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.     

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.     

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.     

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.     

Early category-specific cortical activation revealed by visual stimulus inversion

Visual categorization may already start within the first 100-ms after stimulus onset, in contrast with the long-held view that during this early stage all complex stimuli are processed equally and that category-specific cortical activation occurs only at later stages. The neural basis of this proposed early stage of high-level analysis is however poorly understood. To address this question we used magnetoencephalography and anatomically-constrained distributed source modeling to monitor brain activity with millisecond-resolution while subjects performed an orientation task on the upright and upside-down presented images of three different stimulus categories: faces, houses and bodies. Significant inversion effects were found for all three stimulus categories between 70-100-ms after picture onset with a highly category-specific cortical distribution. Differential responses between upright and inverted faces were found in well-established face-selective areas of the inferior occipital cortex and right fusiform gyrus. In addition, early category-specific inversion effects were found well beyond visual areas. Our results provide the first direct evidence that category-specific processing in high-level category-sensitive cortical areas already takes place within the first 100-ms of visual processing, significantly earlier than previously thought, and suggests the existence of fast category-specific neocortical routes in the human brain.     

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.     

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.     

Sensory competition in the face processing areas of the human brain

The concurrent presentation of multiple stimuli in the visual field may trigger mutually suppressive interactions throughout the ventral visual stream. While several studies have been performed on sensory competition effects among non-face stimuli relatively little is known about the interactions in the human brain for multiple face stimuli. In the present study we analyzed the neuronal basis of sensory competition in an event-related functional magnetic resonance imaging (fMRI) study using multiple face stimuli. We varied the ratio of faces and phase-noise images within a composite display with a constant number of peripheral stimuli, thereby manipulating the competitive interactions between faces. For contralaterally presented stimuli we observed strong competition effects in the fusiform face area (FFA) bilaterally and in the right lateral occipital area (LOC), but not in the occipital face area (OFA), suggesting their different roles in sensory competition. When we increased the spatial distance among pairs of faces the magnitude of suppressive interactions was reduced in the FFA. Surprisingly, the magnitude of competition depended on the visual hemifield of the stimuli: ipsilateral stimulation reduced the competition effects somewhat in the right LOC while it increased them in the left LOC. This suggests a left hemifield dominance of sensory competition. Our results support the sensory competition theory in the processing of multiple faces and suggests that sensory competition occurs in several cortical areas in both cerebral hemispheres.     

Evidence against perceptual bias views for symmetry preferences in human faces

Symmetrical human faces are attractive. Two explanations have been proposed to account for symmetry preferences: (i) the evolutionary advantage view, which posits that symmetry advertises mate quality and (ii) the perceptual bias view, which posits that symmetry preferences are a consequence of greater ease of processing symmetrical images in the visual system. Here, we show that symmetry preferences are greater when face images are upright than when inverted. This is evidence against a simple perceptual bias view, which suggests symmetry preference should be constant across orientation about a vertical axis. We also show that symmetry is preferred even in familiar faces, a finding that is unexpected by perceptual bias views positing that symmetry is only attractive because it represents a familiar prototype of that particular class of stimuli.     

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.     

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.     

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.     

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.     

Adults' awareness of faces follows newborns' looking preferences

From the first days of life, humans preferentially orient towards upright faces, likely reflecting innate subcortical mechanisms. Here, we show that binocular rivalry can reveal face detection mechanisms in adults that are surprisingly similar to inborn face detection mechanism. We used continuous flash suppression (CFS), a variant of binocular rivalry, to render stimuli invisible at the beginning of each trial and measured the time upright and inverted stimuli needed to overcome such interocular suppression. Critically, specific stimulus properties previously shown to modulate looking preferences in neonates similarly modulated adults' awareness of faces presented during CFS. First, the advantage of upright faces in overcoming CFS was strongly modulated by contrast polarity and direction of illumination. Second, schematic patterns consisting of three dark blobs were suppressed for shorter durations when the arrangement of these blobs respected the face-like configuration of the eyes and the mouth, and this effect was modulated by contrast polarity. No such effects were obtained in a binocular control experiment not involving CFS, suggesting a crucial role for face-sensitive mechanisms operating outside of conscious awareness. These findings indicate that visual awareness of faces in adults is governed by perceptual mechanisms that are sensitive to similar stimulus properties as those modulating newborns' face preferences.     

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.     

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.     

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.     

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 neuropsychology of face perception: beyond simple dissociations and functional selectivity

Face processing relies on a distributed, patchy network of cortical regions in the temporal and frontal lobes that respond disproportionately to face stimuli, other cortical regions that are not even primarily visual (such as somatosensory cortex), and subcortical structures such as the amygdala. Higher-level face perception abilities, such as judging identity, emotion and trustworthiness, appear to rely on an intact face-processing network that includes the occipital face area (OFA), whereas lower-level face categorization abilities, such as discriminating faces from objects, can be achieved without OFA, perhaps via the direct connections to the fusiform face area (FFA) from several extrastriate cortical areas. Some lesion, transcranial magnetic stimulation (TMS) and functional magnetic resonance imaging (fMRI) findings argue against a strict feed-forward hierarchical model of face perception, in which the OFA is the principal and common source of input for other visual and non-visual cortical regions involved in face perception, including the FFA, face-selective superior temporal sulcus and somatosensory cortex. Instead, these findings point to a more interactive model in which higher-level face perception abilities depend on the interplay between several functionally and anatomically distinct neural regions. Furthermore, the nature of these interactions may depend on the particular demands of the task. We review the lesion and TMS literature on this topic and highlight the dynamic and distributed nature of face processing.