated whether wild chimpanzee vocal exchanges exhibit uniquely human conversational attributes. The results indicate that wild chimpanzees vocalize at low rates, tend not to respond to calls that they hear, and, when they do respond, tend to give calls that are similar to the ones they have heard. Thus, chimpanzee vocal interactions resemble those of other primate species, and show no special similarity to human conversations. The results support the view that we need to explore cognitive and social continuities and discontinuities with nonhuman primates to understand the origin and evolution of language, but also emphasize the need for fine-grained analyses of wild chimpanzee vocal interactions.     

Human infants and baboons show the same pattern of handedness for a communicative gesture

To test the role of gestures in the origin of language, we studied hand preferences for grasping or pointing to objects at several spatial positions in human infants and adult baboons. If the roots of language are indeed in gestural communication, we expect that human infants and baboons will present a comparable difference in their pattern of laterality according to task: both should be more right-hand/left-hemisphere specialized when communicating by pointing than when simply grasping objects. Our study is the first to test both human infants and baboons on the same communicative task. Our results show remarkable convergence in the distribution of the two species' hand biases on the two kinds of tasks: In both human infants and baboons, right-hand preference was significantly stronger for the communicative task than for grasping objects. Our findings support the hypothesis that left-lateralized language may be derived from a gestural communication system that was present in the common ancestor of baboons and humans.     

A structure-based repertoire of manual gestures in wild chimpanzees: statistical analyses of a graded communication system

Great ape gestural communication is considered important in understanding the evolution of human language as these share important features, namely, flexible and intentional signal use. Although gestural repertoires have been compiled for captive and wild primates, reports are largely qualitative. We quantify the morphological structure and variation of gestural signals identified in the repertoire of a community of wild chimpanzees. Gestures were classified on the basis of 29 morphological features, such as trajectory and orientation during the preparatory and stroke phases of a gesture. Hierarchical cluster and discriminant function analyses identified 30 morphologically distinct manual gesture types; the majority was subsequently correctly classified using a cross-validation technique, with incorrect classifications for rare gesture types only. Comparisons of this statistically determined repertoire with previous repertoires did not identify systematic variation between captive and wild chimpanzees. Moreover, consensus was not greater within studies of the same populations, highlighting the importance of systematic and well-documented inventories. Our morphologically based analyses indicate that manual gestures are best considered as graded rather than discrete communication signals, similar to some vocalisation systems. We discuss these findings in light of current theories of human language evolution.     

The neural and cognitive correlates of aimed throwing in chimpanzees: a magnetic resonance image and behavioural study on a unique form of social tool use

It has been hypothesized that neurological adaptations associated with evolutionary selection for throwing may have served as a precursor for the emergence of language and speech in early hominins. Although there are reports of individual differences in aimed throwing in wild and captive apes, to date there has not been a single study that has examined the potential neuroanatomical correlates of this very unique tool-use behaviour in non-human primates. In this study, we examined whether differences in the ratio of white (WM) to grey matter (GM) were evident in the homologue to Broca's area as well as the motor-hand area of the precentral gyrus (termed the KNOB) in chimpanzees that reliably throw compared with those that do not. We found that the proportion of WM in Broca's homologue and the KNOB was significantly higher in subjects that reliably throw compared with those that do not. We further found that asymmetries in WM within both brain regions were larger in the hemisphere contralateral to the chimpanzee's preferred throwing hand. We also found that chimpanzees that reliably throw show significantly better communication abilities than chimpanzees that do not. These results suggest that chimpanzees that have learned to throw have developed greater cortical connectivity between primary motor cortex and the Broca's area homologue. It is suggested that during hominin evolution, after the split between the lines leading to chimpanzees and humans, there was intense selection on increased motor skills associated with throwing and that this potentially formed the foundation for left hemisphere specialization associated with language and speech found in modern humans.     

The learning and use of gestural signals by young chimpanzees: A trans-generational study

Observations of chimpanzee gestural communication are reported. The observations represent the third longitudinal time point of an ongoing study of the Yerkes Primate Center Field Station chimpanzee group. In contrast to observations at the first two time points, the current observations are of a new generation of infants and juveniles. There were two questions. The first concerned how young chimpanzees used their gestures, with special focus on the flexibility or intentionality displayed. It was found that youngsters quite often used the same gesture in different contexts, and different gestures in the same context. In addition, they sometimes used gestures in combinations in a single social encounter, these combinations did not convey intentions that could not be conveyed by the component gestures, however. It was also found that individuals adjusted their choice of signals depending on the attentional state of the recipient. The second question was how chimpanzees acquired their gestural signals. In general, it was found that there was little consistency in the use of gestures among individuals, especially for non-play gestures, with much individual variability both within and across generations. There were also a number of idiosyncratic gestures used by single individuals at each time point. It was concluded from these results that youngsters were not imitatively learning their communicatory gestures from conspecifics, but rather that they were individually conventionalizing them with each other. Implications of these findings for the understanding of chimpanzee communication and social learning are discussed.     

The sound of one-hand clapping: handedness and perisylvian neural correlates of a communicative gesture in chimpanzees

Whether lateralization of communicative signalling in non-human primates might constitute prerequisites of hemispheric specialization for language is unclear. In the present study, we examined (i) hand preference for a communicative gesture (clapping in 94 captive chimpanzees from two research facilities) and (ii) the in vivo magnetic resonance imaging brain scans of 40 of these individuals. The preferred hand for clapping was defined as the one in the upper position when the two hands came together. Using computer manual tracing of regions of interest, we measured the neuroanatomical asymmetries for the homologues of key language areas, including the inferior frontal gyrus (IFG) and planum temporale (PT). When considering the entire sample, there was a predominance of right-handedness for clapping and the distribution of right- and left-handed individuals did not differ between the two facilities. The direction of hand preference (right- versus left-handed subjects) for clapping explained a significant portion of variability in asymmetries of the PT and IFG. The results are consistent with the view that gestural communication in the common ancestor may have been a precursor of language and its cerebral substrates in modern humans.     

Gestural communication in young gorillas (Gorilla gorilla): gestural repertoire,learning, and use

In the present study we investigated the gestural communication of gorillas (Gorilla gorilla). The subjects were 13 gorillas (1-6 years old) living in two different groups in captivity. Our goal was to compile the gestural repertoire of subadult gorillas, with a special focus on processes of social cognition, including attention to individual and developmental variability, group variability, and flexibility of use. Thirty-three different gestures (six auditory, 11 tactile, and 16 visual gestures) were recorded. We found idiosyncratic gestures, individual differences, and similar degrees of concordance between and within groups, as well as some group-specific gestures. These results provide evidence that ontogenetic ritualization is the main learning process involved, but some form of social learning may also be responsible for the acquisition of special gestures. The present study establishes that gorillas have a multifaceted gestural repertoire, characterized by a great deal of flexibility with accommodations to various communicative circumstances, including the attentional state of the recipient. The possibility of assigning Seyfarth and Cheney's [1997] model for nonhuman primate vocal development to the development of nonhuman primate gestural communication is discussed.     

When the hands speak.

In the present review we will summarize evidence that the control of spoken language shares the same system involved in the control of arm gestures. Studies of primate premotor cortex discovered the existence of the so-called mirror system as well as of a system of double commands to hand and mouth. These systems may have evolved initially in the context of ingestion, and later formed a platform for combined manual and vocal communication. In humans, manual gestures are integrated with speech production, when they accompany speech. Lip kinematics and parameters of voice spectra during speech production are influenced by executing or observing transitive actions (i.e. guided by an object). Manual actions also play an important role in language acquisition in children, from the babbling stage onwards. Behavioural data reported here even show a reciprocal influence between words and symbolic gestures and studies employing neuroimaging and repetitive transcranial magnetic stimulation (rTMS) techniques suggest that the system governing both speech and gesture is located in Broca's area.     

Identification of vocalizers by pant hoots,pant grunts and screams in a chimpanzee

Identification of vocalizers was examined using an auditory-visual matching-to-sample task with a female chimpanzee. She succeeded in selecting the picture of the vocalizer in response to various types of vocalizations: pant hoots, pant grunts, and screams. When pant hoots by two chimpanzees were presented as a "duet", she could identify both of the vocalizers. These results suggest that researchers have underestimated the capability of vocalizer identification in chimpanzees. The chimpanzee correctly chose her own pictures in response to her vocalizations only by exclusion, and she did not show vocal self-recognition. The effect of acoustical modification (pitch shift and filtration) on the performance suggested that pitch is an important cue for the vocalizer identification.     

Begging and social tolerance: Food solicitation tactics in young chimpanzees (Pan troglodytes) in the wild

The substantial role of food sharing in human evolution has been widely recognized, and food-soliciting tactics may have been critical in facilitating these transfers. Great apes, our closest living relatives, also use different food-soliciting tactics to obtain food from both kin and non-kin. However, the individual and social factors involved in requests for and subsequent transfers of food have been relatively little studied. Here, we examined which tactics (e.g., tactile gestures, taking actions, and vocalizations) infant chimpanzees (Pan troglodytes) employ to solicit food as well as the success of obtaining food from their conspecifics. Using a multimodal approach, we focused on food-related interactions in 14 chimpanzee infants of two different subspecies (P. t. schweinfurthii/verus) living in the communities of Kanyawara, Uganda, and Taï South, Côte d'Ivoire. Overall, we found that infants' solicitation tactics included mainly visual or tactile gestural requests and taking attempts, while vocalizations and gestures involving auditory components were rarely used. With increasing age, infants used more visual gestures when soliciting food from conspecifics other than the mother. If food was solicited from mothers or maternal kin, infants predominantly begged for food via (mechanically effective) taking attempts. In terms of subsequent food transfers, taking attempts were more successful than gestures. In light of the prevalent use of non-contact begging despite low rates of success, food solicitation in young great apes might also function to facilitate social tolerance and gain social information. We thus conclude that the food sharing context might represent a critical platform to learn and practice social rules underlying cooperative interactions, which can later be generalized across collaborative domains.     

Wernicke's area homologue in chimpanzees (Pan troglodytes) and its relation to the appearance of modern human language

Human language is distinctive compared with the communication systems of other species. Yet, several questions concerning its emergence and evolution remain unresolved. As a means of evaluating the neuroanatomical changes relevant to language that accompanied divergence from the last common ancestor of chimpanzees, bonobos and humans, we defined the cytoarchitectonic boundaries of area Tpt, a component of Wernicke''s area, in 12 common chimpanzee brains and used design-based stereologic methods to estimate regional volumes, total neuron number and neuron density. In addition, we created a probabilistic map of the location of area Tpt in a template chimpanzee brain coordinate space. Our results show that chimpanzees display significant population-level leftward asymmetry of area Tpt in terms of neuron number, with volume asymmetry approaching significance. Furthermore, asymmetry in the number of neurons in area Tpt was positively correlated with asymmetry of neuron numbers in Brodmann''s area 45, a component of Broca''s frontal language region. Our findings support the conclusion that leftward asymmetry of Wernicke''s area originated prior to the appearance of modern human language and before our divergence from the last common ancestor. Moreover, this study provides the first evidence of covariance between asymmetry of anterior and posterior cortical regions that in humans are important to language and other higher order cognitive functions.     

Signs of intelligence in cross-fostered chimpanzees

In cross-fostering, the young of one species are reared by adults of another, as in the classical ethological studies of imprinting and song-learning. In our laboratory, infant chimpanzees were reared under human conditions that included two-way communication in American Sign Language (A.S.L.), the gestural language of the deaf in North America. A large body of evidence from five chimpanzees demonstrated stage by stage replication of basic aspects of the acquisition of speech and signs by hearing and deaf children. Here we review evidence that, under double-blind conditions: (i) the chimpanzees communicated information in A.S.L. to human observers; (ii) independent human observers agreed in their identification of the chimpanzee signs, (iii) the chimpanzees could use the signs to refer to natural language categories: DOG for any dog, FLOWER for any flower, SHOE for any shoe.     

The origins of non-human primates' manual gestures

The increasing body of research into human and non-human primates' gestural communication reflects the interest in a comparative approach to human communication, particularly possible scenarios of language evolution. One of the central challenges of this field of research is to identify appropriate criteria to differentiate a gesture from other non-communicative actions. After an introduction to the criteria currently used to define non-human primates' gestures and an overview of ongoing research, we discuss different pathways of how manual actions are transformed into manual gestures in both phylogeny and ontogeny. Currently, the relationship between actions and gestures is not only investigated on a behavioural, but also on a neural level. Here, we focus on recent evidence concerning the differential laterality of manual actions and gestures in apes in the framework of a functional asymmetry of the brain for both hand use and language.     

Where did language come from? Connecting sign,song, and speech in hominin evolution

Recently theorists have developed competing accounts of the origins and nature of protolanguage and the subsequent evolution of language. Debate over these accounts is lively. Participants ask: Is music a direct precursor of language? Were the first languages gestural? Or is language continuous with primate vocalizations, such as the alarm calls of vervets? In this article I survey the leading hypotheses and lines of evidence, favouring a largely gestural conception of protolanguage. However, the “sticking point” of gestural accounts, to use Robbins Burling’s phrase, is the need to explain how language shifted to a largely vocal medium. So with a critical eye I consider Michael Corballis’s most recent expression of his ideas about this transition (2017’s The Truth About Language: What It Is And Where It Came From). Corballis’s view is an excellent foil to mine and I present it as such. Contrary to Corballis’s account, and developing Burling’s conjecture that musicality played some role, I argue that the foundations of an evolving musicality (i.e., evolving largely independently of language) provided the means and medium for the shift from gestural to vocal dominance in language. In other words, I suggest that an independently evolving musicality prepared ancient hominins, morphologically and cognitively, for intentional articulate vocal production, enabling the evolution of speech.     

The origins of gestures and language: history,current advances and proposed theories

Investigating in depth the mechanisms underlying human and non‐human primate intentional communication systems (involving gestures, vocalisations, facial expressions and eye behaviours) can shed light on the evolutionary roots of language. Reports on non‐human primates, particularly great apes, suggest that gestural communication would have been a crucial prerequisite for the emergence of language, mainly based on the evidence of large communication repertoires and their associated multifaceted nature of intentionality that are key properties of language. Such research fuels important debates on the origins of gestures and language. We review here three non‐mutually exclusive processes that can explain mainly great apes' gestural acquisition and development: phylogenetic ritualisation, ontogenetic ritualisation, and learning via social negotiation. We hypothesise the following scenario for the evolutionary origins of gestures: gestures would have appeared gradually through evolution via signal ritualisation following the principle of derived activities, with the key involvement of emotional expression and processing. The increasing level of complexity of socioecological lifestyles and associated daily manipulative activities might then have enabled the acquisition and development of different interactional strategies throughout the life cycle. Many studies support a multimodal origin of language. However, we stress that the origins of language are not only multimodal, but more broadly multicausal. We propose a multicausal theory of language origins which better explains current findings. It postulates that primates' communicative signalling is a complex trait continually shaped by a cost–benefit trade‐off of signal production and processing of interactants in relation to four closely interlinked categories of evolutionary and life cycle factors: species, individual and context‐related characteristics as well as behaviour and its characteristics. We conclude by suggesting directions for future research to improve our understanding of the evolutionary roots of gestures and language.