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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.

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.

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.

Summary

Among humans, face recognition involves highly specialized cognitive and neural processes that enable the recognition of specific individuals [1–5]. While comparative studies suggest similar cognitive processes underlie face recognition in chimpanzees and humans [6–8, SOM#1], it remains unknown whether chimpanzees also show face-selective activity in ventral temporal cortex. This study is the first to examine regional cerebral glucose metabolism using 18F-Flurodeoxyglucose Positron Emission Tomography in chimpanzees after they performed computerized tasks matching conspecifics’ faces and nonface objects (SOM#2). A whole brain analysis comparing these two tasks directly in five chimpanzees revealed significant face-selective activity in brain regions known to comprise the distributed cortical face processing network in humans, including superior temporal sulcus and orbitofrontal cortex [9–11]. In order to identify regions that were exclusively active during one task, but not the other, a resting-state condition was subtracted from each task and the activity exclusive to each task was identified. This revealed numerous distinct patches of face-selective activity in the fusiform gyrus that were interspersed within a large expanse of object-selective cortex. This pattern suggests similar object form topography in the ventral temporal cortex of chimpanzees and humans, in which faces may represent a special class of visual stimulus.

Recognition and individuation of conspecifics by their face is essential for primate social cognition. This ability is driven by a mechanism that integrates the appearance of facial features with subtle variations in their configuration (i.e., second-order relational properties) into a holistic representation. So far, there is little evidence of whether our evolutionary ancestors show sensitivity to featural spatial relations and hence holistic processing of faces as shown in humans. Here, we directly compared macaques with humans in their sensitivity to configurally altered faces in upright and inverted orientations using a habituation paradigm and eye tracking technologies. In addition, we tested for differences in processing of conspecific faces (human faces for humans, macaque faces for macaques) and non-conspecific faces, addressing aspects of perceptual expertise. In both species, we found sensitivity to second-order relational properties for conspecific (expert) faces, when presented in upright, not in inverted, orientation. This shows that macaques possess the requirements for holistic processing, and thus show similar face processing to that of humans.

Despite considerable evidence that neural activity in monkeys reflects various aspects of face perception, relatively little is known about monkeys' face processing abilities. Two characteristics of face processing observed in humans are a subordinate-level entry point, here, the default recognition of faces at the subordinate, rather than basic, level of categorization, and holistic effects, i.e. perception of facial displays as an integrated whole. The present study used an adaptation paradigm to test whether untrained rhesus macaques (Macaca mulatta) display these hallmarks of face processing. In experiments 1 and 2, macaques showed greater rebound from adaptation to conspecific faces than to other animals at the individual or subordinate level. In experiment 3, exchanging only the bottom half of a monkey face produced greater rebound in aligned than in misaligned composites, indicating that for normal, aligned faces, the new bottom half may have influenced the perception of the whole face. Scan path analysis supported this assertion: during rebound, fixation to the unchanged eye region was renewed, but only for aligned stimuli. These experiments show that macaques naturally display the distinguishing characteristics of face processing seen in humans and provide the first clear demonstration that holistic information guides scan paths for conspecific faces.

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.

Primates possess the remarkable ability to differentiate faces of group members and to extract relevant information about the individual directly from the face. Recognition of conspecific faces is achieved by means of holistic processing, i.e. the processing of the face as an unparsed, perceptual whole, rather than as the collection of independent features (part-based processing). The most striking example of holistic processing is the Thatcher illusion. Local changes in facial features are hardly noticeable when the whole face is inverted (rotated 180°), but strikingly grotesque when the face is upright. This effect can be explained by a lack of processing capabilities for locally rotated facial features when the face is turned upside down. Recently, a Thatcher illusion was described in the macaque monkey analogous to that known from human investigations. Using a habituation paradigm combined with eye tracking, we address the critical follow-up questions raised in the aforementioned study to show the Thatcher illusion as a function of the observer's species (humans and macaques), the stimulus' species (humans and macaques) and the level of perceptual expertise (novice, expert).

Primates live in complex social groups and rely on social cues to direct their attention. For example, primates react faster to an unpredictable stimulus after seeing a conspecific looking in the direction of that stimulus. In the current study we tested the specificity of facial cues (gaze direction) for orienting attention and their interaction with other cues that are known to guide attention. In particular, we tested whether macaque monkeys only respond to gaze cues from conspecifics or if the effect generalizes across species. We found an attentional advantage of conspecific faces over human and cartoon faces. Because gaze cues are often conveyed by gesture, we also explored the effect of image motion (a simulated glance) on the orienting of attention in monkeys. We found that the simulated glance did not significantly enhance the speed of orienting for monkey-face stimuli, but had a significant effect for images of human faces. Finally, because gaze cues presumably guide attention toward relevant or rewarding stimuli, we explored whether orienting of attention was modulated by reward predictiveness. When the cue predicted reward location, face, and non-face cues were effective in speeding responses toward the cued location. This effect was strongest for conspecific faces. In sum, our results suggest that while conspecific gaze cues activate an intrinsic process that reflexively directs spatial attention, its effect is relatively small in comparison to other features including motion and reward predictiveness. It is possible that gaze cues are more important for decision-making and voluntary orienting than for reflexive orienting.

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.

Perceptual expertise has been studied intensively with faces and object categories involving detailed individuation. A common finding is that experience in fulfilling the task demand of fine, subordinate-level discrimination between highly similar instances is associated with the development of holistic processing. This study examines whether holistic processing is also engaged by expert word recognition, which is thought to involve coarser, basic-level processing that is more part-based. We adopted a paradigm widely used for faces – the composite task, and found clear evidence of holistic processing for English words. A second experiment further showed that holistic processing for words was sensitive to the amount of experience with the language concerned (native vs. second-language readers) and with the specific stimuli (words vs. pseudowords). The adoption of a paradigm from the face perception literature to the study of expert word perception is important for further comparison between perceptual expertise with words and face-like expertise.

Face perception serves as the basis for much of human social exchange. Diverse information can be extracted about an individual from a single glance at their face, including their identity, emotional state, and direction of attention. Neuropsychological and fMRI experiments reveal a complex network of specialized areas in the human brain supporting these face-reading skills. Here we consider the evolutionary roots of human face perception by exploring the manner in which different animal species view and respond to faces. We focus on behavioral experiments collected from both primates and non-primates, assessing the types of information that animals are able to extract from the faces of their conspecifics, human experimenters, and natural predators. These experiments reveal that faces are an important category of visual stimuli for animals in all major vertebrate taxa, possibly reflecting the early emergence of neural specialization for faces in vertebrate evolution. At the same time, some aspects of facial perception are only evident in primates and a few other social mammals, and may therefore have evolved to suit the needs of complex social communication. Since the human brain likely utilizes both primitive and recently evolved neural specializations for the processing of faces, comparative studies may hold the key to understanding how these parallel circuits emerged during human evolution.

Previous studies have shown that a variety of animals including humans are sensitive to social cues from others and shift their attention to the same objects attended to by others. However, little is known about how animals process conspecifics' and another species' actions, although primates recognize conspecific faces better than those of another species. In this study, using unrestrained eye-tracking techniques, we first demonstrated that conspecific social cues modulated looking behaviours of chimpanzees more than human cues, whereas human observers were equally sensitive to both species. Additionally, first pass gaze duration at the face indicates that chimpanzees looked at the chimpanzees' face longer than the human face, suggesting that chimpanzees might extract more referential information from a conspecific face. These results also imply that a unique ability for extracting referential information from a variety of social objects has emerged during human evolution.

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.

Early deprivation in audition can have striking effects on the development of visual processing. Here we investigated whether early deafness induces changes in holistic/configural face processing. To this end, we compared the results of a group of early deaf participants to those of a group of hearing participants in an inversion-matching task (Experiment 1) and a composite face task (Experiment 2). We hypothesized that deaf individuals would show an enhanced inversion effect and/or an increased composite face effect compared to hearing controls in case of enhanced holistic/configural face processing. Conversely, these effects would be reduced if they rely more on facial features than hearing controls. As a result, we found that deaf individuals showed an increased inversion effect for faces, but not for non-face objects. They were also significantly slower than hearing controls to match inverted faces. However, the two populations did not differ regarding the overall size of their composite face effect. Altogether these results suggest that early deafness does not enhance or reduce the amount of holistic/configural processing devoted to faces but may increase the dependency on this mode of processing.

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.

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.

Holistic processing, i.e. the tendency to process objects as wholes, is associated with face perception and also with expertise individuating novel objects. Surprisingly, recent work also reveals holistic effects in novice observers. It is unclear whether the same mechanisms support holistic effects in experts and in novices. Here, we measured holistic processing of music sequences using a selective attention task in participants who vary in music reading expertise. We found that holistic effects were strategic in novices but relatively automatic in experts. Correlational analyses revealed that individual holistic effects were predicted by both individual music reading ability and neural responses for musical notation in the right fusiform face area (rFFA), but in opposite directions for experts and novices, suggesting that holistic effects in the two groups may be of different nature. To characterize expert perception, it is important to measure not only the tendency to process objects as wholes but to test whether this effect is dependent on task constraints.

Summary

Accurate recognition of individuals is a foundation of social cognition. The remarkable ability of humans to distinguish among thousands of similar faces depends on sensitivity to unique configurations of facial features, including subtle differences in the relative placement of the eyes and mouth [1, 2]. Determining whether similar perceptual processes underlie individual recognition in nonhuman primates is important for both the study of cognitive evolution and the appropriate use of primate models in social cognition research. In humans, some of the best evidence for a keen sensitivity to the configuration of features in faces comes from the “Thatcher Effect”. This effect shows that it is difficult to detect changes in the orientation of the eyes and mouth in an image of an inverted face, even though identical changes are unmistakable in an upright face [3, 4]. Here, we demonstrate for the first time that a nonhuman primate species also shows the Thatcher Effect. This direct evidence of configural face perception in monkeys, collected under testing conditions that closely parallel those used with humans, indicates that perceptual mechanisms for individual recognition have been conserved through primate cognitive evolution.

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.

The study of nonhuman primate vocal–auditory behavior continues to provide novel insights into the origins of human language. However, data on the neural systems involved in the perception and processing of conspecific vocalizations in great apes are virtually absent in the scientific literature, yet are critical for understanding the evolution of language. Here we used positron emission tomography to examine the neurological mechanisms associated with the perception of species-specific vocalizations in chimpanzees. The data indicate right-lateralized activity in the chimpanzee posterior temporal lobe, including the planum temporale, in response to certain calls, but not others. In addition, important differences are apparent when these data are compared with those published previously from monkey species suggesting that there may be marked differences in the way chimpanzees and macaque monkeys perceive and process conspecific vocalizations. These results provide the first evidence of the neural correlates of auditory perception in chimpanzees and offer unprecedented information concerning the origins of hemispheric specialization in humans.

Background: Higher levels of facial processing, such as recognition of the individuality and emotional expression of faces, are abnormal in schizophrenia. It is unknown, however, whether the visual detection of a face as face is impaired as well. Methods: We examined the performance of schizophrenia patients (n = 29) and normal controls (n = 28) in locating a line-drawn face on the left or the right side of a larger line drawing. To prevent the normal formation of general facial impressions, stimulus presentations were brief (13–104 ms). The face stimuli were either displayed upright or inverted in order to study the face inversion effect, ie, the specific effect of stimulus inversion on face processing. Results: Schizophrenia patients showed a significantly reduced face inversion effect, resulting primarily from significantly lower accuracy in detecting upright faces than normal controls. In tree detection, a comparison task that was also administered, the stimulus inversion effect was similarly small in both groups. Conclusion: Given the primitive nature and brief duration of the stimuli, and the simplicity of the task, these results indicate that at the initial visual detection stage, facial processing is inefficient in schizophrenia. By isolating face detection from other aspects of face recognition, this study identifies a face-specific visual deficit in schizophrenia, which may ultimately contribute to impaired face-related cognitive and emotional processing and social interaction.

Background

Higher levels of facial processing, such as recognition of the individuality and emotional expression of faces, are abnormal in schizophrenia. It is unknown, however, whether the visual detection of a face as face is impaired as well.

Methods

We examined the performance of schizophrenia patients (n = 29) and normal controls (n = 28) in locating a line-drawn face on the left or the right side of a larger line drawing. To prevent the normal formation of general facial impressions, stimulus presentations were brief (13–104 ms). The face stimuli were either displayed upright or inverted in order to study the face inversion effect, ie, the specific effect of stimulus inversion on face processing.

Results

Schizophrenia patients showed a significantly reduced face inversion effect, resulting primarily from significantly lower accuracy in detecting upright faces than normal controls. In tree detection, a comparison task that was also administered, the stimulus inversion effect was similarly small in both groups.

Conclusion

Given the primitive nature and brief duration of the stimuli, and the simplicity of the task, these results indicate that at the initial visual detection stage, facial processing is inefficient in schizophrenia. By isolating face detection from other aspects of face recognition, this study identifies a face-specific visual deficit in schizophrenia, which may ultimately contribute to impaired face-related cognitive and emotional processing and social interaction.

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.

Background

While own-age faces have been reported to be better recognized than other-age faces, the underlying cause of this phenomenon remains unclear. One potential cause is holistic face processing, a special kind of perceptual and cognitive processing reserved for perceiving upright faces. Previous studies have indeed found that adults show stronger holistic processing when looking at adult faces compared to child faces, but whether a similar own-age bias exists in children remains to be shown.

Methodology/Principal Findings

Here we used the composite face task – a standard test of holistic face processing – to investigate if, for child faces, holistic processing is stronger for children than adults. Results showed child participants (8–13 years) had a larger composite effect than adult participants (22–65 years).

Conclusions/Significance

Our finding suggests that differences in strength of holistic processing may underlie the own-age bias on recognition memory. We discuss the origin of own-age biases in terms of relative experience, face-space tuning, and social categorization.