Bridget M. Waller

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.

Selection for universal facial emotion

Facial expression is heralded as a communication system common to all human populations, and thus is generally accepted as a biologically based, universal behavior. Happiness, sadness, fear, anger, surprise, and disgust are universally recognized and produced emotions, and communication of these states is deemed essential in order to navigate the social environment. It is puzzling, however, how individuals are capable of producing similar facial expressions when facial musculature is known to vary greatly among individuals. Here, the authors show that although some facial muscles are not present in all individuals, and often exhibit great asymmetry (larger or absent on one side), the facial muscles that are essential in order to produce the universal facial expressions exhibited 100% occurrence and showed minimal gross asymmetry in 18 cadavers. This explains how universal facial expression production is achieved, implies that facial muscles have been selected for essential nonverbal communicative function, and yet also accommodate individual variation.

Classifying Chimpanzee Facial Expressions Using Muscle Action

The Chimpanzee Facial Action Coding System (ChimpFACS) is an objective, standardized observational tool for measuring facial movement in chimpanzees based on the well-known human Facial Action Coding System (FACS; P. Ekman & W. V. Friesen, 1978). This tool enables direct structural comparisons of facial expressions between humans and chimpanzees in terms of their common underlying musculature. Here the authors provide data on the first application of the ChimpFACS to validate existing categories of chimpanzee facial expressions using discriminant functions analyses. The ChimpFACS validated most existing expression categories (6 of 9) and, where the predicted group memberships were poor, the authors discuss potential problems with ChimpFACS and/or existing categorizations. The authors also report the prototypical movement configurations associated with these 6 expression categories. For all expressions, unique combinations of muscle movements were identified, and these are illustrated as peak intensity prototypical expression configurations. Finally, the authors suggest a potential homology between these prototypical chimpanzee expressions and human expressions based on structural similarities. These results contribute to our understanding of the evolution of emotional communication by suggesting several structural homologies between the facial expressions of chimpanzees and humans and facilitating future research.

Brief communication: MaqFACS: A muscle-based facial movement coding system for the rhesus macaque.

Over 125 years ago, Charles Darwin (1872) suggested that the only way to fully understand the form and function of human facial expression was to make comparisons with other species. Nevertheless, it has been only recently that facial expressions in humans and related primate species have been compared using systematic, anatomically based techniques. Through this approach, large-scale evolutionary and phylogenetic analyses of facial expressions, including their homology, can now be addressed. Here, the development of a muscular-based system for measuring facial movement in rhesus macaques (Macaca mulatta) is described based on the well-known FACS (Facial Action Coding System) and ChimpFACS. These systems describe facial movement according to the action of the underlying facial musculature, which is highly conserved across primates. The coding systems are standardized; thus, their use is comparable across laboratories and study populations. In the development of MaqFACS, several species differences in the facial movement repertoire of rhesus macaques were observed in comparison with chimpanzees and humans, particularly with regard to brow movements, puckering of the lips, and ear movements. These differences do not seem to be the result of constraints imposed by morphological differences in the facial structure of these three species. It is more likely that they reflect unique specializations in the communicative repertoire of each species.

Understanding chimpanzee facial expression: insights into the evolution of communication

To understand the evolution of emotional communication, comparative research on facial expression similarities between humans and related species is essential. Chimpanzees display a complex, flexible facial expression repertoire with many physical and functional similarities to humans. This paper reviews what is known about these facial expression repertoires, discusses the importance of social organization in understanding the meaning of different expressions, and introduces a new coding system, the ChimpFACS, and describes how it can be used to determine homologies between human and chimpanzee facial expressions. Finally, it reviews previous studies on the categorization of facial expressions by chimpanzees using computerized tasks, and discusses the importance of configural processing for this skill in both humans and chimpanzees. Future directions for understanding the evolution of emotional communication will include studies on the social function of facial expressions in ongoing social interactions, the development of facial expression communication and more studies that examine the perception of these important social signals.

Intramuscular Electrical Stimulation of Facial Muscles in Humans and Chimpanzees: Duchenne Revisited and Extended

The pioneering work of Duchenne (1862/1990) was replicated in humans using intramuscular electrical stimulation and extended to another species (Pan troglodytes: chimpanzees) to facilitate comparative facial expression research. Intramuscular electrical stimulation, in contrast to the original surface stimulation, offers the opportunity to activate individual muscles as opposed to groups of muscles. In humans, stimulation resulted in appearance changes in line with Facial Action Coding System (FACS) action units (AUs), and chimpanzee facial musculature displayed functional similarity to human facial musculature. The present results provide objective identification of the muscle substrate of human and chimpanzee facial expressions- data that will be useful in providing a common language to compare the units of human and chimpanzee facial expression.

Facial expression categorization by chimpanzees using standardized stimuli

The ability to recognize and accurately interpret facial expressions are critical social cognition skills in primates, yet very few studies have examined how primates discriminate these social signals and which features are the most salient. Four experiments examined chimpanzee facial expression processing using a set of standardized, prototypical stimuli created using the new ChimpFACS coding system. First, chimpanzees were found to accurately discriminate between these expressions using a computerized matching-to-sample task, and recognition was impaired for all but one expression category when they were inverted. Third, a multidimensional scaling analysis examined the perceived dissimilarity among these facial expressions revealing 2 main dimensions, the degree of mouth closure and extent of lip-puckering and retraction. Finally, subjects were asked to match each facial expression category using only individual component features. For each expression category, at least 1 component movement was more salient or representative of that expression than the others. However, these were not necessarily the only movements implicated in subjects overall pattern of errors. Therefore, similar to humans, both configuration and component movements are important during chimpanzee facial expression processing.

Facial Expression in Nonhuman Animals

Many nonhuman animals produce facial expressions which sometimes bear clear resemblance to the facial expressions seen in humans. An understanding of this evolutionary continuity between species, and how this relates to social and ecological variables, can help elucidate the meaning, function, and evolution of facial expression. This aim, however, requires researchers to overcome the theoretical and methodological differences in how human and nonhuman facial expressions are approached. Here, we review the literature relating to nonhuman facial expressions and suggest future directions that could facilitate a better understanding of facial expression within an evolutionary context.

Paedomorphic Facial Expressions Give Dogs a Selective Advantage

How wolves were first domesticated is unknown. One hypothesis suggests that wolves underwent a process of self-domestication by tolerating human presence and taking advantage of scavenging possibilities. The puppy-like physical and behavioural traits seen in dogs are thought to have evolved later, as a byproduct of selection against aggression. Using speed of selection from rehoming shelters as a proxy for artificial selection, we tested whether paedomorphic features give dogs a selective advantage in their current environment. Dogs who exhibited facial expressions that enhance their neonatal appearance were preferentially selected by humans. Thus, early domestication of wolves may have occurred not only as wolf populations became tamer, but also as they exploited human preferences for paedomorphic characteristics. These findings, therefore, add to our understanding of early dog domestication as a complex co-evolutionary process.

Facial musculature in the rhesus macaque (Macaca mulatta): evolutionary and functional contexts with comparisons to chimpanzees and humans

Facial expression is a common mode of visual communication in mammals but especially so in primates. Rhesus macaques (Macaca mulatta) have a well‐documented facial expression repertoire that is controlled by the facial/mimetic musculature as in all mammals. However, little is known about the musculature itself and how it compares with those of other primates. Here we present a detailed description of the facial musculature in rhesus macaques in behavioral, evolutionary and comparative contexts. Formalin‐fixed faces from six adult male specimens were dissected using a novel technique. The morphology, attachments, three‐dimensional relationships and variability of muscles were noted and compared with chimpanzees (Pan troglodytes) and with humans. The results showed that there was a greater number of facial muscles in rhesus macaques than previously described (24 muscles), including variably present (and previously unmentioned) zygomaticus minor, levator labii superioris alaeque nasi, depressor septi, anterior auricularis, inferior auricularis and depressor supercilii muscles. The facial muscles of the rhesus macaque were very similar to those in chimpanzees and humans but M. mulatta did not possess a risorius muscle. These results support previous studies that describe a highly graded and intricate facial expression repertoire in rhesus macaques. Furthermore, these results indicate that phylogenetic position is not the primary factor governing the structure of primate facial musculature and that other factors such as social behavior are probably more important. The results from the present study may provide valuable input to both biomedical studies that use rhesus macaques as a model for human disease and disorder that includes assessment of facial movement and studies into the evolution of primate societies and communication.