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.     

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.     

The Early Time Course of Compensatory Face Processing in Congenital Prosopagnosia

Background

Prosopagnosia is a selective deficit in facial identification which can be either acquired, (e.g., after brain damage), or present from birth (congenital). The face recognition deficit in prosopagnosia is characterized by worse accuracy, longer reaction times, more dispersed gaze behavior and a strong reliance on featural processing.

Methods/Principal Findings

We introduce a conceptual model of an apperceptive/associative type of congenital prosopagnosia where a deficit in holistic processing is compensated by a serial inspection of isolated, informative features. Based on the model proposed we investigated performance differences in different face and shoe identification tasks between a group of 16 participants with congenital prosopagnosia and a group of 36 age-matched controls. Given enough training and unlimited stimulus presentation prosopagnosics achieved normal face identification accuracy evincing longer reaction times. The latter increase was paralleled by an equally-sized increase in stimulus presentation times needed achieve an accuracy of 80%. When the inspection time of stimuli was limited (50ms to 750ms), prosopagnosics only showed worse accuracy but no difference in reaction time. Tested for the ability to generalize from frontal to rotated views, prosopagnosics performed worse than controls across all rotation angles but the magnitude of the deficit didn''t change with increasing rotation. All group differences in accuracy, reaction or presentation times were selective to face stimuli and didn''t extend to shoes.

Conclusions/Significance

Our study provides a characterization of congenital prosopagnosia in terms of early processing differences. More specifically, compensatory processing in congenital prosopagnosia requires an inspection of faces that is sufficiently long to allow for sequential focusing on informative features. This characterization of dysfunctional processing in prosopagnosia further emphasizes fast and holistic information encoding as two defining characteristics of normal face processing.     

It’s All in the Eyes: Subcortical and Cortical Activation during Grotesqueness Perception in Autism

Atypical face processing plays a key role in social interaction difficulties encountered by individuals with autism. In the current fMRI study, the Thatcher illusion was used to investigate several aspects of face processing in 20 young adults with high-functioning autism spectrum disorder (ASD) and 20 matched neurotypical controls. “Thatcherized” stimuli were modified at either the eyes or the mouth and participants discriminated between pairs of faces while cued to attend to either of these features in upright and inverted orientation. Behavioral data confirmed sensitivity to the illusion and intact configural processing in ASD. Directing attention towards the eyes vs. the mouth in upright faces in ASD led to (1) improved discrimination accuracy; (2) increased activation in areas involved in social and emotional processing; (3) increased activation in subcortical face-processing areas. Our findings show that when explicitly cued to attend to the eyes, activation of cortical areas involved in face processing, including its social and emotional aspects, can be enhanced in autism. This suggests that impairments in face processing in autism may be caused by a deficit in social attention, and that giving specific cues to attend to the eye-region when performing behavioral therapies aimed at improving social skills may result in a better outcome.     

Baboons (Papio papio) spontaneously process the first-order but not second-order configural properties of faces

A two-alternative forced-choice discrimination task was used to assess whether baboons (N=7) spontaneously process qualitative (i.e., first-order) or quantitative (i.e., second-order) variations in the configural arrangement of facial features. Experiment 1 used as test stimuli second-order pictorial faces of humans or baboons in which the mouth and the eyes were rotated upside down relative to the normal face. Baboons readily discriminated two different normal faces but did not discriminate a normal face from its second-order modified version. Experiment 2 used human or baboon faces for which the first-order configural properties had been distorted by reversing the location of the eyes and mouth within the face. Discrimination was prompt with these stimuli. Experiment 3 replicated some of the conditions and the results of experiment 1, thus ruling out possible effects of learning. It is concluded that baboons are more adept at spontaneously processing first- than second-order configural facial properties, similar to what is known in the human developmental literature.     

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.     

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.     

Scanning Strategies Do Not Modulate Face Identification: Eye-Tracking and Near-Infrared Spectroscopy Study

Background

During face identification in humans, facial information is sampled (seeing) and handled (processing) in ways that are influenced by the kind of facial image type, such as a self-image or an image of another face. However, the relationship between seeing and information processing is seldom considered. In this study, we aimed to reveal this relationship using simultaneous eye-tracking measurements and near-infrared spectroscopy (NIRS) in face identification tasks.

Methodology/Principal Findings

22 healthy adult subjects (8 males and 14 females) were shown facial morphing movies in which an initial facial image gradually changed into another facial image (that is, the subject''s own face was changed to a familiar face). The fixation patterns on facial features were recorded, along with changes in oxyhemoglobin (oxyHb) levels in the frontal lobe, while the subjects identified several faces. In the self-face condition (self-face as the initial image), hemodynamic activity around the right inferior frontal gyrus (IFG) was significantly greater than in the familiar-face condition. On the other hand, the scanning strategy was similar in almost all conditions with more fixations on the eyes and nose than on other areas. Fixation time on the eye area did not correlate with changes in oxyHb levels, and none of the scanning strategy indices could estimate the hemodynamic changes.

Conclusions/Significance

We conclude that hemodynamic activity, i.e., the means of processing facial information, is not always modulated by the face-scanning strategy, i.e., the way of seeing, and that the right IFG plays important roles in both self-other facial discrimination and self-evaluation.     

Part-Based and Configural Processing of Owner's Face in Dogs

Dogs exhibit characteristic looking patterns when looking at human faces but little is known about what the underlying cognitive mechanisms are and how much these are influenced by individual experience. In Experiment 1, seven dogs were trained in a simultaneous discrimination procedure to assess whether they could discriminate a) the owner''s face parts (eyes, nose or mouth) presented in isolation and b) whole faces where the same parts were covered. Dogs discriminated all the three parts of the owner''s face presented in isolation, but needed fewer sessions to reach the learning criterion for the eyes than for both nose and mouth. Moreover, covering the eyes region significantly disrupted face discriminability compared to the whole face condition while such difference was not found when the nose or mouth was hidden. In Experiment 2, dogs were presented with manipulated images of the owner''s face (inverted, blurred, scrambled, grey-scale) to test the relative contribution of part-based and configural processing in the discrimination of human faces. Furthermore, by comparing the dogs enrolled in the previous experiment and seven ‘naïve’ dogs we examined if the relative contribution of part-based and configural processing was affected by dogs'' experience with the face stimuli. Naïve dogs discriminated the owner only when configural information was provided, whereas expert dogs could discriminate the owner also when part-based processing was necessary. The present study provides the first evidence that dogs can discriminate isolated internal features of a human face and corroborate previous reports of salience of the eyes region for human face processing. Although the reliance on part-perception may be increased by specific experience, our findings suggest that human face discrimination by dogs relies mainly on configural rather than on part-based elaboration.     

Individual recognition is associated with holistic face processing in Polistes paper wasps in a species-specific way

Most recognition is based on identifying features, but specialization for face recognition in primates relies on a different mechanism, termed ‘holistic processing’ where facial features are bound together into a gestalt which is more than the sum of its parts. Here, we test whether individual face recognition in paper wasps also involved holistic processing using a modification of the classic part-whole test in two related paper wasp species: Polistes fuscatus, which use facial patterns to individually identify conspecifics, and Polistes dominula, which lacks individual recognition. We show that P. fuscatus use holistic processing to discriminate between P. fuscatus face images but not P. dominula face images. By contrast, P. dominula do not rely on holistic processing to discriminate between conspecific or heterospecific face images. Therefore, P. fuscatus wasps have evolved holistic face processing, but this ability is highly specific and shaped by species-specific and stimulus-specific selective pressures. Convergence towards holistic face processing in distant taxa (primates, wasps) as well as divergence among closely related taxa with different recognition behaviour (P. dominula, P. fuscatus) suggests that holistic processing may be a universal adaptive strategy to facilitate expertise in face recognition.     

Visual search for orientation of faces by a chimpanzee (<Emphasis Type="Italic">Pan troglodytes</Emphasis>): face-specific upright superiority and the role of facial configural properties

A previous experiment showed that a chimpanzee performed better in searching for a target human face that differed in orientation from distractors when the target had an upright orientation than when targets had inverted or horizontal orientation [Tomonaga (1999a) Primate Res 15:215–229]. This upright superiority effect was also seen when using chimpanzee faces as targets but not when using photographs of a house. The present study sought to extend these results and explore factors affecting the face-specific upright superiority effect. Upright superiority was shown in a visual search for orientation when caricaturized human faces and dog faces were used as stimuli for the chimpanzee but not when shapes of a hand and chairs were presented. Thus, the configural properties of facial features, which cause an inversion effect in face recognition in humans and chimpanzees, were thought to be a source of the upright superiority effect in the visual search process. To examine this possibility, various stimuli manipulations were introduced in subsequent experiments. The results clearly show that the configuration of facial features plays a critical role in the upright superiority effect, and strongly suggest similarity in face processing in humans and chimpanzees.     

Context modulation of facial emotion perception differed by individual difference

Background

Certain facial configurations are believed to be associated with distinct affective meanings (i.e. basic facial expressions), and such associations are common across cultures (i.e. universality of facial expressions). However, recently, many studies suggest that various types of contextual information, rather than facial configuration itself, are important factor for facial emotion perception.

Methodology/Principal Findings

To examine systematically how contextual information influences individuals’ facial emotion perception, the present study estimated direct observers’ perceptual thresholds for detecting negative facial expressions via a forced-choice psychophysical procedure using faces embedded in various emotional contexts. We additionally measured the individual differences in affective information-processing tendency (BIS/BAS) as a possible factor that may determine the extent to which contextual information on facial emotion perception is used. It was found that contextual information influenced observers'' perceptual thresholds for facial emotion. Importantly, individuals’ affective-information tendencies modulated the extent to which they incorporated context information into their facial emotion perceptions.

Conclusions/Significance

The findings of this study suggest that facial emotion perception not only depends on facial configuration, but the context in which the face appears as well. This contextual influence appeared differently with individual’s characteristics of information processing. In summary, we conclude that individual character traits, as well as facial configuration and the context in which a face appears, need to be taken into consideration regarding facial emotional perception.     

Spontaneous gender categorization in masking and priming studies: key for distinguishing Jane from John Doe but not Madonna from Sinatra

Facial recognition is key to social interaction, however with unfamiliar faces only generic information, in the form of facial stereotypes such as gender and age is available. Therefore is generic information more prominent in unfamiliar versus familiar face processing? In order to address the question we tapped into two relatively disparate stages of face processing. At the early stages of encoding, we employed perceptual masking to reveal that only perception of unfamiliar face targets is affected by the gender of the facial masks. At the semantic end; using a priming paradigm, we found that while to-be-ignored unfamiliar faces prime lexical decisions to gender congruent stereotypic words, familiar faces do not. Our findings indicate that gender is a more salient dimension in unfamiliar relative to familiar face processing, both in early perceptual stages as well as later semantic stages of person construal.     

Symmetry and Human Facial Attractiveness

Symmetry may act as a marker of phenotypic and genetic quality and is preferred during mate selection in a variety of species. Measures of human body symmetry correlate with attractiveness, but studies manipulating human face images report a preference for asymmetry. These results may reflect unnatural feature shapes and changes in skin textures introduced by image processing. When the shape of facial features is varied (with skin textures held constant), increasing symmetry of face shape increases ratings of attractiveness for both male and female faces. These findings imply facial symmetry may have a positive impact on mate selection in humans.     

Infant monkeys' visual responses to drawings of normal and distorted faces

Face-like patterns attract attention from both human and nonhuman primates. The present study explored the facial preferences in infant pigtailed macaques (Macaca nemestrina). Twenty-five subjects looked at 20 paired drawings of adult conspecific monkey faces, and their looking time was recorded. The facial features in the drawings were arranged in positions ranging from a normal to a scrambled face. The subjects looked at the normal face more than expected by chance (P < .02), suggesting a preference, whereas the distorted faces were observed randomly. The normal face may have been preferred because the eyes were in a normal position within the facial outline. Am. J. Primatol. 44:169–174, 1998. © 1998 Wiley-Liss, Inc.     

Testosterone-mediated sex differences in the face shape during adolescence: subjective impressions and objective features

Sex identification of a face is essential for social cognition. Still, perceptual cues indicating the sex of a face, and mechanisms underlying their development, remain poorly understood. Previously, our group described objective age- and sex-related differences in faces of healthy male and female adolescents (12–18 years of age), as derived from magnetic resonance images (MRIs) of the adolescents' heads. In this study, we presented these adolescent faces to 60 female raters to determine which facial features most reliably predicted subjective sex identification. Identification accuracy correlated highly with specific MRI-derived facial features (e.g. broader forehead, chin, jaw, and nose). Facial features that most reliably cued male identity were associated with plasma levels of testosterone (above and beyond age). Perceptible sex differences in face shape are thus associated with specific facial features whose emergence may be, in part, driven by testosterone.     

Object recognition: holistic representations in the monkey brain

Cognitive-psychological and neuropsychological studies suggest that the human brain processes facial information in a distinct manner, relying on mechanisms that are anatomically and functionally different from those underlying the recognition of other objects. Face recognition, for instance, can be disrupted selectively as a result of localized brain damage, and relies strongly on holistic information rather than on the mere processing of local features. Similarly, in the non-human primate, distinct neocortical and limbic structures have cell populations responding specifically to face stimuli and only weakly to other visual patterns. Moreover, such cells tend to respond to the entire configuration of a face rather than to individual facial features. But are faces the only objects represented in this way? Here I present some evidence suggesting that at least one aspect of facial processing, the processing of holistic information, may be employed by the primate brain when recognizing any arbitrary homogeneous class of even artificial objects, which the monkey has to individually learn, remember, and recognize again and again from among a large number of distractors sharing a number of common features with the target. Acquiring such an expertise can induce configurational selectivity in the response of neurons in the visual system. Our findings suggests that regarding their neural encoding faces are unlikely to be 'special', but they rather are the default 'special class' of the primate visual system.     

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.     

Observed Touch on a Non-Human Face Is Not Remapped onto the Human Observer's Own Face

Visual remapping of touch (VRT) is a phenomenon in which seeing a human face being touched enhances detection of tactile stimuli on the observer''s own face, especially when the observed face expresses fear. This study tested whether VRT would occur when seeing touch on monkey faces and whether it would be similarly modulated by facial expressions. Human participants detected near-threshold tactile stimulation on their own cheeks while watching fearful, happy, and neutral human or monkey faces being concurrently touched or merely approached by fingers. We predicted minimal VRT for neutral and happy monkey faces but greater VRT for fearful monkey faces. The results with human faces replicated previous findings, demonstrating stronger VRT for fearful expressions than for happy or neutral expressions. However, there was no VRT (i.e. no difference between accuracy in touch and no-touch trials) for any of the monkey faces, regardless of facial expression, suggesting that touch on a non-human face is not remapped onto the somatosensory system of the human observer.