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.

Mapping the contribution of single muscles to facial movements in the rhesus macaque.

The rhesus macaque (Macaca mulatta) is the most utilized primate model in the biomedical and psychological sciences. Expressive behavior is of interest to scientists studying these animals, both as a direct variable (modeling neuropsychiatric disease, where expressivity is a primary deficit), as an indirect measure of health and welfare, and also in order to understand the evolution of communication. Here, intramuscular electrical stimulation of facial muscles was conducted in the rhesus macaque in order to document the relative contribution of each muscle to the range of facial movements and to compare the expressive function of homologous muscles in humans, chimpanzees and macaques. Despite published accounts that monkeys possess less differentiated and less complex facial musculature, the majority of muscles previously identified in humans and chimpanzees were stimulated successfully in the rhesus macaque and caused similar appearance changes. These observations suggest that the facial muscular apparatus of the monkey has extensive homology to the human face. The muscles of the human face, therefore, do not represent a significant evolutionary departure from those of a monkey species. Thus, facial expressions can be compared between humans and rhesus macaques at the level of the facial musculature, facilitating the systematic investigation of comparative facial communication.

Rearing experience differentially affects somatic and cardiac startle responses in rhesus monkeys (Macaca mulatta).

The present study reports, for the first time, somatic and cardiac responses to acoustic startle in 2 groups of rhesus monkeys (Macaca mulatta) with different rearing experiences. Both groups showed a significant direct relationship between startle amplitude and the intensity of the acoustic startle stimulus (80-120 dB) and rapid heart rate acceleration after a 120-dB stimulus. Monkeys reared with a same-age peer (PR) showed higher startle amplitudes than those reared with their mothers (MR), consistent with rearing effects in rodents. The MR monkeys, however, showed faster heart rate acceleration of greater overall magnitude than that of the PR group. The results are discussed with regard to a monkey model for neuropsychiatric disease.

Cognitive and physiological markers of emotional awareness in chimpanzees (Pan troglodytes).

The ability to understand emotion in others is one of the most important factors involved in regulating social interactions in primates. Such emotional awareness functions to coordinate activity among group members, enable the formation of long-lasting individual relationships, and facilitate the pursuit of shared interests. Despite these important evolutionary implications, comparative studies of emotional processing in humans and great apes are practically nonexistent, constituting a major gap in our understanding of the extent to which emotional awareness has played an important role in shaping human behavior and societies. This paper presents the results of two experiments that examine chimpanzees' responses to emotional stimuli. First, changes in peripheral skin temperature were measured while subjects viewed three categories of emotionally negative video scenes; conspecifics being injected with needles (INJ), darts and needles alone (DART), and conspecific directing agonism towards the veterinarians (CHASE). Second, chimpanzees were required to use facial expressions to categorize emotional video scenes, i.e., favorite food and objects and veterinarian procedures, according to their positive and negative valence. With no prior training, subjects spontaneously matched the emotional videos to conspecific facial expressions according to their shared emotional meaning, indicating that chimpanzee facial expressions are processed emotionally, as are human expressions. Decreases in peripheral skin temperature, indicative of negative sympathetic arousal, were significantly lower when subjects viewed the INJ and DART videos, compared to the CHASE videos, indicating greater negative arousal when viewing conspecifics being injected with needles, and needles themselves, than when viewing conspecifics engaged in general agonism.

Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta).

Faces are one of the most salient classes of stimuli involved in social communication. Three experiments compared face-recognition abilities in chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). In the face-matching task, the chimpanzees matched identical photographs of conspecifics' faces on Trial 1, and the rhesus monkeys did the same after 4 generalization trials. In the individual-recognition task, the chimpanzees matched 2 different photographs of the same individual after 2 trials, and the rhesus monkeys generalized in fewer than 6 trials. The feature-masking task showed that the eyes were the most important cue for individual recognition. Thus, chimpanzees and rhesus monkeys are able to use facial cues to discriminate unfamiliar conspecifics. Although the rhesus monkeys required many trials to learn the tasks, this is not evidence that faces are not as important social stimuli for them as for the chimpanzees.

Brain temperature asymmetries and emotional perception in chimpanzees, Pan troglodytes.

The lateralization of emotion has received a great deal of attention over the last few decades, resulting in two main theories. The Right Hemisphere Theory states that the right hemisphere is primarily responsible for emotional processes, while the Valence Theory suggests that the right hemisphere regulates negative emotion and the left hemisphere regulates positive emotion. Despite the important implications of these theories for the evolution of emotion processes, few studies have attempted to assess the lateralization of emotion in non-human primates. This study uses the novel technique of measuring tympanic membrane temperature (Tty) to assess asymmetries in the perception of emotional stimuli in chimpanzees. The tympanic membrane is an indirect, but reliable, site from which to measure brain temperature, and is strongly influenced by autonomic and behavioral activity. Six chimpanzees were shown positive, neutral, and negative emotional videos depicting scenes of play, scenery, and severe aggression, respectively. During the negative emotion condition, right Tty was significantly higher than the baseline temperature. This effect was relatively stable, long lasting, and consistent across subjects. Temperatures did not change significantly from baseline in the neutral or positive emotion condition, although a significant number of measurements showed increased left Tty during the neutral emotion condition. These data suggest that viewing emotional stimuli results in asymmetrical changes in brain temperature, in particular increased right Tty during the negative emotion condition, evidence of emotional arousal in chimpanzees, and in providing partial support of both the Right Hemisphere and Valence Theories of emotional lateralization in our closest living ancestor.

Why faces may be special: evidence of the inversion effect in chimpanzees.

Five chimpanzees were tested on their ability to discriminate faces and automobiles presented in both their upright and inverted orientations. The face stimuli consisted of 30 black and white photographs, 10 each of unfamiliar chimpanzees (Pan troblodytes), brown capuchins (Cebus apella), and humans (Homo sapiens). Ten black and white photographs of automobiles were also used. The stimuli were presented in a sequential matching-to-sample (SMTS) format using a computerized joystick-testing apparatus. Subjects performed better on upright than inverted stimuli in all classes. Performance was significantly better on upright than inverted presentations of chimpanzee and human faces but not on capuchin monkey faces or automobiles. These data support previous studies in humans that suggest the inversion effect occurs for stimuli for which subjects have developed an expertise. Alternative explanations for the inversion effect based on the type of spatial frequency contained in the stimuli are also discussed. These data are the first to provide evidence for the inversion effect using several classes of face stimuli in a great ape species.

Haptic discrimination in capuchin monkeys (Cebus apella): evidence of manual specialization.

Two experiments investigated the effects of haptic and visual discrimination on hand preference in 22 brown capuchin monkeys (Cebus apella). The percentage of left-handed subjects in Experiment 1 were 63.6%, 45.5%, and 18.2% for haptic, bipedal, and quadrupedal reaching, respectively. In Experiment 2, the haptic demands of the task were manipulated by using additional food types and another tactile medium. Left-hand preferences were further strengthened when reaching into water compared to pineshavings in Experiment 1. Reaching with no tactile interference resulted in equal numbers of lateralized and nonlateralized subjects. These results show that when reaching demands the use of haptic cues, as opposed to visual ones, monkeys shift towards greater left hand use. This is consistent with what is known about right hemisphere superiority for haptic discrimination in humans.