Katja Liebal

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.

The quartet theory of human emotions: An integrative and neurofunctional model

Despite an explosion of research in the affective sciences during the last few decades, interdisciplinary theories of human emotions are lacking. Here we present a neurobiological theory of emotions that includes emotions which are uniquely human (such as complex moral emotions), considers the role of language for emotions, advances the understanding of neural correlates of attachment-related emotions, and integrates emotion theories from different disciplines. We propose that four classes of emotions originate from four neuroanatomically distinct cerebral systems. These emotional core systems constitute a quartet of affect systems: the brainstem-, diencephalon-, hippocampus-, and orbitofrontal-centred affect systems. The affect systems were increasingly differentiated during the course of evolution, and each of these systems generates a specific class of affects (e.g., ascending activation, pain/pleasure, attachment-related affects, and moral affects). The affect systems interact with each other, and activity of the affect systems has effects on - and interacts with - biological systems denoted here as emotional effector systems. These effector systems include motor systems (which produce actions, action tendencies, and motoric expression of emotion), peripheral physiological arousal, as well as attentional and memory systems. Activity of affect systems and effector systems is synthesized into an emotion percept (pre-verbal subjective feeling), which can be transformed (or reconfigured) into a symbolic code such as language. Moreover, conscious cognitive appraisal (involving rational thought, logic, and usually language) can regulate, modulate, and partly initiate, activity of affect systems and effector systems. Our emotion theory integrates psychological, neurobiological, sociological, anthropological, and psycholinguistic perspectives on emotions in an interdisciplinary manner, aiming to advance the understanding of human emotions and their neural correlates.

The language void: the need for multimodality in primate communication research

Theories of language evolution often draw heavily on comparative evidence of the communicative abilities of extant nonhuman primates (primates). Many theories have argued exclusively for a unimodal origin of language, usually gestural or vocal. Theories are often strengthened by research on primates that indicates the absence of certain linguistic precursors in the opposing communicative modality. However, a systematic review of the primate communication literature reveals that vocal, gestural and facial signals have attracted differing theoretical and methodological approaches, rendering cross-modal comparisons problematic. The validity of the theories based on such comparisons can therefore be questioned. We propose that these a priori biases, inherent in unimodal research, highlight the need for integrated multimodal research. By examining communicative signals in concert we can both avoid methodological discontinuities as well as better understand the phylogenetic precursors to human language as part of a multimodal system.

Focus on the essential: all great apes know when others are being attentive

When begging for food, all great ape species are sensitive to a human’s attention. However, studies investigating which cues are relevant for chimpanzees to assess the attentional state of others have produced highly inconsistent results. Some have suggested chimpanzees differentiate attention based on the status of the face or even the eyes, while others have indicated that body posture alone is the relevant cue. Kaminski et al. (Anim Cogn 7:216–223, 2004) compared the behaviour of chimpanzees, bonobos and orangutans while begging for food from a human experimenter who systematically varied his face and body orientation. Their results indicated that both factors, face and body orientation, affect apes’ begging behaviour. The authors claimed that while body orientation provides information about the experimenter’s general disposition to offer food, the visibility of the face provides information about the human’s attentional state. In the current study, we tested this hypothesis with all four great apes species. However, unlike Kaminski et al. (Anim Cogn 7:216–223, 2004), the experimenter was able to hand over food regardless of body orientation. The results show that as soon as the offering of the food was no longer restricted, the orientation of the face became the key factor. Therefore, we present the first evidence that all great ape species are able to assess the attentional state of a recipient based on the orientation of the face.

GibbonFACS: a muscle-based facial movement coding system for hylobatids

The evolution and function of human and nonhuman primate facial expression can be better understood through multispecies comparative analyses. Anatomically based coding systems (Facial Action Coding Systems [FACS]) are developed to enable such analyses because they are standardized and systematic and aid identification of homologous expressions underpinned by similar muscle contractions. To date, FACS has been developed for humans, and subsequently modified for chimpanzees and rhesus macaques. Through detailed examination of facial anatomy and spontaneous movement, here we present a FACS for hylobatids (gibbons and siamangs): apes living in small groups and often thought not to display extensive facial movement. We identified and described 18 independent facial movements (Action Units and Action Descriptors) in the hylobatid face, and compared to humans, chimpanzees, and rhesus macaques. The findings show that the facial movement capacity of hylobatids bears great similarity to species living in much larger groups. The findings could be explained by phylogenetic inertia (especially because pair-bonding is likely to have emerged from social living) and/or the social demands of pair-bonding.

Exorcising Grice's ghost: an empirical approach to studying intentional communication in animals

Languages intentional nature has been highlighted as a crucial feature distinguishing it from other communication systems. Specifically, language is often thought to depend on highly structured intentional action and mutual mindreading by a communicator and recipient. Whilst similar abilities in animals can shed light on the evolution of intentionality, they remain challenging to detect unambiguously. We revisit animal intentional communication and suggest that progress in identifying analogous capacities has been complicated by (i) the assumption that intentional (that is, voluntary) production of communicative acts requires mental‐state attribution, and (ii) variation in approaches investigating communication across sensory modalities. To move forward, we argue that a framework fusing research across modalities and species is required. We structure intentional communication into a series of requirements, each of which can be operationalised, investigated empirically, and must be met for purposive, intentionally communicative acts to be demonstrated. Our unified approach helps elucidate the distribution of animal intentional communication and subsequently serves to clarify what is meant by attributions of intentional communication in animals and humans.

Pseudoreplication : a widespread problem in primate communication research

Pseudoreplication (the pooling fallacy) is a widely acknowledged statistical error in the behavioural sciences. Taking a large number of data points from a small number of animals creates a false impression of a better representation of the population. Studies of communication may be particularly prone to artificially inflating the data set in this way, as the unit of interest (the facial expression, the call or the gesture) is a tempting unit of analysis. Primate communication studies (551) published in scientific journals from 1960 to 2008 were examined for the simplest form of pseudoreplication (taking more than one data point from each individual). Of the studies that used inferential statistics, 38% presented at least one case of pseudoreplicated data. An additional 16% did not provide enough information to rule out pseudoreplication. Generalized linear mixed models determined that one variable significantly increased the likelihood of pseudoreplication: using observational methods. Actual sample size (number of animals) and year of publication were not associated with pseudoreplication. The high prevalence of pseudoreplication in the primate communication research articles, and the fact that there has been no decline since key papers warned against pseudoreplication, demonstrates that the problem needs to be more actively addressed.

Evolution of the Muscles of Facial Expression in a Monogamous Ape: Evaluating the Relative Influences of Ecological and Phylogenetic Factors in Hylobatids

Facial expression is a communication mode produced by facial (mimetic) musculature. Hylobatids (gibbons and siamangs) have a poorly documented facial display repertoire and little is known about their facial musculature. These lesser apes represent an opportunity to test hypotheses related to the evolution of primate facial musculature as they are the only hominoid with a monogamous social structure, and thus live in very small groups. Primate species living in large groups with numerous social relationships, such as chimpanzees and rhesus macaques, have been shown to have a complex facial display repertoire and a high number of discrete facial muscles. The present study was designed to examine the relative influence of social structure and phylogeny on facial musculature evolution by comparing facial musculature complexity among hylobatids, chimpanzees, and rhesus macaques. Four faces were dissected from four hylobatid species. Morphology, attachments, three‐dimensional relationships, and variation among specimens were noted and compared to rhesus macaques and chimpanzees. Microanatomical characteristics of the orbicularis oris muscle were also compared. Facial muscles of hylobatids were generally gracile and less complex than both the rhesus macaque and chimpanzee. Microanatomically, the orbicularis oris muscle of hylobatids was relatively loosely packed with muscle fibers. These results indicate that environmental and social factors may have been important in determining morphology and complexity of facial musculature in the less social hylobatids and that they may not have experienced as strong selection pressure for mimetic muscle complexity as other, more social primates. Anat Rec, 294:645–663, 2011.

Does Sympathy Motivate Prosocial Behaviour in Great Apes

Prosocial behaviours such as helping, comforting, or sharing are central to human social life. Because they emerge early in ontogeny, it has been proposed that humans are prosocial by nature and that from early on empathy and sympathy motivate such behaviours. The emerging question is whether humans share these abilities to feel with and for someone with our closest relatives, the great apes. Although several studies demonstrated that great apes help others, little is known about their underlying motivations. This study addresses this issue and investigates whether four species of great apes (Pongo pygmaeus, Gorilla gorilla, Pan troglodytes, Pan paniscus) help a conspecific more after observing the conspecific being harmed (a human experimenter steals the conspecific’s food) compared to a condition where no harming occurred. Results showed that in regard to the occurrence of prosocial behaviours, only orangutans, but not the African great apes, help others when help is needed, contrasting prior findings on chimpanzees. However, with the exception of one population of orangutans that helped significantly more after a conspecific was harmed than when no harm occurred, prosocial behaviour in great apes was not motivated by concern for others.

Gibbons (Hylobates pileatus, H. moloch, H. lar, Symphalangus syndactylus) follow human gaze, but do not take the visual perspective of others

We investigated four gibbon species of two different genera (Hylobates pileatus, H. moloch, H. lar, Symphalangus syndactylus) in terms of their looking behavior in response to a human who either looked up or looked at the gibbon. Comparing those two conditions, gibbons as a group looked up more when the human was looking up, but they also performed more looks in other directions and thus generally looked more in this condition. Unlike great apes, gibbons did not respond differently between conditions when only the first look on every trial was considered. Furthermore, they did not perform double looks up to check where the human was looking and also did not habituate to the human’s looks up. This suggests that gibbons co-orient with human gaze, but unlike great apes, they do not take the visual perspective of others.