Face perception: domain specific, not process specific

Evidence that face perception is mediated by special cognitive and neural mechanisms comes from fMRI studies of the fusiform face area (FFA) and behavioral studies of the face inversion effect. Here, we used these two methods to ask whether face perception mechanisms are stimulus specific, process specific, or both. Subjects discriminated pairs of upright or inverted faces or house stimuli that differed in either the spatial distance among parts (configuration) or the shape of the parts. The FFA showed a much higher response to faces than to houses, but no preference for the configuration task over the part task. Similarly, the behavioral inversion effect was as large in the part task as the configuration task for faces, but absent in both part and configuration tasks for houses. These findings indicate that face perception mechanisms are not process specific for parts or configuration but are domain specific for face stimuli per se.     

Super-Memorizers Are Not Super-Recognizers

Humans have a natural expertise in recognizing faces. However, the nature of the interaction between this critical visual biological skill and memory is yet unclear. Here, we had the unique opportunity to test two individuals who have had exceptional success in the World Memory Championships, including several world records in face-name association memory. We designed a range of face processing tasks to determine whether superior/expert face memory skills are associated with distinctive perceptual strategies for processing faces. Superior memorizers excelled at tasks involving associative face-name learning. Nevertheless, they were as impaired as controls in tasks probing the efficiency of the face system: face inversion and the other-race effect. Super memorizers did not show increased hippocampal volumes, and exhibited optimal generic eye movement strategies when they performed complex multi-item face-name associations. Our data show that the visual computations of the face system are not malleable and are robust to acquired expertise involving extensive training of associative memory.     

Inversion leads to quantitative, not qualitative, changes in face processing

Humans are remarkably adept at recognizing objects across a wide range of views. A notable exception to this general rule is that turning a face upside down makes it particularly difficult to recognize. This striking effect has prompted speculation that inversion qualitatively changes the way faces are processed. Researchers commonly assume that configural cues strongly influence the recognition of upright, but not inverted, faces. Indeed, the assumption is so well accepted that the inversion effect itself has been taken as a hallmark of qualitative processing differences. Here, we took a novel approach to understand the inversion effect. We used response classification to obtain a direct view of the perceptual strategies underlying face discrimination and to determine whether orientation effects can be explained by differential contributions of nonlinear processes. Inversion significantly impaired performance in our face discrimination task. However, surprisingly, observers utilized similar, local regions of faces for discrimination in both upright and inverted face conditions, and the relative contributions of nonlinear mechanisms to performance were similar across orientations. Our results suggest that upright and inverted face processing differ quantitatively, not qualitatively; information is extracted more efficiently from upright faces, perhaps as a by-product of orientation-dependent expertise.     

How Well Do Computer-Generated Faces Tap Face Expertise?

The use of computer-generated (CG) stimuli in face processing research is proliferating due to the ease with which faces can be generated, standardised and manipulated. However there has been surprisingly little research into whether CG faces are processed in the same way as photographs of real faces. The present study assessed how well CG faces tap face identity expertise by investigating whether two indicators of face expertise are reduced for CG faces when compared to face photographs. These indicators were accuracy for identification of own-race faces and the other-race effect (ORE)–the well-established finding that own-race faces are recognised more accurately than other-race faces. In Experiment 1 Caucasian and Asian participants completed a recognition memory task for own- and other-race real and CG faces. Overall accuracy for own-race faces was dramatically reduced for CG compared to real faces and the ORE was significantly and substantially attenuated for CG faces. Experiment 2 investigated perceptual discrimination for own- and other-race real and CG faces with Caucasian and Asian participants. Here again, accuracy for own-race faces was significantly reduced for CG compared to real faces. However the ORE was not affected by format. Together these results signal that CG faces of the type tested here do not fully tap face expertise. Technological advancement may, in the future, produce CG faces that are equivalent to real photographs. Until then caution is advised when interpreting results obtained using CG faces.     

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.     

The Part Task of the Part-Spacing Paradigm Is Not a Pure Measurement of Part-Based Information of Faces

Background

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.

Conclusions/Significance

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.     

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.     

Neural manifestations of memory with and without awareness

Neurophysiological events responsible for different types of human memory tend to occur concurrently and are therefore difficult to measure independently. To surmount this problem, we produced perceptual priming (indicated by speeded responses) in the absence of conscious remembering. At encoding, faces appeared briefly while subjects' attention was diverted to other stimuli. Faces appeared again in either an implicit or explicit memory test. Neural correlates of priming were identified as brain potentials beginning 270 ms after face onset with more negative amplitudes for repeated than for new faces. Remembered faces, in contrast, activated a different configuration of intracranial sources producing positive potentials maximal at 600-700 ms. We thus disentangled and characterized distinct neural events associated with memory with and without awareness.     

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.     

Perceptual expertise in forensic facial image comparison

Forensic facial identification examiners are required to match the identity of faces in images that vary substantially, owing to changes in viewing conditions and in a person''s appearance. These identifications affect the course and outcome of criminal investigations and convictions. Despite calls for research on sources of human error in forensic examination, existing scientific knowledge of face matching accuracy is based, almost exclusively, on people without formal training. Here, we administered three challenging face matching tests to a group of forensic examiners with many years'' experience of comparing face images for law enforcement and government agencies. Examiners outperformed untrained participants and computer algorithms, thereby providing the first evidence that these examiners are experts at this task. Notably, computationally fusing responses of multiple experts produced near-perfect performance. Results also revealed qualitative differences between expert and non-expert performance. First, examiners'' superiority was greatest at longer exposure durations, suggestive of more entailed comparison in forensic examiners. Second, experts were less impaired by image inversion than non-expert students, contrasting with face memory studies that show larger face inversion effects in high performers. We conclude that expertise in matching identity across unfamiliar face images is supported by processes that differ qualitatively from those supporting memory for individual faces.     

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.     

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.     

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.     

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.     

Recognition of monkey faces by monkey experts

Human beings automatically discriminate human faces at the individual level. Infants aged 3 months implicitly recognise monkey faces, but this capacity disappears as recognition skills mature. Expertise is known to affect recognition capacities for different categories of stimuli that are not even face-like in their configuration. We have explored the capacity of adult experts and non-experts in primatology to recognise monkey faces in both explicit and implicit recognition tasks. In the explicit task, where subjects received the instruction to recognise a face seen previously, experts proved to be more accurate than non-experts. Experts were more affected by inversion than non-experts, suggesting that the processing of those faces is based on their configuration, as is generally observed for human faces. This replicates findings from Diamond and Carey (J Exp Psychol Gen 115:107–117, 1986) in dog experts. In the implicit recognition task, assessed by a visual paired comparison task where no instruction of recognition was given, automatic discrimination was observed for human faces but not for monkey faces. These results suggest that experience acquired by the time of adulthood did not lead the experts to develop recognition skills to the point of matching those exhibited for human 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.     

Normal greeble learning in a severe case of developmental prosopagnosia

A central question in cognitive neuroscience is whether mechanisms exist that are specialized for particular domains. One of the most commonly cited examples of a domain-specific competence is the human ability to recognize upright faces. However, according to a widely discussed alternative hypothesis, face recognition is instead performed by mechanisms specialized for processing any object class for which an individual has expertise. Faces, according to this domain-general hypothesis, are just one example of an expert class. Nonface object expertise has been intensively investigated using a training procedure involving an artificial stimulus class known as greebles. A key prediction of this hypothesis is that individuals with face recognition impairments will also have impairments with other categories that control subjects have expertise with. Our results show that a man with severe prosopagnosia performed normally throughout the standard greeble training procedure. These findings indicate that face recognition and greeble recognition rely on separate mechanisms.     

Natural Experience Modulates the Processing of Older Adult Faces in Young Adults and 3-Year-Old Children

Just like other face dimensions, age influences the way faces are processed by adults as well as by children. However, it remains unclear under what conditions exactly such influence occurs at both ages, in that there is some mixed evidence concerning the presence of a systematic processing advantage for peer faces (own-age bias) across the lifespan. Inconsistency in the results may stem from the fact that the individual’s face representation adapts to represent the most predominant age traits of the faces present in the environment, which is reflective of the individual’s specific living conditions and social experience. In the current study we investigated the processing of younger and older adult faces in two groups of adults (Experiment 1) and two groups of 3-year-old children (Experiment 2) who accumulated different amounts of experience with elderly people. Contact with elderly adults influenced the extent to which both adult and child participants showed greater discrimination abilities and stronger sensitivity to configural/featural cues in younger versus older adult faces, as measured by the size of the inversion effect. In children, the size of the inversion effect for older adult faces was also significantly correlated with the amount of contact with elderly people. These results show that, in both adults and children, visual experience with older adult faces can tune perceptual processing strategies to the point of abolishing the discrimination disadvantage that participants typically manifest for those faces in comparison to younger adult faces.     

A two-base mechanism for Escherichia coli ADP-L-glycero-D-manno-heptose 6-epimerase

ADP-l-glycero-d-manno-heptose 6-epimerase (HldD or AGME, formerly RfaD) catalyzes the inversion of configuration at C-6' ' of the heptose moiety of ADP-d-glycero-d-manno-heptose and ADP-l-glycero-d-manno-heptose. The epimerase HldD operates in the biosynthetic pathway of l-glycero-d-manno-heptose, which is a conserved sugar in the core region of lipopolysaccharide (LPS) of Gram-negative bacteria. Previous studies support a mechanism in which HldD uses its tightly bound NADP+ cofactor to oxidize directly at C-6' ', generating a ketone intermediate. A reduction of the ketone from the opposite face then occurs, generating the epimeric product. How the epimerase is able access both faces of the ketone intermediate with correct alignment of the three required components, NADPH, the ketone carbonyl, and a catalytic acid/base residue, is addressed here. It is proposed that the epimerase active site contains two catalytic pockets, each of which bears a catalytic acid/base residue that facilitates reduction of the C-6' ' ketone but leads to a distinct epimeric product. The ketone carbonyl may access either pocket via rotation about the C-5' '-C-6' ' bond of the sugar nucleotide and in doing so presents opposing faces to the bound cofactor. Evidence in support of the two-base mechanism is found in studies of two single mutants of the Escherichia coli K-12 epimerase, Y140F and K178M, both of which have severely compromised epimerase activities that are more than 3 orders of magnitude lower than that of the wild type. The catalytic competency of these two mutants in promoting redox chemistry is demonstrated with an alternate catalytic activity that requires only one catalytic base: dismutation of a C-6' ' aldehyde substrate analogue (ADP-beta-d-manno-hexodialdose) to an acid and an alcohol (ADP-beta-d-mannuronic acid and ADP-beta-d-mannose). This study identifies the two catalytic bases as tyrosine 140 and lysine 178. A one-step enzymatic conversion of mannose into ADP-beta-mannose is also described and used to make C-6' '-substituted derivatives of this sugar nucleotide.