Discriminating grotesque from typical faces: evidence from the Thatcher illusion

The discrimination of thatcherized faces from typical faces was explored in two simultaneous alternative forced choice tasks. Reaction times (RTs) and errors were measured in a behavioural task. Brain activation was measured in an equivalent fMRI task. In both tasks, participants were tested with upright and inverted faces. Participants were also tested on churches in the behavioural task. The behavioural task confirmed the face specificity of the illusion (by comparing inversion effects for faces against churches) but also demonstrated that the discrimination was primarily, although not exclusively, driven by attending to eyes. The fMRI task showed that, relative to inverted faces, upright grotesque faces are discriminated via activation of a network of emotion/social evaluation processing areas. On the other hand, discrimination of inverted thatcherized faces was associated with increased activation of brain areas that are typically involved in perceptual processing of faces.     

Face inversion reduces the persistence of global form and its neural correlates

Face inversion produces a detrimental effect on face recognition. The extent to which the inversion of faces and other kinds of objects influences the perceptual binding of visual information into global forms is not known. We used a behavioral method and functional MRI (fMRI) to measure the effect of face inversion on visual persistence, a type of perceptual memory that reflects sustained awareness of global form. We found that upright faces persisted longer than inverted versions of the same images; we observed a similar effect of inversion on the persistence of animal stimuli. This effect of inversion on persistence was evident in sustained fMRI activity throughout the ventral visual hierarchy, including the lateral occipital area (LO), two face-selective visual areas--the fusiform face area (FFA) and the occipital face area (OFA)--and several early visual areas. V1 showed the same initial fMRI activation to upright and inverted forms but this activation lasted longer for upright stimuli. The inversion effect on persistence-related fMRI activity in V1 and other retinotopic visual areas demonstrates that higher-tier visual areas influence early visual processing via feedback. This feedback effect on figure-ground processing is sensitive to the orientation of the figure.     

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.     

Are faces of different species perceived categorically by human observers?

What are the species boundaries of face processing? Using a face-feature morphing algorithm, image series intermediate between human, monkey (macaque), and bovine faces were constructed. Forced-choice judgement of these images showed sharply bounded categories for upright face images of each species. These predicted the perceptual discrimination boundaries for upright monkey-cow and cow-human images, but not human-monkey images. Species categories were also well-judged for inverted face images, but these did not give sharpened discrimination (categorical perception) at the category boundaries. While categorical species judgements are made reliably, only the distinction between primate faces and cow faces appears to be categorically perceived, and only in upright faces. One inference is that humans may judge monkey faces in terms of human characteristics, albeit distinctive ones.     

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 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.     

Start position strongly influences fixation patterns during face processing: difficulties with eye movements as a measure of information use

Fixation patterns are thought to reflect cognitive processing and, thus, index the most informative stimulus features for task performance. During face recognition, initial fixations to the center of the nose have been taken to indicate this location is optimal for information extraction. However, the use of fixations as a marker for information use rests on the assumption that fixation patterns are predominantly determined by stimulus and task, despite the fact that fixations are also influenced by visuo-motor factors. Here, we tested the effect of starting position on fixation patterns during a face recognition task with upright and inverted faces. While we observed differences in fixations between upright and inverted faces, likely reflecting differences in cognitive processing, there was also a strong effect of start position. Over the first five saccades, fixation patterns across start positions were only coarsely similar, with most fixations around the eyes. Importantly, however, the precise fixation pattern was highly dependent on start position with a strong tendency toward facial features furthest from the start position. For example, the often-reported tendency toward the left over right eye was reversed for the left starting position. Further, delayed initial saccades for central versus peripheral start positions suggest greater information processing prior to the initial saccade, highlighting the experimental bias introduced by the commonly used center start position. Finally, the precise effect of face inversion on fixation patterns was also dependent on start position. These results demonstrate the importance of a non-stimulus, non-task factor in determining fixation patterns. The patterns observed likely reflect a complex combination of visuo-motor effects and simple sampling strategies as well as cognitive factors. These different factors are very difficult to tease apart and therefore great caution must be applied when interpreting absolute fixation locations as indicative of information use, particularly at a fine spatial scale.     

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.     

Famous faces demand attention due to reduced inhibitory processing

People have particular difficulty ignoring distractors that depict faces. This phenomenon has been attributed to the high level of biological significance that faces carry. The current study aimed to elucidate the mechanism by which faces gain processing priority. We used a focused attention paradigm that tracks the influence of a distractor over time and provides a measure of inhibitory processing. Upright famous faces served as test stimuli and inverted versions of the faces as well as upright non-face objects served as control stimuli. The results revealed that although all of the stimuli elicited similar levels of distraction, only inverted distractor faces and non-face objects elicited inhibitory effects. The lack of inhibitory effects for upright famous faces provides novel evidence that reduced inhibitory processing underlies the mandatory nature of face processing.     

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.     

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 neural basis of the behavioral face-inversion effect

Two of the most robust markers for "special" face processing are the behavioral face-inversion effect (FIE)-the disproportionate drop in recognition of upside-down (inverted) stimuli relative to upright faces-and the face-selective fMRI response in the fusiform face area (FFA). However, the relationship between these two face-selective markers is unknown. Here we report that the behavioral FIE is closely associated with the fMRI response in the FFA, but not in other face-selective or object-selective regions. The FFA and the face-selective region in the superior temporal sulcus (f_STS), but not the occipital face-selective region (OFA), showed a higher response to upright than inverted faces. However, only in the FFA was this fMRI-FIE positively correlated across subjects with the behavioral FIE. Second, the FFA, but not the f_STS, showed greater neural sensitivity to differences between faces when they were upright than inverted, suggesting a possible neural mechanism for the behavioral FIE. Although a similar trend was found in the occipital face area (OFA), it was less robust than the FFA. Taken together, our data suggest that among the face-selective and object-selective regions, the FFA is a primary neural source of the behavioral FIE.     

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.     

Implicit Processing of the Eyes and Mouth: Evidence from Human Electrophysiology

The current study examined the time course of implicit processing of distinct facial features and the associate event-related potential (ERP) components. To this end, we used a masked priming paradigm to investigate implicit processing of the eyes and mouth in upright and inverted faces, using a prime duration of 33 ms. Two types of prime-target pairs were used: 1. congruent (e.g., open eyes only in both prime and target or open mouth only in both prime and target); 2. incongruent (e.g., open mouth only in prime and open eyes only in target or open eyes only in prime and open mouth only in target). The identity of the faces changed between prime and target. Participants pressed a button when the target face had the eyes open and another button when the target face had the mouth open. The behavioral results showed faster RTs for the eyes in upright faces than the eyes in inverted faces, the mouth in upright and inverted faces. Moreover they also revealed a congruent priming effect for the mouth in upright faces. The ERP findings showed a face orientation effect across all ERP components studied (P1, N1, N170, P2, N2, P3) starting at about 80 ms, and a congruency/priming effect on late components (P2, N2, P3), starting at about 150 ms. Crucially, the results showed that the orientation effect was driven by the eye region (N170, P2) and that the congruency effect started earlier (P2) for the eyes than for the mouth (N2). These findings mark the time course of the processing of internal facial features and provide further evidence that the eyes are automatically processed and that they are very salient facial features that strongly affect the amplitude, latency, and distribution of neural responses to faces.     

Visual discrimination of primate species based on faces in chimpanzees

Many primate studies have investigated discrimination of individual faces within the same species. However, few studies have looked at discrimination between primate species faces at the categorical level. This study systematically examined the factors important for visual discrimination between primate species faces in chimpanzees, including: colour, orientation, familiarity, and perceptual similarity. Five adult female chimpanzees were tested on their ability to discriminate identical and categorical (non-identical) images of different primate species faces in a series of touchscreen matching-to-sample experiments. Discrimination performance for chimpanzee, gorilla, and orangutan faces was better in colour than in greyscale. An inversion effect was also found, with higher accuracy for upright than inverted faces. Discrimination performance for unfamiliar (baboon and capuchin monkey) and highly familiar (chimpanzee and human) but perceptually different species was equally high. After excluding effects of colour and familiarity, difficulty in discriminating between different species faces can be best explained by their perceptual similarity to each other. Categorical discrimination performance for unfamiliar, perceptually similar faces (gorilla and orangutan) was significantly worse than unfamiliar, perceptually different faces (baboon and capuchin monkey). Moreover, multidimensional scaling analysis of the image similarity data based on local feature matching revealed greater similarity between chimpanzee, gorilla and orangutan faces than between human, baboon and capuchin monkey faces. We conclude our chimpanzees appear to perceive similarity in primate faces in a similar way to humans. Information about perceptual similarity is likely prioritized over the potential influence of previous experience or a conceptual representation of species for categorical discrimination between species faces.     

Impaired Perception of Facial Motion in Autism Spectrum Disorder

Facial motion is a special type of biological motion that transmits cues for socio-emotional communication and enables the discrimination of properties such as gender and identity. We used animated average faces to examine the ability of adults with autism spectrum disorders (ASD) to perceive facial motion. Participants completed increasingly difficult tasks involving the discrimination of (1) sequences of facial motion, (2) the identity of individuals based on their facial motion and (3) the gender of individuals. Stimuli were presented in both upright and upside-down orientations to test for the difference in inversion effects often found when comparing ASD with controls in face perception. The ASD group’s performance was impaired relative to the control group in all three tasks and unlike the control group, the individuals with ASD failed to show an inversion effect. These results point to a deficit in facial biological motion processing in people with autism, which we suggest is linked to deficits in lower level motion processing we have previously reported.     

Altering Visual Perception Abnormalities: A Marker for Body Image Concern

The body image concern (BIC) continuum ranges from a healthy and positive body image, to clinical diagnoses of abnormal body image, like body dysmorphic disorder (BDD). BDD and non-clinical, yet high-BIC participants have demonstrated a local visual processing bias, characterised by reduced inversion effects. To examine whether this bias is a potential marker of BDD, the visual processing of individuals across the entire BIC continuum was examined. Dysmorphic Concern Questionnaire (DCQ; quantified BIC) scores were expected to correlate with higher discrimination accuracy and faster reaction times of inverted stimuli, indicating reduced inversion effects (occurring due to increased local visual processing). Additionally, an induced global or local processing bias via Navon stimulus presentation was expected to alter these associations. Seventy-four participants completed the DCQ and upright-inverted face and body stimulus discrimination task. Moderate positive associations were revealed between DCQ scores and accuracy rates for inverted face and body stimuli, indicating a graded local bias accompanying increases in BIC. This relationship supports a local processing bias as a marker for BDD, which has significant assessment implications. Furthermore, a moderate negative relationship was found between DCQ score and inverted face accuracy after inducing global processing, indicating the processing bias can temporarily be reversed in high BIC individuals. Navon stimuli were successfully able to alter the visual processing of individuals across the BIC continuum, which has important implications for treating BDD.     

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.     

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.