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1.  Human Faces Are Slower than Chimpanzee Faces 
PLoS ONE  2014;9(10):e110523.
Background
While humans (like other primates) communicate with facial expressions, the evolution of speech added a new function to the facial muscles (facial expression muscles). The evolution of speech required the development of a coordinated action between visual (movement of the lips) and auditory signals in a rhythmic fashion to produce “visemes” (visual movements of the lips that correspond to specific sounds). Visemes depend upon facial muscles to regulate shape of the lips, which themselves act as speech articulators. This movement necessitates a more controlled, sustained muscle contraction than that produced during spontaneous facial expressions which occur rapidly and last only a short period of time. Recently, it was found that human tongue musculature contains a higher proportion of slow-twitch myosin fibers than in rhesus macaques, which is related to the slower, more controlled movements of the human tongue in the production of speech. Are there similar unique, evolutionary physiologic biases found in human facial musculature related to the evolution of speech?
Methodology/Prinicipal Findings
Using myosin immunohistochemistry, we tested the hypothesis that human facial musculature has a higher percentage of slow-twitch myosin fibers relative to chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). We sampled the orbicularis oris and zygomaticus major muscles from three cadavers of each species and compared proportions of fiber-types. Results confirmed our hypothesis: humans had the highest proportion of slow-twitch myosin fibers while chimpanzees had the highest proportion of fast-twitch fibers.
Conclusions/significance
These findings demonstrate that the human face is slower than that of rhesus macaques and our closest living relative, the chimpanzee. They also support the assertion that human facial musculature and speech co-evolved. Further, these results suggest a unique set of evolutionary selective pressures on human facial musculature to slow down while the function of this muscle group diverged from that of other primates.
doi:10.1371/journal.pone.0110523
PMCID: PMC4206419  PMID: 25338058
2.  Intranasal Oxytocin Selectively Attenuates Rhesus Monkeys’ Attention to Negative Facial Expressions 
Psychoneuroendocrinology  2013;38(9):1748-1756.
Intranasal oxytocin (IN-OT) modulates social perception and cognition in humans and could be an effective pharmacotherapy for treating social impairments associated with neuropsychiatric disorders, like autism. However, it is unknown how IN-OT modulates social cognition, its effect after repeated use, or its impact on the developing brain. Animal models are urgently needed. This study examined the effect of IN-OT on social perception in monkeys using tasks that reveal some of the social impairments seen in autism. Six rhesus macaques (Macaca mulatta, 4 males) received a 48 IU dose of OT or saline placebo using a pediatric nebulizer. An hour later, they performed a computerized task (the dot-probe task) to measure their attentional bias to social, emotional, and nonsocial images. Results showed that IN-OT significantly reduced monkeys’ attention to negative facial expressions, but not neutral faces or clip art images and, additionally, showed a trend to enhance monkeys’ attention to direct versus averted gaze faces. This study is the first to demonstrate an effect of IN-OT on social perception in monkeys, IN-OT selectively reduced monkey’s attention to negative facial expressions, but not neutral social or nonsocial images. These findings complement several reports in humans showing that IN-OT reduces the aversive quality of social images suggesting that, like humans, monkey social perception is mediated by the oxytocinergic system. Importantly, these results in monkeys suggest that IN-OT does not dampen the emotional salience of social stimuli, but rather acts to affect the evaluation of emotional images during the early stages of information processing.
doi:10.1016/j.psyneuen.2013.02.011
PMCID: PMC3743934  PMID: 23490074
Oxytocin; attention; gaze; facial expression; social cognition; autism
3.  Process Versus Product in Social Learning: Comparative Diffusion Tensor Imaging of Neural Systems for Action Execution–Observation Matching in Macaques, Chimpanzees, and Humans 
Cerebral Cortex (New York, NY)  2012;23(5):1014-1024.
Social learning varies among primate species. Macaques only copy the product of observed actions, or emulate, while humans and chimpanzees also copy the process, or imitate. In humans, imitation is linked to the mirror system. Here we compare mirror system connectivity across these species using diffusion tensor imaging. In macaques and chimpanzees, the preponderance of this circuitry consists of frontal–temporal connections via the extreme/external capsules. In contrast, humans have more substantial temporal–parietal and frontal–parietal connections via the middle/inferior longitudinal fasciculi and the third branch of the superior longitudinal fasciculus. In chimpanzees and humans, but not in macaques, this circuitry includes connections with inferior temporal cortex. In humans alone, connections with superior parietal cortex were also detected. We suggest a model linking species differences in mirror system connectivity and responsivity with species differences in behavior, including adaptations for imitation and social learning of tool use.
doi:10.1093/cercor/bhs097
PMCID: PMC3615349  PMID: 22539611
diffusion tensor imaging; evolution; imitation; mirror system; social learning
4.  Differences in Neural Activation for Object-Directed Grasping in Chimpanzees and Humans 
The Journal of Neuroscience  2013;33(35):14117-14134.
The human faculty for object-mediated action, including tool use and imitation, exceeds that of even our closest primate relatives and is a key foundation of human cognitive and cultural uniqueness. In humans and macaques, observing object-directed grasping actions activates a network of frontal, parietal, and occipitotemporal brain regions, but differences in human and macaque activation suggest that this system has been a focus of selection in the primate lineage. To study the evolution of this system, we performed functional neuroimaging in humans' closest living relatives, chimpanzees. We compare activations during performance of an object-directed manual grasping action, observation of the same action, and observation of a mimed version of the action that consisted of only movements without results. Performance and observation of the same action activated a distributed frontoparietal network similar to that reported in macaques and humans. Like humans and unlike macaques, these regions were also activated by observing movements without results. However, in a direct chimpanzee/human comparison, we also identified unique aspects of human neural responses to observed grasping. Chimpanzee activation showed a prefrontal bias, including significantly more activity in ventrolateral prefrontal cortex, whereas human activation was more evenly distributed across more posterior regions, including significantly more activation in ventral premotor cortex, inferior parietal cortex, and inferotemporal cortex. This indicates a more “bottom-up” representation of observed action in the human brain and suggests that the evolution of tool use, social learning, and cumulative culture may have involved modifications of frontoparietal interactions.
doi:10.1523/JNEUROSCI.2172-13.2013
PMCID: PMC3756757  PMID: 23986247
5.  Validation of a field technique and characterization of fecal glucocorticoid metabolite analysis in wild chimpanzees (Pan troglodytes) 
Monitoring adrenocortical activity in wild primate populations is critical, given the well-documented relationship between stress, health and reproduction. Although many primate studies have quantified fecal glucocorticoid metabolite (FGM) concentrations, it is imperative that researchers validate their method for each species. Here, we describe and validate a technique for field extraction and storage of FGMs in wild chimpanzees (Pan troglodytes). Our method circumvents many of the logistical challenges associated with field studies while yielding similar results to a commonly-used laboratory method. We further validate that our method accurately reflects stress physiology using an ACTH challenge in a captive chimpanzee and a FGM peak at parturition in a wild subject. Finally, we quantify circadian patterns for FGMs for the first time in this species. Understanding these patterns may allow researchers to directly link specific events with the stress response.
doi:10.1002/ajp.22078
PMCID: PMC3619224  PMID: 22968979
chimpanzee; fecal glucocorticoid metabolites; field methods; ACTH; parturition; circadian rhythm
6.  The organization of conspecific face space in nonhuman primates 
Humans and chimpanzees demonstrate numerous cognitive specializations for processing faces, but comparative studies with monkeys suggest that these may be the result of recent evolutionary adaptations. The present study utilized the novel approach of face space, a powerful theoretical framework used to understand the representation of face identity in humans, to further explore species differences in face processing. According to the theory, faces are represented by vectors in a multidimensional space, the centre of which is defined by an average face. Each dimension codes features important for describing a face’s identity, and vector length codes the feature’s distinctiveness. Chimpanzees and rhesus monkeys discriminated male and female conspecifics’ faces, rated by humans for their distinctiveness, using a computerized task. Multidimensional scaling analyses showed that the organization of face space was similar between humans and chimpanzees. Distinctive faces had the longest vectors and were the easiest for chimpanzees to discriminate. In contrast, distinctiveness did not correlate with the performance of rhesus monkeys. The feature dimensions for each species’ face space were visualized and described using morphing techniques. These results confirm species differences in the perceptual representation of conspecific faces, which are discussed within an evolutionary framework.
doi:10.1080/17470218.2012.693110
PMCID: PMC3544001  PMID: 22670823
Face space; Multidimensional scaling; Face identity; Rhesus monkey; Chimpanzee; Species differences
7.  Early life stress affects cerebral glucose metabolism in adult rhesus monkeys (Macaca mulatta) 
Early life stress (ELS) is a risk factor for anxiety, mood disorders and alterations in stress responses. Less is known about the long-term neurobiological impact of ELS. We used [18F]-fluorodeoxyglucose Positron Emission Tomography (FDG-PET) to assess neural responses to a moderate stress test in adult monkeys that experienced ELS as infants. Both groups of monkeys showed hypothalamic-pituitary-adrenal (HPA) axis stress-induced activations and cardiac arousal in response to the stressor. A whole brain analysis detected significantly greater regional cerebral glucose metabolism (rCGM) in superior temporal sulcus, putamen, thalamus, and inferotemporal cortex of ELS animals compared to controls. Region of interest (ROI) analyses performed in areas identified as vulnerable to ELS showed greater activity in the orbitofrontal cortex of ELS compared to control monkeys, but greater hippocampal activity in the control compared to ELS monkeys. Together, these results suggest hyperactivity in emotional and sensory processing regions of adult monkeys with ELS, and greater activity in stress-regulatory areas in the controls. Despite these neural responses, no group differences were detected in neuroendocrine, autonomic or behavioral responses, except for a trend towards increased stillness in the ELS monkeys. Together, these data suggest hypervigilance in the ELS monkeys in the absence of immediate danger.
doi:10.1016/j.dcn.2011.09.003
PMCID: PMC3372874  PMID: 22682736
Early life stress; rearing; HPA axis; monkey; PET; social brain
8.  The perception of two-tone Mooney faces in chimpanzees (Pan troglodytes) 
Cognitive neuroscience  2011;3(1):21-28.
Neurological experiments have revealed a complex network of areas in the human brain that respond more to faces than to other categories of objects and thus have been implemented in face categorization. The aim of this study was to investigate whether chimpanzees (N = 5), our closest living relatives, detect and categorize faces on the basis of first-order information. Further, whether this sensitivity is specific to faces or generalizes to other objects. In service to this aim, we created multiple categories of two-tone ‘Mooney’ objects (chimpanzee faces, shoes, human hands) because, by maximizing contrast, the Mooney transformation selectively degrades second-order information (the basis for individual discrimination in humans), leaving only first-order information intact. Two experiments were carried out using a 2AFC MTS procedure. The first experiment providing strong evidence that, like humans, chimpanzees categorize Mooney faces as faces. However, without second-order information, the chimpanzees could not match Mooney faces at the individual-level. In Experiment 2 four of the five chimpanzees found it easier to categorize Mooney faces than Mooney shoes. Neurological evidence strongly implicates a dedicated neural mechanism for face categorization in the human brain and our data suggest that chimpanzees share this level of specialization.
doi:10.1080/17588928.2011.578737
PMCID: PMC3377185  PMID: 22737182
9.  The inversion effect reveals species differences in face processing 
Acta psychologica  2011;138(1):204-210.
Face recognition is a complex skill that requires the integration of facial features across the whole face, e.g., holistic processing. It is unclear whether, and to what extent, other species process faces in a manner that is similar to humans. Previous studies on the inversion effect, a marker of holistic processing, in nonhuman primates have revealed mixed results in part because many studies have failed to include alternative image categories necessary to understand whether the effects are truly face-specific. The present study re-examined the inversion effect in rhesus monkeys and chimpanzees using comparable testing methods and a variety of high quality stimuli including faces and nonfaces. The data support an inversion effect in chimpanzees only for conspecifics’ faces (expert category), suggesting face-specific holistic processing similar to humans. Rhesus monkeys showed inversion effects for conspecifics, but also for heterospecifics’ faces (chimpanzees), and nonfaces images (houses), supporting important species differences in this simple test of holistic face processing.
doi:10.1016/j.actpsy.2011.06.005
PMCID: PMC3208376  PMID: 21784381
face recognition; inversion effect; holistic processing; matching-to-sample; comparative
10.  The importance of surface-based cues for face discrimination in non-human primates 
Understanding how individual identity is processed from faces remains a complex problem. Contrast reversal, showing faces in photographic negative, impairs face recognition in humans and demonstrates the importance of surface-based information (shading and pigmentation) in face recognition. We tested the importance of contrast information for face encoding in chimpanzees and rhesus monkeys using a computerized face-matching task. Results showed that contrast reversal (positive to negative) selectively impaired face processing in these two species, although the impairment was greater for chimpanzees. Unlike chimpanzees, however, monkeys performed just as well matching negative to positive faces, suggesting that they retained some ability to extract identity information from negative faces. A control task showed that chimpanzees, but not rhesus monkeys, performed significantly better matching face parts compared with whole faces after a contrast reversal, suggesting that contrast reversal acts selectively on face processing, rather than general visual-processing mechanisms. These results confirm the importance of surface-based cues for face processing in chimpanzees and humans, while the results were less salient for rhesus monkeys. These findings make a significant contribution to understanding the evolution of cognitive specializations for face processing among primates, and suggest potential differences between monkeys and apes.
doi:10.1098/rspb.2010.2333
PMCID: PMC3107657  PMID: 21123266
face recognition; contrast reversal; configuration; chimpanzee; rhesus monkey; evolution
11.  Effect of familiarity and viewpoint on face recognition in chimpanzees 
Perception  2011;40(7):863-872.
Numerous studies have shown that familiarity strongly influences how well humans recognize faces. This is particularly true when faces are encountered across a change in viewpoint. In this situation, recognition may be accomplished by matching partial or incomplete information about a face to a stored representation of the known individual, whereas such representations are not available for unknown faces. Chimpanzees, our closest living relatives, share many of the same behavioral specializations for face processing as humans, but the influence of familiarity and viewpoint have never been compared in the same study. Here, we examined the ability of chimpanzees to match the faces of familiar and unfamiliar conspecifics in their frontal and 3/4 views using a computerized task. Results showed that, while chimpanzees were able to accurately match both familiar and unfamiliar faces in their frontal orientations, performance was significantly impaired only when unfamiliar faces were presented across a change in viewpoint. Therefore, like in humans, face processing in chimpanzees appears to be sensitive to individual familiarity. We propose that familiarization is a robust mechanism for strengthening the representation of faces and has been conserved in primates to achieve efficient individual recognition over a range of natural viewing conditions.
PMCID: PMC3342667  PMID: 22128558
12.  Geometric distortions affect face recognition in chimpanzees (Pan troglodytes) and monkeys (Macaca mulatta) 
Animal cognition  2010;14(1):35-43.
All primates can recognize faces and do so by analyzing the subtle variation that exists between faces. Through a series of three experiments, we attempted to clarify the nature of second-order information processing in nonhuman primates. Experiment one showed that both chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta) tolerate geometric distortions along the vertical axis, suggesting that information about absolute position of features does not contribute to accurate face recognition. Chimpanzees differed from monkeys, however, in that they were more sensitive to distortions along the horizontal axis, suggesting that when building a global representation of facial identity, horizontal relations between features are more diagnostic of identity than vertical relations. Two further experiments were performed to determine whether the monkeys were simply less sensitive to horizontal relations compared to chimpanzees or were instead relying on local features. The results of these experiments confirm that monkeys can utilize a holistic strategy when discriminating between faces regardless of familiarity. In contrast, our data show that chimpanzees, like humans, use a combination of holistic and local features when the faces are unfamiliar, but primarily holistic information when the faces become familiar. We argue that our comparative approach to the study of face recognition reveals the impact that individual experience and social organization has on visual cognition.
doi:10.1007/s10071-010-0341-x
PMCID: PMC3014412  PMID: 20632050
Visual cognition; Comparative psychology; Face perception; Face recognition
13.  The evolution of face processing in primates 
The ability to recognize faces is an important socio-cognitive skill that is associated with a number of cognitive specializations in humans. While numerous studies have examined the presence of these specializations in non-human primates, species where face recognition would confer distinct advantages in social situations, results have been mixed. The majority of studies in chimpanzees support homologous face-processing mechanisms with humans, but results from monkey studies appear largely dependent on the type of testing methods used. Studies that employ passive viewing paradigms, like the visual paired comparison task, report evidence of similarities between monkeys and humans, but tasks that use more stringent, operant response tasks, like the matching-to-sample task, often report species differences. Moreover, the data suggest that monkeys may be less sensitive than chimpanzees and humans to the precise spacing of facial features, in addition to the surface-based cues reflected in those features, information that is critical for the representation of individual identity. The aim of this paper is to provide a comprehensive review of the available data from face-processing tasks in non-human primates with the goal of understanding the evolution of this complex cognitive skill.
doi:10.1098/rstb.2010.0358
PMCID: PMC3130377  PMID: 21536559
face recognition; primates; holistic processing
14.  Visual Kin Recognition in Nonhuman Primates: (Pan troglodytes and Macaca mulatta): Inbreeding Avoidance or Male Distinctiveness? 
Faces provide important information about identity, age, and even kinship. A previous study in chimpanzees reported greater similarity between the faces of mothers and sons compared with mothers and daughters, or unrelated individuals. This was interpreted as an inbreeding avoidance mechanism where females, the dispersing gender, should avoid mating with any male that resembles their mother. Alternatively, male faces may be more distinctive than female faces, biasing attention toward males. To test these hypotheses, chimpanzees and rhesus monkeys matched conspecifics’ faces of unfamiliar mothers and fathers with their sons and daughters. Results showed no evidence of male distinctiveness, rather a cross-gender effect was found: chimpanzees were better matching moms with sons and fathers with daughters. Rhesus monkeys, however, showed an overwhelming bias toward male-distinctiveness. They were faster to learn male faces, performed better on father– offspring and parent–son trials, and were best matching fathers with sons. This suggests that for the rhesus monkey, inbreeding avoidance involves something other than facial phenotypic matching but that among chimpanzees, the visual recognition of facial similarities may play an important role.
doi:10.1037/a0020545
PMCID: PMC3075607  PMID: 21090888
kin recognition; face; phenotypic matching; male distinctiveness; inbreeding
15.  A Cross-species Comparison of Facial Morphology and Movement in Humans and Chimpanzees Using the Facial Action Coding System (FACS) 
Journal of nonverbal behavior  2007;31(1):1-20.
A comparative perspective has remained central to the study of human facial expressions since Darwin’s [(1872/1998). The expression of the emotions in man and animals (3rd ed.). New York: Oxford University Press] insightful observations on the presence and significance of cross-species continuities and species-unique phenomena. However, cross-species comparisons are often difficult to draw due to methodological limitations. We report the application of a common methodology, the Facial Action Coding System (FACS) to examine facial movement across two species of hominoids, namely humans and chimpanzees. FACS [Ekman & Friesen (1978). Facial action coding system. CA: Consulting Psychology Press] has been employed to identify the repertoire of human facial movements. We demonstrate that FACS can be applied to other species, but highlight that any modifications must be based on both underlying anatomy and detailed observational analysis of movements. Here we describe the ChimpFACS and use it to compare the repertoire of facial movement in chimpanzees and humans. While the underlying mimetic musculature shows minimal differences, important differences in facial morphology impact upon the identification and detection of related surface appearance changes across these two species.
doi:10.1007/s10919-006-0017-z
PMCID: PMC3008553  PMID: 21188285
Comparative anatomy; Chimpanzees; Facial action coding system (FACS); Facial morphology
16.  Visual expertise does not predict the composite effect across species: A comparison between spider (Ateles geoffroyi) and rhesus (Macaca mulatta) monkeys 
Brain and cognition  2009;71(3):187-195.
Humans are subject to the composite illusion: two identical top halves of a face are perceived as “different” when they are presented with different bottom halves. This observation suggests that when building a mental representation of a face, the underlying system perceives the whole face, and has difficulty decomposing facial features. We adapted a behavioural task that measures the composite illusion to examine the perception of faces in two nonhuman species. Specifically we had spider (Ateles geoffroyi) and rhesus monkeys (Macaca mulatta) perform a two-forced choice, match-to-sample task where only the top half of sample was relevant to the task. The results of Experiment 1 show that spider monkeys (N = 2) process the faces of familiar species (conspecifics and humans, but not chimpanzees, sheep, or sticks), holistically. The second experiment tested rhesus monkeys (N = 7) with the faces of humans, chimpanzees, gorillas, sheep and sticks. Contrary to prediction, there was no evidence of a composite effect in the human (or familiar primate) condition. Instead, we present evidence of a composite illusion in the chimpanzee condition (an unfamiliar primate). Together, these experiments show that visual expertise does not predict the composite effect across the primate order.
doi:10.1016/j.bandc.2009.09.002
PMCID: PMC2783790  PMID: 19815323
comparative psychology; face perception; holistic processing
17.  Facial Musculature in the Rhesus Macaque (Macaca mulatta): Evolutionary and Functional Contexts with Comparisons to Chimpanzees and Humans 
Journal of anatomy  2009;215(3):320-334.
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 to those of other primates. Here we present a detailed description of the facial musculature in rhesus macaques in behavioral, evolutionary, and comparative contexts. Foramlin-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. Results showed that there was a greater number of facial muscles in rhesus macaques than previously described (24) including variably present (and previously unmentioned) zygomaticus minor, levator labii superioris alaeque nasi, depressor septi, anterior auricularis, inferior auricularis, and depressor supercilii muscles. Facial muscles of the rhesus macaque were very similar to those in chimpanzees and in 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 structure of primate facial musculature and that other factors such as social behavior are probably more important. 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.
doi:10.1111/j.1469-7580.2009.01113.x
PMCID: PMC2750044  PMID: 19563473
macaque; facial muscle; mimetic; chimpanzee; evolution; facial expression; primate
18.  Rhesus Monkeys (Macaca mulatta) Lack Expertise in Face Processing 
Faces are salient stimuli for primates that rely predominantly on visual cues for recognizing conspecifics and maintaining social relationships. While previous studies have shown similar face discrimination processes in chimpanzees and humans, data from monkeys are unclear. Therefore, three studies examined face processing in rhesus monkeys using the face inversion effect, a fractured face task, and an individual recognition task. Unlike chimpanzees and humans, the monkeys showed a general face inversion effect reflected by significantly better performance on upright compared to inverted faces (conspecifics, human and chimpanzees faces) regardless of the subjects’ expertise with those categories. Fracturing faces alters first- and second-order configural manipulations whereas previous studies in chimpanzees showed selective deficits for second-order configural manipulations. Finally, when required to individuate conspecific’s faces, i.e., matching two different photographs of the same conspecific, monkeys showed poor discrimination and repeated training. These results support evolutionary differences between rhesus monkeys and Hominoids in the importance of configural cues and their ability to individuate conspecifics’ faces, suggesting a lack of face expertise in rhesus monkeys.
doi:10.1037/0735-7036.122.4.390
PMCID: PMC2859434  PMID: 19014263
face processing; configural cues; inversion effect; rhesus monkey
19.  Facial expression recognition in rhesus monkeys, Macaca mulatta 
Animal behaviour  2009;77(6):1507-1513.
The ability to recognize and accurately interpret facial expressions is critically important for nonhuman primates that rely on these nonverbal signals for social communication. Despite this, little is known about how nonhuman primates, particularly monkeys, discriminate between facial expressions. In the present study, seven rhesus monkeys were required to discriminate four categories of conspecific facial expressions using a matching-to-sample task. In experiment 1, the matching pair showed identical photographs of facial expressions, paired with every other expression type as the nonmatch. The identity of the nonmatching stimulus monkey differed from the one in the sample. Subjects performed above chance on session 1, with no difference in performance across the four expression types. In experiment 2, the identity of all three monkeys differed in each trial, and a neutral portrait was also included as the nonmatching stimulus. Monkeys discriminated expressions across individual identity when the non-match was a neutral stimulus, but they had difficulty when the nonmatch was another expression type. We analysed the degree to which specific feature redundancy could account for these error patterns using a multidimensional scaling analysis which plotted the perceived dissimilarity between expression dyads along a two-dimensional axis. One axis appeared to represent mouth shape, stretched open versus funnelled, while the other appeared to represent a combination of lip retraction and mouth opening. These features alone, however, could not account for overall performance and suggest that monkeys do not rely solely on distinctive features to discriminate among different expressions.
doi:10.1016/j.anbehav.2009.02.024
PMCID: PMC2836777  PMID: 20228886
facial expression; facial features; FACS; Macaca mulatta; matching-to-sample; rhesus monkey
20.  Discrimination of faces and houses by rhesus monkeys: the role of stimulus expertise and rotation angle 
Animal cognition  2008;11(3):467-474.
The face inversion effect, or impaired recognition of upside down compared to upright faces, is used as a marker for the configural processing of faces in primates. The inversion effect in humans and chimpanzees is strongest for categories of stimuli for which subjects have considerable expertise, primarily conspecifics' faces. Moreover, discrimination performance decreases linearly as faces are incrementally rotated from upright to inverted. This suggests that rotated faces must be transformed, or normalized back into their most typical viewpoint before configural processing can ensue, and the greater the required normalization, the greater the likelihood of errors resulting. Previous studies in our lab have demonstrated a general face inversion effect in rhesus monkeys that was not influenced by expertise. Therefore, the present study examined the influence of rotation angle on the visual perception of face and nonface stimuli that varied in their level of expertise to further delineate the processes underlying the inversion effect in rhesus monkeys. Five subjects discriminated images in five orientation angles. Results showed significant linear impairments for all stimulus categories, including houses. However, compared to the upright images, only rhesus faces resulted in worse performance at rotation angles greater than 45°, suggesting stronger configural processing for stimuli for which subjects had the greatest expertise.
doi:10.1007/s10071-008-0137-4
PMCID: PMC2829979  PMID: 18256863
Face processing; Expertise; Configural cues; Rotation
21.  New Developments in Understanding Emotional Facial Signals in Chimpanzees 
There has been little research over the past few decades focusing on similarities and differences in the form and function of emotional signals in nonhuman primates, or whether these communication systems are homologous with those of humans. This is, in part, due to the fact that detailed and objective measurement tools to answer such questions have not been systematically developed for nonhuman primate research. Despite this, emotion research in humans has benefited for over 30 years from an objective, anatomically based facial-measurement tool: the Facial Action Coding System. In collaboration with other researchers, we have now developed a similar system for chimpanzees (ChimpFACS) and, in the process, have made exciting new discoveries regarding chimpanzees’ perception and categorization of emotional facial expressions, similarities in the facial anatomy of chimpanzees and humans, and we have identified homologous facial movements in the two species. Investigating similarities and differences in primate emotional communication systems is essential if we are to understand unique evolutionary specializations among different species.
doi:10.1111/j.1467-8721.2007.00487.x
PMCID: PMC2826813  PMID: 20182651
emotion; facial expression; chimpanzee Facial Action Coding System; evolution; communication
22.  Intramuscular Electrical Stimulation of Facial Muscles in Humans and Chimpanzees: Duchenne Revisited and Extended 
Emotion (Washington, D.C.)  2006;6(3):367-382.
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.
doi:10.1037/1528-3542.6.3.367
PMCID: PMC2826128  PMID: 16938079
facial muscles; intramuscular electrical stimulation; primates; Duchenne
23.  Classifying Chimpanzee Facial Expressions Using Muscle Action 
Emotion (Washington, D.C.)  2007;7(1):172-181.
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.
doi:10.1037/1528-3542.7.1.172
PMCID: PMC2826116  PMID: 17352572
ChimpFACS; facial expressions; emotion; homology
24.  Three studies on configural face processing by chimpanzees 
Brain and cognition  2006;62(1):30-42.
Previous studies have demonstrated the sensitivity of chimpanzees to facial configurations. Three studies further these findings by showing this sensitivity to be specific to second-order relational properties. In humans, this type of configural processing requires prolonged experience and enables subordinate-level discriminations of many individuals. Chimpanzees showed evidence of a composite-like effect for conspecific but not human faces despite extensive experience with humans. Chimpanzee face recognition was impaired only when manipulations targeted second-order properties. Finally, face processing was impaired when individual features were blurred through pixelation. Results confirm that chimpanzee face discrimination, like humans, depends on the integrity of second-order relational properties.
doi:10.1016/j.bandc.2006.03.006
PMCID: PMC2826113  PMID: 16678323
Face processing; Configuration; Expertise; Chimpanzee; Composite effect
25.  Facial Expression Categorization by Chimpanzees Using Standardized Stimuli 
Emotion (Washington, D.C.)  2008;8(2):216-231.
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 subject's overall pattern of errors. Therefore, similar to humans, both configuration and component movements are important during chimpanzee facial expression processing.
doi:10.1037/1528-3542.8.2.216
PMCID: PMC2826112  PMID: 18410196
facial expression; FACS; social cognition; visual processing; inversion

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