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1.  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.
PMCID: PMC2829979  PMID: 18256863
Face processing; Expertise; Configural cues; Rotation
2.  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.
PMCID: PMC2859434  PMID: 19014263
face processing; configural cues; inversion effect; rhesus monkey
3.  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.
PMCID: PMC2783790  PMID: 19815323
comparative psychology; face perception; holistic processing
4.  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.
PMCID: PMC3014412  PMID: 20632050
Visual cognition; Comparative psychology; Face perception; Face recognition
5.  The other-race and other-species effects in face perception – a subordinate-level analysis 
Frontiers in Psychology  2014;5:1068.
The ability of face discrimination is modulated by the frequency of exposure to a category of faces. In other words, lower discrimination performance was measured for infrequently encountered faces as opposed to frequently encountered ones. This phenomenon has been described in the literature: the own-race advantage, a benefit in processing own-race as opposed to the other-race faces, and the own-species advantage, a benefit in processing the conspecific type of faces as opposed to the heterospecific type. So far, the exact parameters that drive either of these two effects are not fully understood. In the following we present a full assessment of data in human participants describing the discrimination performances across two races (Asian and Caucasian) as well as a range of non-human primate faces (chimpanzee, Rhesus macaque and marmoset). We measured reaction times of Asian participants performing a delayed matching-to-sample task, and correlated the results with similarity estimates of facial configuration and face parts. We found faster discrimination of own-race above other-race/species faces. Further, we found a strong reliance on configural information in upright own-species/-race faces and on individual face parts in all inverted face classes, supporting the assumption of specialized processing for the face class of most frequent exposure.
PMCID: PMC4168679  PMID: 25285092
face perception; other-race effect; other-species effect; own-race advantage; own-species advantage; similarity; configural processing; heterospecific faces
6.  Individuation and holistic processing of faces in rhesus monkeys 
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.
PMCID: PMC1919404  PMID: 17609192
face perception; scan path; habituation; dishabituation; preferential looking; inferotemporal cortex
7.  Second-Order Relational Manipulations Affect Both Humans and Monkeys 
PLoS ONE  2011;6(10):e25793.
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.
PMCID: PMC3185012  PMID: 21991354
8.  Face processing in the chimpanzee brain 
Current biology : CB  2008;19(1):50-53.
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.
PMCID: PMC2651677  PMID: 19097899
9.  The face inversion effect in non-human primates revisited - an investigation in chimpanzees (Pan troglodytes) 
Scientific Reports  2013;3:2504.
Faces presented upside-down are harder to recognize than presented right-side up, an effect known as the face inversion effect. With inversion the perceptual processing of the spatial relationship among facial parts is disrupted. Previous literature indicates a face inversion effect in chimpanzees toward familiar and conspecific faces. Although these results are not inconsistent with findings from humans they have some controversy in their methodology. Here, we employed a delayed matching-to-sample task to test captive chimpanzees on discriminating chimpanzee and human faces. Their performances were deteriorated by inversion. More importantly, the discrimination deterioration was systematically different between the two age groups of chimpanzee participants, i.e. young chimpanzees showed a stronger inversion effect for chimpanzee than for human faces, while old chimpanzees showed a stronger inversion effect for human than for chimpanzee faces. We conclude that the face inversion effect in chimpanzees is modulated by the level of expertise of face processing.
PMCID: PMC3753590  PMID: 23978930
10.  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.
PMCID: PMC3544001  PMID: 22670823
Face space; Multidimensional scaling; Face identity; Rhesus monkey; Chimpanzee; Species differences
11.  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.
PMCID: PMC3107657  PMID: 21123266
face recognition; contrast reversal; configuration; chimpanzee; rhesus monkey; evolution
12.  Orienting of Attention to Gaze Direction Cues in Rhesus Macaques: Species-Specificity, and Effects of Cue Motion and Reward Predictiveness 
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.
PMCID: PMC3382411  PMID: 22737139
monkey; conspecific; reflexive; learned; Posner; endogenous; decision-making
13.  Species sensitivity of early face and eye processing 
NeuroImage  2010;54(1):705-713.
Humans are better at recognizing human faces than faces of other species. However, it is unclear whether this species sensitivity can be seen at early perceptual stages of face processing and whether it involves species sensitivity for important facial features like the eyes. These questions were addressed by comparing the modulations of the N170 ERP component to faces, eyes and eyeless faces of humans, apes, cats and dogs, presented upright and inverted. Although all faces and isolated eyes yielded larger responses than the control object category (houses), the N170 was shorter and smaller to human than animal faces and larger to human than animal eyes. Most importantly, while the classic inversion effect was found for human faces, animal faces yielded no inversion effect or an opposite inversion effect, as seen for objects, suggesting a different neural process involved for humans faces compared to faces of other species. Thus, in addition to its general face and eye categorical sensitivity, the N170 appears particularly sensitive to the human species for both faces and eyes. The results are discussed in the context of a recent model of the N170 response involving face and eye sensitive neurons (Itier et al., 2007) where the eyes play a central role in face perception. The data support the intuitive idea that eyes are what make animal head fronts look face-like and that proficiency for the human species involves visual expertise for the human eyes.
PMCID: PMC3933319  PMID: 20650321 CAMSID: cams3880
Face; Eyes; Species; Perception; N170; Inversion
14.  Disrupting perceptual grouping of face parts impairs holistic face processing 
Face perception is widely believed to involve integration of facial features into a holistic perceptual unit, but the mechanisms underlying this integration are relatively unknown. We examined whether perceptual grouping cues influence a classic marker of holistic face perception, the “composite-face effect.” Participants made same–different judgments about a cued part of sequentially presented chimeric faces, and holistic processing was indexed as the degree to which the task-irrelevant face halves impacted performance. Grouping was encouraged or discouraged by adjusting the backgrounds behind the face halves: Although the face halves were always aligned, their respective backgrounds could be misaligned and of different colors. Holistic processing of face, but not of nonface, stimuli was significantly reduced when the backgrounds were misaligned and of different colors, cues that discouraged grouping of the face halves into a cohesive unit (Exp. 1). This effect was sensitive to stimulus orientation at short (200 ms) but not at long (2,500 ms) encoding durations, consistent with the previously documented temporal properties of the holistic processing of upright and inverted faces (Exps. 2 and 3). These results suggest that grouping mechanisms, typically involved in the perception of objecthood more generally, might contribute in important ways to the holistic perception of faces.
PMCID: PMC3824569  PMID: 23179914
Face perception; Object-based attention; Grouping; Segmentation; Holistic processing
15.  The Thatcher illusion in humans and monkeys 
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).
PMCID: PMC2982021  PMID: 20484235
Thatcher illusion; monkey; face recognition; holistic perception
16.  Heterochrony and Cross-Species Intersensory Matching by Infant Vervet Monkeys 
PLoS ONE  2009;4(1):e4302.
Understanding the evolutionary origins of a phenotype requires understanding the relationship between ontogenetic and phylogenetic processes. Human infants have been shown to undergo a process of perceptual narrowing during their first year of life, whereby their intersensory ability to match the faces and voices of another species declines as they get older. We investigated the evolutionary origins of this behavioral phenotype by examining whether or not this developmental process occurs in non-human primates as well.
Methodology/Principal Findings
We tested the ability of infant vervet monkeys (Cercopithecus aethiops), ranging in age from 23 to 65 weeks, to match the faces and voices of another non-human primate species (the rhesus monkey, Macaca mulatta). Even though the vervets had no prior exposure to rhesus monkey faces and vocalizations, our findings show that infant vervets can, in fact, recognize the correspondence between rhesus monkey faces and voices (but indicate that they do so by looking at the non-matching face for a greater proportion of overall looking time), and can do so well beyond the age of perceptual narrowing in human infants. Our results further suggest that the pattern of matching by vervet monkeys is influenced by the emotional saliency of the Face+Voice combination. That is, although they looked at the non-matching screen for Face+Voice combinations, they switched to looking at the matching screen when the Voice was replaced with a complex tone of equal duration. Furthermore, an analysis of pupillary responses revealed that their pupils showed greater dilation when looking at the matching natural face/voice combination versus the face/tone combination.
Because the infant vervets in the current study exhibited cross-species intersensory matching far later in development than do human infants, our findings suggest either that intersensory perceptual narrowing does not occur in Old World monkeys or that it occurs later in development. We argue that these findings reflect the faster rate of neural development in monkeys relative to humans and the resulting differential interaction of this factor with the effects of early experience.
PMCID: PMC2627929  PMID: 19172998
17.  Sensitivity to first-order relations of facial elements in infant rhesus macaques 
Infant and child development  2013;22(3):320-330.
Faces are visually attractive to both human and nonhuman primates. Human neonates are thought to have a broad template for faces at birth and prefer face-like to non-face-like stimuli. To better compare developmental trajectories of face processing phylogenetically, here we investigated preferences for face-like stimuli in infant rhesus macaques using photographs of real faces. We presented infant macaques aged 15–25days with human, macaque, and abstract faces with both normal and linear arrangements of facial features, and measured infants’ gaze durations, number of fixations, and latency to look to each face using eye-tracking technology. There was an overall preference for normal over linear facial arrangements for abstract and monkey faces, but not human faces. Moreover, infant macaques looked less at monkey faces than at abstract or human faces. These results suggest that species and facial configurations affect face processing in infant macaques, and we discuss potential explanations for these findings. Further, carefully controlled studies are required to ascertain whether infant macaques’ face template can be considered as broad as human infants’ face template.
PMCID: PMC3753110  PMID: 23997657
Rhesus Macaque; Infant; Face Perception; Eyes; Eye Tracking
18.  The Part Task of the Part-Spacing Paradigm Is Not a Pure Measurement of Part-Based Information of Faces 
PLoS ONE  2009;4(7):e6239.
Faces are arguably one of the most important object categories encountered by human observers, yet they present one of the most difficult challenges to both the human and artificial visual systems. A variety of experimental paradigms have been developed to study how faces are represented and recognized, among which is the part-spacing paradigm. This paradigm is presumed to characterize the processing of both the featural and configural information of faces, and it has become increasingly popular for testing hypotheses on face specificity and in the diagnosis of face perception in cognitive disorders.
Methodology/Principal Findings
In two experiments we questioned the validity of the part task of this paradigm by showing that, in this task, measuring pure information about face parts is confounded by the effect of face configuration on the perception of those parts. First, we eliminated or reduced contributions from face configuration by either rearranging face parts into a non-face configuration or by removing the low spatial frequencies of face images. We found that face parts were no longer sensitive to inversion, suggesting that the previously reported inversion effect observed in the part task was due in fact to the presence of face configuration. Second, self-reported prosopagnosic patients who were selectively impaired in the holistic processing of faces failed to detect part changes when face configurations were presented. When face configurations were scrambled, however, their performance was as good as that of normal controls.
In sum, consistent evidence from testing both normal and prosopagnosic subjects suggests the part task of the part-spacing paradigm is not an appropriate task for either measuring how face parts alone are processed or for providing a valid contrast to the spacing task. Therefore, conclusions from previous studies using the part-spacing paradigm may need re-evaluation with proper paradigms.
PMCID: PMC2706049  PMID: 19603077
19.  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.
PMCID: PMC3075607  PMID: 21090888
kin recognition; face; phenotypic matching; male distinctiveness; inbreeding
20.  Elastic facial movement influences part-based but not holistic processing 
Face processing has been studied for decades. However, most of the empirical investigations have been conducted using static face images as stimuli. Little is known about whether static face processing findings can be generalized to real world contexts, in which faces are constantly moving. The present study investigates the nature of face processing (holistic vs. part-based) in elastic moving faces. Specifically, we focus on whether elastic moving faces, as compared to static ones, can facilitate holistic or part-based face processing. Using the composite paradigm, participants were asked to remember either an elastic moving face (i.e., a face that blinks and chews) or a static face, and then tested with a static composite face. The composite effect was (1) significantly smaller in the dynamic condition than in the static condition, (2) consistently found with different face encoding times (Experiments 1–3), and (3) present for the recognition of both upper and lower face parts (Experiment 4). These results suggest that elastic facial motion facilitates part-based processing, rather than holistic processing. Thus, while previous work with static faces has emphasized an important role for holistic processing, the current work highlights an important role for featural processing with moving faces.
PMCID: PMC3889867  PMID: 23398253
elastic facial movement; holistic processing; part-based processing; composite face paradigm
21.  The Face Inversion Effect Following Pitch and Yaw Rotations: Investigating the Boundaries of Holistic Processing 
Upright faces are thought to be processed holistically. However, the range of views within which holistic processing occurs is unknown. Recent research by McKone (2008) suggests that holistic processing occurs for all yaw-rotated face views (i.e., full-face through to profile). Here we examined whether holistic processing occurs for pitch, as well as yaw, rotated face views. In this face recognition experiment: (i) participants made same/different judgments about two sequentially presented faces (either both upright or both inverted); (ii) the test face was pitch/yaw rotated by between 0° and 75° from the encoding face (always a full-face view). Our logic was as follows: if a particular pitch/yaw-rotated face view is being processed holistically when upright, then this processing should be disrupted by inversion. Consistent with previous research, significant face inversion effects (FIEs) were found for all yaw-rotated views. However, while FIEs were found for pitch rotations up to 45°, none were observed for 75° pitch rotations (rotated either above or below the full face). We conclude that holistic processing does not occur for all views of upright faces (e.g., not for uncommon pitch rotated views), only those that can be matched to a generic global representation of a face.
PMCID: PMC3525703  PMID: 23267337
face recognition; inversion; holistic processing; pitch and yaw axes
22.  Responses of chimpanzees to cues of conspecific observation☆ 
Animal Behaviour  2013;86(3):595-602.
Recent evidence has shown that humans are remarkably sensitive to artificial cues of conspecific observation when making decisions with potential social consequences. Whether similar effects are found in other great apes has not yet been investigated. We carried out two experiments in which individual chimpanzees, Pan troglodytes, took items of food from an array in the presence of either an image of a large conspecific face or a scrambled control image. In experiment 1 we compared three versions of the face image varying in size and the amount of the face displayed. In experiment 2 we compared a fourth variant of the image with more prominent coloured eyes displayed closer to the focal chimpanzee. The chimpanzees did not look at the face images significantly more than at the control images in either experiment. Although there were trends for some individuals in each experiment to be slower to take high-value food items in the face conditions, these were not consistent or robust. We suggest that the extreme human sensitivity to cues of potential conspecific observation may not be shared with chimpanzees.
•Humans respond strongly to ‘watching eyes’, but whether chimpanzees do is unknown.•We investigated if chimpanzees' readiness to take food was affected by face images.•There was no clear evidence that subjects looked at faces more than control images.•Any effect of the faces on chimpanzees' decisions was weak and inconsistent.•Chimpanzees may not be as sensitive to cues of being watched as humans are.
PMCID: PMC3763378  PMID: 24027343
chimpanzee; cooperation; Pan troglodytes; reputation; social intelligence; watching eyes
23.  Stimulus Requirements for Face Perception: An Analysis Based on “Totem Poles” 
The stimulus requirements for perceiving a face are not well defined but are presumably simple, for vivid faces can often by seen in random or natural images such as cloud or rock formations. To characterize these requirements, we measured where observers reported the impression of faces in images defined by symmetric 1/f noise. This allowed us to examine the prominence and properties of different features and their necessary configurations. In these stimuli many faces can be perceived along the vertical midline, and appear stacked at multiple scales, reminiscent of “totem poles.” In addition to symmetry, the faces in noise are invariably upright and thus reveal the inversion effects that are thought to be a defining property of configural face processing. To a large extent, seeing a face required seeing eyes, and these were largely restricted to dark regions in the images. Other features were more subordinate and showed relatively little bias in polarity. Moreover, the prominence of eyes depended primarily on their luminance contrast and showed little influence of chromatic contrast. Notably, most faces were rated as clearly defined with highly distinctive attributes, suggesting that once an image area is coded as a face it is perceptually completed consistent with this interpretation. This suggests that the requisite trigger features are sufficient to holistically “capture” the surrounding noise structure to form the facial representation. Yet despite these well articulated percepts, we show in further experiments that while a pair of dark spots added to noise images appears face-like, these impressions fail to elicit other signatures of face processing, and in particular, fail to elicit an N170 or fixation patterns typical for images of actual faces. These results suggest that very simple stimulus configurations are sufficient to invoke many aspects of holistic and configural face perception while nevertheless failing to fully engage the neural machinery of face coding, implying that that different signatures of face processing may have different stimulus requirements.
PMCID: PMC3569666  PMID: 23407599
face perception; face detection; configural coding; facial features; symmetry; inversion effects; noise
24.  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.
PMCID: PMC3130377  PMID: 21536559
face recognition; primates; holistic processing
25.  Thatcher effect in monkeys demonstrates conservation of face perception across primates 
Current biology : CB  2009;19(15):1270-1273.
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.
PMCID: PMC2726903  PMID: 19559613

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