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.     

Higher-level mechanisms detect facial symmetry

The role of symmetry detection in early visual processing and the sensitivity of biological visual systems to symmetry across a wide range of organisms suggest that symmetry can be detected by low-level visual mechanisms. However, computational and functional considerations suggest that higher-level mechanisms may also play a role in facial symmetry detection. We tested this hypothesis by examining whether symmetry detection is better for faces than comparable patterns, which share low-level properties with faces. Symmetry detection was better for upright faces than for inverted faces (experiment 1) and contrast-reversed faces (experiment 2), implicating high-level mechanisms in facial symmetry detection. In addition, facial symmetry detection was sensitive to spatial scale, unlike low-level symmetry detection mechanisms (experiment 3), and showed greater sensitivity to a 45 degrees deviation from vertical than is found for other aspects of face perception (experiment 4). These results implicate specialized, higher-level mechanisms in the detection of facial symmetry. This specialization may reflect perceptual learning resulting from extensive experience detecting symmetry in faces or evolutionary selection pressures associated with the important role of facial symmetry in mate choice and 'mind-reading' or both.     

The effect of real-world personal familiarity on the speed of face information processing

Background

Previous studies have explored the effects of familiarity on various kinds of visual face judgments, yet the role of familiarity in face processing is not fully understood. Across different face judgments and stimulus sets, the data is equivocal as to whether or not familiarity impacts recognition processes.

Methodology/Principal Findings

Here, we examine the effect of real-world personal familiarity in three simple delayed-match-to-sample tasks in which subjects were required to match faces on the basis of orientation (upright v. inverted), gender and identity. We find that subjects had a significant speed advantage with familiar faces in all three tasks, with large effects for the gender and identity matching tasks.

Conclusion/Significance

Our data indicates that real-world experience with a face exerts a powerful influence on face processing in tasks where identity information is irrelevant, even in tasks that could in principle be solved via low-level cues. These results underscore the importance of experience in shaping visual recognition processes.     

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.     

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.     

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 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.     

The roles of featural and configural face processing in snap judgments of sexual orientation

Research has shown that people are able to judge sexual orientation from faces with above-chance accuracy, but little is known about how these judgments are formed. Here, we investigated the importance of well-established face processing mechanisms in such judgments: featural processing (e.g., an eye) and configural processing (e.g., spatial distance between eyes). Participants judged sexual orientation from faces presented for 50 milliseconds either upright, which recruits both configural and featural processing, or upside-down, when configural processing is strongly impaired and featural processing remains relatively intact. Although participants judged women's and men's sexual orientation with above-chance accuracy for upright faces and for upside-down faces, accuracy for upside-down faces was significantly reduced. The reduced judgment accuracy for upside-down faces indicates that configural face processing significantly contributes to accurate snap judgments of sexual orientation.     

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.     

MPI CyberMotion Simulator: implementation of a novel motion simulator to investigate multisensory path integration in three dimensions

Path integration is a process in which self-motion is integrated over time to obtain an estimate of one's current position relative to a starting point (1). Humans can do path integration based exclusively on visual (2-3), auditory (4), or inertial cues (5). However, with multiple cues present, inertial cues - particularly kinaesthetic - seem to dominate (6-7). In the absence of vision, humans tend to overestimate short distances (<5 m) and turning angles (<30°), but underestimate longer ones (5). Movement through physical space therefore does not seem to be accurately represented by the brain. Extensive work has been done on evaluating path integration in the horizontal plane, but little is known about vertical movement (see (3) for virtual movement from vision alone). One reason for this is that traditional motion simulators have a small range of motion restricted mainly to the horizontal plane. Here we take advantage of a motion simulator (8-9) with a large range of motion to assess whether path integration is similar between horizontal and vertical planes. The relative contributions of inertial and visual cues for path navigation were also assessed. 16 observers sat upright in a seat mounted to the flange of a modified KUKA anthropomorphic robot arm. Sensory information was manipulated by providing visual (optic flow, limited lifetime star field), vestibular-kinaesthetic (passive self motion with eyes closed), or visual and vestibular-kinaesthetic motion cues. Movement trajectories in the horizontal, sagittal and frontal planes consisted of two segment lengths (1st: 0.4 m, 2nd: 1 m; ±0.24 m/s(2) peak acceleration). The angle of the two segments was either 45° or 90°. Observers pointed back to their origin by moving an arrow that was superimposed on an avatar presented on the screen. Observers were more likely to underestimate angle size for movement in the horizontal plane compared to the vertical planes. In the frontal plane observers were more likely to overestimate angle size while there was no such bias in the sagittal plane. Finally, observers responded slower when answering based on vestibular-kinaesthetic information alone. Human path integration based on vestibular-kinaesthetic information alone thus takes longer than when visual information is present. That pointing is consistent with underestimating and overestimating the angle one has moved through in the horizontal and vertical planes respectively, suggests that the neural representation of self-motion through space is non-symmetrical which may relate to the fact that humans experience movement mostly within the horizontal plane.     

Seeing emotion with your ears: emotional prosody implicitly guides visual attention to faces

Interpersonal communication involves the processing of multimodal emotional cues, particularly facial expressions (visual modality) and emotional speech prosody (auditory modality) which can interact during information processing. Here, we investigated whether the implicit processing of emotional prosody systematically influences gaze behavior to facial expressions of emotion. We analyzed the eye movements of 31 participants as they scanned a visual array of four emotional faces portraying fear, anger, happiness, and neutrality, while listening to an emotionally-inflected pseudo-utterance (Someone migged the pazing) uttered in a congruent or incongruent tone. Participants heard the emotional utterance during the first 1250 milliseconds of a five-second visual array and then performed an immediate recall decision about the face they had just seen. The frequency and duration of first saccades and of total looks in three temporal windows ([0-1250 ms], [1250-2500 ms], [2500-5000 ms]) were analyzed according to the emotional content of faces and voices. Results showed that participants looked longer and more frequently at faces that matched the prosody in all three time windows (emotion congruency effect), although this effect was often emotion-specific (with greatest effects for fear). Effects of prosody on visual attention to faces persisted over time and could be detected long after the auditory information was no longer present. These data imply that emotional prosody is processed automatically during communication and that these cues play a critical role in how humans respond to related visual cues in the environment, such as facial expressions.     

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.     

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.     

Regional Neural Response Differences in the Determination of Faces or Houses Positioned in a Wide Visual Field

In human visual cortex, the primary visual cortex (V1) is considered to be essential for visual information processing; the fusiform face area (FFA) and parahippocampal place area (PPA) are considered as face-selective region and places-selective region, respectively. Recently, a functional magnetic resonance imaging (fMRI) study showed that the neural activity ratios between V1 and FFA were constant as eccentricities increasing in central visual field. However, in wide visual field, the neural activity relationships between V1 and FFA or V1 and PPA are still unclear. In this work, using fMRI and wide-view present system, we tried to address this issue by measuring neural activities in V1, FFA and PPA for the images of faces and houses aligning in 4 eccentricities and 4 meridians. Then, we further calculated ratio relative to V1 (RRV1) as comparing the neural responses amplitudes in FFA or PPA with those in V1. We found V1, FFA, and PPA showed significant different neural activities to faces and houses in 3 dimensions of eccentricity, meridian, and region. Most importantly, the RRV1s in FFA and PPA also exhibited significant differences in 3 dimensions. In the dimension of eccentricity, both FFA and PPA showed smaller RRV1s at central position than those at peripheral positions. In meridian dimension, both FFA and PPA showed larger RRV1s at upper vertical positions than those at lower vertical positions. In the dimension of region, FFA had larger RRV1s than PPA. We proposed that these differential RRV1s indicated FFA and PPA might have different processing strategies for encoding the wide field visual information from V1. These different processing strategies might depend on the retinal position at which faces or houses are typically observed in daily life. We posited a role of experience in shaping the information processing strategies in the ventral visual cortex.     

Do I Have My Attention? Speed of Processing Advantages for the Self-Face Are Not Driven by Automatic Attention Capture

We respond more quickly to our own face than to other faces, but there is debate over whether this is connected to attention-grabbing properties of the self-face. In two experiments, we investigate whether the self-face selectively captures attention, and the attentional conditions under which this might occur. In both experiments, we examined whether different types of face (self, friend, stranger) provide differential levels of distraction when processing self, friend and stranger names. In Experiment 1, an image of a distractor face appeared centrally – inside the focus of attention – behind a target name, with the faces either upright or inverted. In Experiment 2, distractor faces appeared peripherally – outside the focus of attention – in the left or right visual field, or bilaterally. In both experiments, self-name recognition was faster than other name recognition, suggesting a self-referential processing advantage. The presence of the self-face did not cause more distraction in the naming task compared to other types of face, either when presented inside (Experiment 1) or outside (Experiment 2) the focus of attention. Distractor faces had different effects across the two experiments: when presented inside the focus of attention (Experiment 1), self and friend images facilitated self and friend naming, respectively. This was not true for stranger stimuli, suggesting that faces must be robustly represented to facilitate name recognition. When presented outside the focus of attention (Experiment 2), no facilitation occurred. Instead, we report an interesting distraction effect caused by friend faces when processing strangers’ names. We interpret this as a “social importance” effect, whereby we may be tuned to pick out and pay attention to familiar friend faces in a crowd. We conclude that any speed of processing advantages observed in the self-face processing literature are not driven by automatic attention capture.     

Access to Awareness for Faces during Continuous Flash Suppression Is Not Modulated by Affective Knowledge

It is a controversially debated topic whether stimuli can be analyzed up to the semantic level when they are suppressed from visual awareness during continuous flash suppression (CFS). Here, we investigated whether affective knowledge, i.e., affective biographical information about faces, influences the time it takes for initially invisible faces with neutral expressions to overcome suppression and break into consciousness. To test this, we used negative, positive, and neutral famous faces as well as initially unfamiliar faces, which were associated with negative, positive or neutral biographical information. Affective knowledge influenced ratings of facial expressions, corroborating recent evidence and indicating the success of our affective learning paradigm. Furthermore, we replicated shorter suppression durations for upright than for inverted faces, demonstrating the suitability of our CFS paradigm. However, affective biographical information did not modulate suppression durations for newly learned faces, and even though suppression durations for famous faces were influenced by affective knowledge, these effects did not differ between upright and inverted faces, indicating that they might have been due to low-level visual differences. Thus, we did not obtain unequivocal evidence for genuine influences of affective biographical information on access to visual awareness for faces during CFS.     

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.     

Cortical networks for face perception in two-month-old infants

Newborns have an innate system for preferentially looking at an upright human face. This face preference behaviour disappears at approximately one month of age and reappears a few months later. However, the neural mechanisms underlying this U-shaped behavioural change remain unclear. Here, we isolate the functional development of the cortical visual pathway for face processing using S-cone-isolating stimulation, which blinds the subcortical visual pathway. Using luminance stimuli, which are conveyed by both the subcortical and cortical visual pathways, the preference for upright faces was not observed in two-month-old infants, but it was observed in four- and six-month-old infants, confirming the recovery phase of the U-shaped development. By contrast, using S-cone stimuli, two-month-old infants already showed a preference for upright faces, as did four- and six-month-old infants, demonstrating that the cortical visual pathway for face processing is already functioning at the bottom of the U-shape at two months of age. The present results suggest that the transient functional deterioration stems from a conflict between the subcortical and cortical functional pathways, and that the recovery thereafter involves establishing a level of coordination between the two pathways.