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 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.     

Agnosia.

Object recognition can break down in a variety of ways after brain damage. The resulting different forms of agnosia provide us with useful constraints on theories of normal object recognition. Recent studies suggest a division of labor for the recognition of different types of stimuli (common objects, words, faces, direction of eye gaze, spatial relations among parts of the human body), a high degree of interactivity in the processes underlying object recognition, and the possibility that recognition and awareness of recognition may be neurally distinct.     

Orientation-contingent face aftereffects and implications for face-coding mechanisms

Humans have an impressive ability to discriminate between faces despite their similarity as visual patterns. This expertise relies on configural coding of spatial relations between face features and/or holistic coding of overall facial structure. These expert face-coding mechanisms appear to be engaged most effectively by upright faces, with inverted faces engaging primarily feature-coding mechanisms. We show that opposite figural aftereffects can be induced simultaneously for upright and inverted faces, demonstrating that distinct neural populations code upright and inverted faces. This result also suggests that expert (upright) face-coding mechanisms can be selectively adapted. These aftereffects occur for judgments of face normality and face gender and are robust to changes in face size, ruling out adaptation of low-level, retinotopically organized coding mechanisms. Our results suggest a resolution of a paradox in the face recognition literature. Neuroimaging studies have found surprisingly little orientation selectivity in the fusiform face area (FFA) despite evidence that this region plays a role in expert face coding and that expert face-coding mechanisms are selectively engaged by upright faces. Our results, demonstrating orientation-contingent adaptation of face-coding mechanisms, suggest that the FFA's apparent lack of orientation selectivity may be an artifact of averaging across distinct populations within the FFA that respond to upright and inverted faces.     

Haptic object perception: spatial dimensionality and relation to vision

Enabled by the remarkable dexterity of the human hand, specialized haptic exploration is a hallmark of object perception by touch. Haptic exploration normally takes place in a spatial world that is three-dimensional; nevertheless, stimuli of reduced spatial dimensionality are also used to display spatial information. This paper examines the consequences of full (three-dimensional) versus reduced (two-dimensional) spatial dimensionality for object processing by touch, particularly in comparison with vision. We begin with perceptual recognition of common human-made artefacts, then extend our discussion of spatial dimensionality in touch and vision to include faces, drawing from research on haptic recognition of facial identity and emotional expressions. Faces have often been characterized as constituting a specialized input for human perception. We find that contrary to vision, haptic processing of common objects is impaired by reduced spatial dimensionality, whereas haptic face processing is not. We interpret these results in terms of fundamental differences in object perception across the modalities, particularly the special role of manual exploration in extracting a three-dimensional structure.     

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).     

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.     

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.     

Does Facial Resemblance Enhance Cooperation?

Facial self-resemblance has been proposed to serve as a kinship cue that facilitates cooperation between kin. In the present study, facial resemblance was manipulated by morphing stimulus faces with the participants'' own faces or control faces (resulting in self-resemblant or other-resemblant composite faces). A norming study showed that the perceived degree of kinship was higher for the participants and the self-resemblant composite faces than for actual first-degree relatives. Effects of facial self-resemblance on trust and cooperation were tested in a paradigm that has proven to be sensitive to facial trustworthiness, facial likability, and facial expression. First, participants played a cooperation game in which the composite faces were shown. Then, likability ratings were assessed. In a source memory test, participants were required to identify old and new faces, and were asked to remember whether the faces belonged to cooperators or cheaters in the cooperation game. Old-new recognition was enhanced for self-resemblant faces in comparison to other-resemblant faces. However, facial self-resemblance had no effects on the degree of cooperation in the cooperation game, on the emotional evaluation of the faces as reflected in the likability judgments, and on the expectation that a face belonged to a cooperator rather than to a cheater. Therefore, the present results are clearly inconsistent with the assumption of an evolved kin recognition module built into the human face recognition system.     

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.     

Familiar Face Detection in 180ms

The visual system is tuned for rapid detection of faces, with the fastest choice saccade to a face at 100ms. Familiar faces have a more robust representation than do unfamiliar faces, and are detected faster in the absence of awareness and with reduced attentional resources. Faces of family and close friends become familiar over a protracted period involving learning the unique visual appearance, including a view-invariant representation, as well as person knowledge. We investigated the effect of personal familiarity on the earliest stages of face processing by using a saccadic-choice task to measure how fast familiar face detection can happen. Subjects made correct and reliable saccades to familiar faces when unfamiliar faces were distractors at 180ms—very rapid saccades that are 30 to 70ms earlier than the earliest evoked potential modulated by familiarity. By contrast, accuracy of saccades to unfamiliar faces with familiar faces as distractors did not exceed chance. Saccades to faces with object distractors were even faster (110 to 120 ms) and equivalent for familiar and unfamiliar faces, indicating that familiarity does not affect ultra-rapid saccades. We propose that detectors of diagnostic facial features for familiar faces develop in visual cortices through learning and allow rapid detection that precedes explicit recognition of identity.     

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.     

Using Effort to Measure Reward Value of Faces in Children with Autism

According to one influential account, face processing atypicalities in autism reflect reduced reward value of faces, which results in limited attention to faces during development and a consequent failure to acquire face expertise. Surprisingly, however, there is a paucity of work directly investigating the reward value of faces for individuals with autism and the evidence for diminished face rewards in this population remains equivocal. In the current study, we measured how hard children with autism would work to view faces, using an effortful key-press sequence, and whether they were sensitive to the differential reward value of attractive and unattractive faces. Contrary to expectations, cognitively able children with autism did not differ from typically developing children of similar age and ability in their willingness to work to view faces. Moreover, the effort expended was strongly positively correlated with facial attractiveness ratings in both groups of children. There was also no evidence of atypical reward values for other, less social categories (cars and inverted faces) in the children with autism. These results speak against the possibility that face recognition difficulties in autism are explained by atypical reward value of faces.     

The effect of face inversion on activity in human neural systems for face and object perception

The differential effect of stimulus inversion on face and object recognition suggests that inverted faces are processed by mechanisms for the perception of other objects rather than by face perception mechanisms. We investigated the face inversion using functional magnetic resonance imaging (fMRI). The principal effect of face inversion on was an increased response in ventral extrastriate regions that respond preferentially to another class of objects (houses). In contrast, house inversion did not produce a similar change in face-selective regions. Moreover, stimulus inversion had equivalent, minimal effects for faces in in face-selective regions and for houses in house-selective regions. The results suggest that the failure of face perception systems with inverted faces leads to the recruitment of processing resources in object perception systems, but this failure is not reflected by altered activity in face perception systems.     

Are All Types of Expertise Created Equal? Car Experts Use Different Spatial Frequency Scales for Subordinate Categorization of Cars and Faces

A much-debated question in object recognition is whether expertise for faces and expertise for non-face objects utilize common perceptual information. We investigated this issue by assessing the diagnostic information required for different types of expertise. Specifically, we asked whether face categorization and expert car categorization at the subordinate level relies on the same spatial frequency (SF) scales. Fifteen car experts and fifteen novices performed a category verification task with spatially filtered images of faces, cars, and airplanes. Images were categorized based on their basic (e.g. “car”) and subordinate level (e.g. “Japanese car”) identity. The effect of expertise was not evident when objects were categorized at the basic level. However, when the car experts categorized faces and cars at the subordinate level, the two types of expertise required different kinds of SF information. Subordinate categorization of faces relied on low SFs more than on high SFs, whereas subordinate expert car categorization relied on high SFs more than on low SFs. These findings suggest that expertise in the recognition of objects and faces do not utilize the same type of information. Rather, different types of expertise require different types of diagnostic visual information.     

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.     

Spatial aspects of spontaneous object grouping by young chimpanzees(Pan troglodytes)

I report spontaneous spatial object grouping in five chimpanzees (Pan troglodytes)ranging from 1 to 4 years of age. I recorded subjects' spontaneous interactions with groups of objects, noting the spatial relations in the groupings and the constructive processes that the subjects adopted. Though one subject developed vertical stacks, none of them realized horizontal alignments or spatial correspondences between groups. All subjects showed consistent trends in their constructive processes toward manipulating objects in relation to the body: they increasingly manipulated objects globally, that is to say, they moved or held objects together with the same part of the body. They also increasingly placed objects on the body or in correspondence to their symmetrical body parts. The increasing importance assigned by chimpanzees to body- object relations over object- object relations contrasts with human developmental trends in the domain of manipulative space.     

The neural basis of object perception

Humans can recognize an object within a fraction of a second, even if there are no clues about what kind of object it might be. Recent findings have identified functional properties of extrastriate regions in the ventral visual pathway that are involved in the representation and perception of objects and faces. The functional properties of these regions, and the correlation between the activation of these regions and visual recognition, indicate that the lateral and ventral occipito-temporal areas are important in perceiving and recognizing objects and faces.