Second-order relational manipulations affect both humans and monkeys

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.     

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).     

Early Electrophysiological Basis of Experience-Associated Holistic Processing of Chinese Characters

Recent studies have found holistic processing to be a marker of expertise for perception of words in alphabetic (e.g., English) and non-alphabetic (e.g., Chinese) writing systems, consistent with what has been found for faces and other objects of face-like expertise. It is unknown, however, whether holistic processing of words occurs in an early, perceptual stage as it does for faces. We examined how early holistic processing of Chinese characters emerges by recording the event-related potentials (ERPs) in an adaptation paradigm. Participants judged if the top parts of two sequentially presented characters were the same or different while ignoring the bottom part. An early potential (P1) at the posterior channels was smaller when the attended top parts were the same compared with when they are different, indicating an adaptation effect. Critically, for trials with identical top parts, P1 was larger when the irrelevant bottom parts were different, indicating a release of adaptation. This effect was present only when the two character parts were aligned but not misaligned, and only for characters but not for pseudocharacters. The finding of early sensitivity to all parts of a Chinese character suggests that Chinese characters are represented holistically at a perceptual level.     

Cross-Category Adaptation: Objects Produce Gender Adaptation in the Perception of Faces

Adaptation aftereffects have been found for low-level visual features such as colour, motion and shape perception, as well as higher-level features such as gender, race and identity in domains such as faces and biological motion. It is not yet clear if adaptation effects in humans extend beyond this set of higher order features. The aim of this study was to investigate whether objects highly associated with one gender, e.g. high heels for females or electric shavers for males can modulate gender perception of a face. In two separate experiments, we adapted subjects to a series of objects highly associated with one gender and subsequently asked participants to judge the gender of an ambiguous face. Results showed that participants are more likely to perceive an ambiguous face as male after being exposed to objects highly associated to females and vice versa. A gender adaptation aftereffect was obtained despite the adaptor and test stimuli being from different global categories (objects and faces respectively). These findings show that our perception of gender from faces is highly affected by our environment and recent experience. This suggests two possible mechanisms: (a) that perception of the gender associated with an object shares at least some brain areas with those responsible for gender perception of faces and (b) adaptation to gender, which is a high-level concept, can modulate brain areas that are involved in facial gender perception through top-down processes.     

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.     

Categorical Perception of Fear and Anger Expressions in Whole,Masked and Composite Faces

Human observers are remarkably proficient at recognizing expressions of emotions and at readily grouping them into distinct categories. When morphing one facial expression into another, the linear changes in low-level features are insufficient to describe the changes in perception, which instead follow an s-shaped function. Important questions are, whether there are single diagnostic regions in the face that drive categorical perception for certain parings of emotion expressions, and how information in those regions interacts when presented together. We report results from two experiments with morphed fear-anger expressions, where (a) half of the face was masked or (b) composite faces made up of different expressions were presented. When isolated upper and lower halves of faces were shown, the eyes were found to be almost as diagnostic as the whole face, with the response function showing a steep category boundary. In contrast, the mouth allowed for a substantially lesser amount of accuracy and responses followed a much flatter psychometric function. When a composite face consisting of mismatched upper and lower halves was used and observers were instructed to exclusively judge either the expression of mouth or eyes, the to-be-ignored part always influenced perception of the target region. In line with experiment 1, the eye region exerted a much stronger influence on mouth judgements than vice versa. Again, categorical perception was significantly more pronounced for upper halves of faces. The present study shows that identification of fear and anger in morphed faces relies heavily on information from the upper half of the face, most likely the eye region. Categorical perception is possible when only the upper face half is present, but compromised when only the lower part is shown. Moreover, observers tend to integrate all available features of a face, even when trying to focus on only one part.     

From single cells to social perception

Research describing the cellular coding of faces in non-human primates often provides the underlying physiological framework for our understanding of face processing in humans. Models of face perception, explanations of perceptual after-effects from viewing particular types of faces, and interpretation of human neuroimaging data rely on monkey neurophysiological data and the assumption that neurophysiological responses of humans are comparable to those recorded in the non-human primate. Here, we review studies that describe cells that preferentially respond to faces, and assess the link between the physiological characteristics of single cells and social perception. Principally, we describe cells recorded from the non-human primate, although a limited number of cells have been recorded in humans, and are included in order to appraise the validity of non-human physiological data for our understanding of human face and social perception.     

Holistic processing of words modulated by reading experience

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.     

Inversion effect in perception of human faces in a chimpanzee (Pan troglodytes)

Three experiments investigated the inversion effect in face perception by a chimpanzee (Pantroglodytes) under the matching-to-sample paradigm. The first two experiments addressed the inversion effect in the perception of human faces. In Experiment 1, the subject received identity matching using 104 photographs of faces and houses presented in four different orientations. The chimpanzee showed better accuracy when the faces were presented upright than when they were inverted. The inversion effect was not found for photographs of houses. In Experiment 2, the subject received rotational matching in which the sample and comparisons differed in orientation. The subject showed a clear inversion effect for faces but not for houses. Experiment 3 explored the hemispheric specialization of the face inversion effect with chimeric (artificially composed) faces. The subject showed no visual-field preference when the chimeric faces were presented as samples under nonreinforced probe testing, while the inversion effect was evident when the discrimination was based on the left part of the chimeric sample. The results suggested that the face-inversion was specific to the left visual field (i.e. right hemispheric processing). In general, these results were consistent with those found in humans in similar testing situations.     

On the Other Side of the Fence: Effects of Social Categorization and Spatial Grouping on Memory and Attention for Own-Race and Other-Race Faces

The term “own-race bias” refers to the phenomenon that humans are typically better at recognizing faces from their own than a different race. The perceptual expertise account assumes that our face perception system has adapted to the faces we are typically exposed to, equipping it poorly for the processing of other-race faces. Sociocognitive theories assume that other-race faces are initially categorized as out-group, decreasing motivation to individuate them. Supporting sociocognitive accounts, a recent study has reported improved recognition for other-race faces when these were categorized as belonging to the participants'' in-group on a second social dimension, i.e., their university affiliation. Faces were studied in groups, containing both own-race and other-race faces, half of each labeled as in-group and out-group, respectively. When study faces were spatially grouped by race, participants showed a clear own-race bias. When faces were grouped by university affiliation, recognition of other-race faces from the social in-group was indistinguishable from own-race face recognition. The present study aimed at extending this singular finding to other races of faces and participants. Forty Asian and 40 European Australian participants studied Asian and European faces for a recognition test. Faces were presented in groups, containing an equal number of own-university and other-university Asian and European faces. Between participants, faces were grouped either according to race or university affiliation. Eye tracking was used to study the distribution of spatial attention to individual faces in the display. The race of the study faces significantly affected participants'' memory, with better recognition of own-race than other-race faces. However, memory was unaffected by the university affiliation of the faces and by the criterion for their spatial grouping on the display. Eye tracking revealed strong looking biases towards both own-race and own-university faces. Results are discussed in light of the theoretical accounts of the own-race bias.     

The Composite Task Reveals Stronger Holistic Processing in Children than Adults for Child Faces

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.     

Prolonged visual experience in adulthood modulates holistic face perception

Background

Using the well-known composite illusion as a marker of the holistic perception of faces, we tested how prolonged visual experience with a specific population of faces (4- to 6-year-old children) modulates the face perception system in adulthood.

Methodology/Principal Findings

We report a face composite effect that is larger for adult than children faces in a group of adults without experience with children faces (“children-face novices”), while it is of equal magnitude for adults and children faces in a population of preschool teachers (“children-face experts”). When considering preschool teachers only, we observed a significant correlation between the number of years of experience with children faces and the differential face composite effect between children and adults faces. Participants with at least 10 years of qualitative experience with children faces had a larger composite face effect for children than adult faces.

Conclusions/Significance

Overall, these observations indicate that even in adulthood face processes can be reshaped qualitatively, presumably to facilitate efficient processing of the differential morphological features of the frequently encountered population of faces.     

The fusiform face area is engaged in holistic, not parts-based, representation of faces

Numerous studies with functional magnetic resonance imaging have shown that the fusiform face area (FFA) in the human brain plays a key role in face perception. Recent studies have found that both the featural information of faces (e.g., eyes, nose, and mouth) and the configural information of faces (i.e., spatial relation among features) are encoded in the FFA. However, little is known about whether the featural information is encoded independent of or combined with the configural information in the FFA. Here we used multi-voxel pattern analysis to examine holistic representation of faces in the FFA by correlating spatial patterns of activation with behavioral performance in discriminating face parts with face configurations either present or absent. Behaviorally, the absence of face configurations (versus presence) impaired discrimination of face parts, suggesting a holistic representation in the brain. Neurally, spatial patterns of activation in the FFA were more similar among correct than incorrect trials only when face parts were presented in a veridical face configuration. In contrast, spatial patterns of activation in the occipital face area, as well as the object-selective lateral occipital complex, were more similar among correct than incorrect trials regardless of the presence of veridical face configurations. This finding suggests that in the FFA faces are represented not on the basis of individual parts but in terms of the whole that emerges from the parts.     

The Effects of Prediction on the Perception for Own-Race and Other-Race Faces

Human beings do not passively perceive important social features about others such as race and age in social interactions. Instead, it is proposed that humans might continuously generate predictions about these social features based on prior similar experiences. Pre-awareness of racial information conveyed by others'' faces enables individuals to act in “culturally appropriate” ways, which is useful for interpersonal relations in different ethnicity groups. However, little is known about the effects of prediction on the perception for own-race and other-race faces. Here, we addressed this issue using high temporal resolution event-related potential techniques. In total, data from 24 participants (13 women and 11 men) were analyzed. It was found that the N170 amplitudes elicited by other-race faces, but not own-race faces, were significantly smaller in the predictable condition compared to the unpredictable condition, reflecting a switch to holistic processing of other-race faces when those faces were predictable. In this respect, top-down prediction about face race might contribute to the elimination of the other-race effect (one face recognition impairment). Furthermore, smaller P300 amplitudes were observed for the predictable than for unpredictable conditions, which suggested that the prediction of race reduced the neural responses of human brains.     

Selectivity of Face Perception to Horizontal Information over Lifespan (from 6 to 74 Year Old)

Face recognition in young human adults preferentially relies on the processing of horizontally-oriented visual information. We addressed whether the horizontal tuning of face perception is modulated by the extensive experience humans acquire with faces over the lifespan, or whether it reflects an invariable processing bias for this visual category. We tested 296 subjects aged from 6 to 74 years in a face matching task. Stimuli were upright and inverted faces filtered to preserve information in the horizontal or vertical orientation, or both (HV) ranges. The reliance on face-specific processing was inferred based on the face inversion effect (FIE). FIE size increased linearly until young adulthood in the horizontal but not the vertical orientation range of face information. These findings indicate that the protracted specialization of the face processing system relies on the extensive experience humans acquire at encoding the horizontal information conveyed by upright faces.     

The evolution of the multicoloured face of mandrills: insights from the perceptual space of colour vision

Multicomponent signals consist of several traits that are perceived as a whole. Although many animals rely on multicomponent signals to communicate, the selective pressures shaping these signals are still poorly understood. Previous work has mainly investigated the evolution of multicomponent signals by studying each trait individually, which may not accurately reflect the selective pressures exerted by the holistic perception of signal receivers. Here, we study the design of the multicoloured face of an Old World primate, the mandrill (Mandrillus sphinx), in relation to two aspects of signalling that are expected to be selected by receivers: conspicuousness and information. Using reflectance data on the blue and red colours of the faces of 34 males and a new method of hue vectorisation in a perceptual space of colour vision, we show that the blue hue maximises contrasts to both the red hue and the foliage background colouration, thereby increasing the conspicuousness of the whole display. We further show that although blue saturation, red saturation and the contrast between blue and red colours are all correlated with dominance, dominance is most accurately indicated by the blue-red contrast. Taken together our results suggest that the evolution of blue and red facial colours in male mandrills are not independent and are likely driven by the holistic perception of conspecifics. In this view, we propose that the multicoloured face of mandrills acts as a multicomponent signal. Last, we show that information accuracy increases with the conspicuousness of the whole display, indicating that both aspects of signalling can evolve in concert.     

Adaptation Aftereffects in Vocal Emotion Perception Elicited by Expressive Faces and Voices

The perception of emotions is often suggested to be multimodal in nature, and bimodal as compared to unimodal (auditory or visual) presentation of emotional stimuli can lead to superior emotion recognition. In previous studies, contrastive aftereffects in emotion perception caused by perceptual adaptation have been shown for faces and for auditory affective vocalization, when adaptors were of the same modality. By contrast, crossmodal aftereffects in the perception of emotional vocalizations have not been demonstrated yet. In three experiments we investigated the influence of emotional voice as well as dynamic facial video adaptors on the perception of emotion-ambiguous voices morphed on an angry-to-happy continuum. Contrastive aftereffects were found for unimodal (voice) adaptation conditions, in that test voices were perceived as happier after adaptation to angry voices, and vice versa. Bimodal (voice + dynamic face) adaptors tended to elicit larger contrastive aftereffects. Importantly, crossmodal (dynamic face) adaptors also elicited substantial aftereffects in male, but not in female participants. Our results (1) support the idea of contrastive processing of emotions (2), show for the first time crossmodal adaptation effects under certain conditions, consistent with the idea that emotion processing is multimodal in nature, and (3) suggest gender differences in the sensory integration of facial and vocal emotional stimuli.     

Human face recognition in sheep: lack of configurational coding and right hemisphere advantage

Face recognition in sheep is qualitatively similar to that in humans in terms of its left visual field bias, and the effects of expertise and configural coding. The current study was designed to determine whether such effects are species specific by investigating the case of sheep recognising humans. It was found that the sheep could identify human faces and while they showed a small inversion-induced decline in discriminatory performance, this was significantly less than seen with sheep faces. In other aspects, there were qualitative differences with human face recognition compared with conspecific recognition. In contrast with sheep faces there was no left visual field advantage in the recognition of human faces and the internal features were not used at all as visual cues. The data suggest that these sheep, whilst being extensively exposed to interactions with humans, were unable to identify them with all the same 'expert' methods as were used to discriminate other sheep. This suggests that different neural systems may, to some extent, be used for recognition of sheep as opposed to human faces. The relative contribution to differential neural processing of the faces of the different species and the role of expertise are discussed.     

The many faces of research on face perception

Face perception is fundamental to human social interaction. Many different types of important information are visible in faces and the processes and mechanisms involved in extracting this information are complex and can be highly specialized. The importance of faces has long been recognized by a wide range of scientists. Importantly, the range of perspectives and techniques that this breadth has brought to face perception research has, in recent years, led to many important advances in our understanding of face processing. The articles in this issue on face perception each review a particular arena of interest in face perception, variously focusing on (i) the social aspects of face perception (attraction, recognition and emotion), (ii) the neural mechanisms underlying face perception (using brain scanning, patient data, direct stimulation of the brain, visual adaptation and single-cell recording), and (iii) comparative aspects of face perception (comparing adult human abilities with those of chimpanzees and children). Here, we introduce the central themes of the issue and present an overview of the articles.     

Face processing limitation to own species in primates: a comparative study in brown capuchins, Tonkean macaques and humans

Most primates live in social groups which survival and stability depend on individuals' abilities to create strong social relationships with other group members. The existence of those groups requires to identify individuals and to assign to each of them a social status. Individual recognition can be achieved through vocalizations but also through faces. In humans, an efficient system for the processing of own species faces exists. This specialization is achieved through experience with faces of conspecifics during development and leads to the loss of ability to process faces from other primate species. We hypothesize that a similar mechanism exists in social primates. We investigated face processing in one Old World species (genus Macaca) and in one New World species (genus Cebus). Our results show the same advantage for own species face recognition for all tested subjects. This work suggests in all species tested the existence of a common trait inherited from the primate ancestor: an efficient system to identify individual faces of own species only.