Parafoveal vision reveals qualitative differences between fusiform face area and parahippocampal place area.

The center-periphery visual field axis guides early visual system organization with enhanced resources devoted to central vision leading to reduced peripheral performance relative to that of central vision (i.e., behavioral eccentricity effect) for many visual functions. The center-periphery organization extends to high-order visual cortex where, for example, the well-studied face-sensitive fusiform face area (FFA) shows sensitivity to central vision and the place-sensitive parahippocampal place area (PPA) shows sensitivity to peripheral vision. As we have recently found that face perception is more sensitive to eccentricity than place perception, here we examined whether these behavioral findings reflect differences in FFA's and PPA's sensitivities to eccentricity. We assumed FFA would show higher sensitivity to eccentricity than PPA would, but that both regions' modulation by eccentricity would be invariant to the viewed category. We parametrically investigated (fMRI, n = 32) how FFA's and PPA's activations are modulated by eccentricity (≤8°) and category (upright/inverted faces/houses) while keeping stimulus size constant. As expected, FFA showed an overall higher sensitivity to eccentricity than PPA. However, both regions' activation modulations by eccentricity were dependent on the viewed category. In FFA, a reduction of activation with growing eccentricity ("BOLD eccentricity effect") was found (with different amplitudes) for all categories. In PPA however, qualitatively different BOLD eccentricity effect modulations were found (e.g., at 8° mild BOLD eccentricity effect for houses but a reverse BOLD eccentricity effect for faces and no modulation for inverted faces). Our results emphasize that peripheral vision investigations are critical to further our understanding of visual processing.

Tracking the temporal dynamics of the face-like inversion effect as revealed by Chinese characters using magnetoencephalography.

The neural basis of configural processing has been extensively studied by exploiting face inversion during recognition, and growing evidence has revealed that word inversion also involves changes in configuration. However, the neural dynamics of face-like inversion effects remain unclear. Here, we tracked the temporal dynamics of neural responses that were sensitive to inversion during Chinese character recognition as they occurred during face recognition using multivariate decoding and temporal generalization analyses. We recorded magnetoencephalography while participants performed a one-back task for faces, compound characters, and simple characters with upright and inverted orientations. We showed that the inversion effect (inverted versus upright) can be decoded at occipitotemporal sensors for all stimulus types over and across time points, with a stronger impact on faces and compound characters than on simple characters. The inversion effect occurred earlier and lasted longer for faces than for characters, and the effect was also stronger for compound characters than for simple characters. Finally, we demonstrated inversion effects in the event-related field for all stimulus types and identified their sources in the ventral occipitotemporal areas. Overall, this study provides novel evidence for the temporal dynamics of the face-like inversion effect occurring during Chinese character recognition.

Using transcranial direct current stimulation (tDCS) to selectively modulate the face inversion effect and N170 event-related potentials.

We report a large study (n = 72) using combined transcranial direct current stimulation-electroencephalography (tDCS-EEG) to investigate the modulation of perceptual learning indexed by the face inversion effect. Participants were engaged with an old/new recognition task involving intermixed upright and inverted, normal and Thatcherized faces. The accuracy results showed anodal tDCS delivered at the Fp3 scalp area (cathode/reference electrode placed at Fp2) increased the behavioural inversion effect for normal faces versus sham/control and this covaried with a modulation of the N170 event-related potential component. A reduced inversion effect for normal faces was found on the N170 latency and amplitude versus sham/control, extending recent work that combined tDCS and EEG in circumstances where the behavioural face inversion effect was reduced. Our results advance understanding of the neural mechanisms responsible for perceptual learning by revealing a dissociation between the N170 amplitude and latency in response to the tDCS-induced modulation of the face inversion effect. The behavioural modulation of the inversion effect tracks the modulation of the N170 amplitudes, albeit it is negatively correlated (i.e., reduced inversion effect-larger N170 amplitude inversion effect, increased inversion effect-reduced N170 amplitude inversion effect). For the N170 latencies, the inversion effect is reduced by the tDCS protocol we use irrespective of any modulation of the behavioural inversion effect.

The face inversion effect does not provide a pure measure of holistic face processing.

It is widely held that upright faces are processed more holistically than inverted faces and that this difference is reflected in the face inversion effect. It is not clear, however, how the inversion effect can best be measured, whether it is task specific, or even whether it specifically correlates with processing of upright faces. We examined these questions in a large sample (N = 420) who provided data on processing of upright and inverted stimuli in two different tasks with faces and one with objects. We find that the inversion effects are task dependent, and that they do not correlate better among face processing tasks than they do across face and object processing tasks. These findings were obtained regardless of whether inversion effects were measured by means of difference scores or regression. In comparison, only inversion effects based on regression predicted performance with upright faces in tasks other than those the inversion effects were derived from. Critically, however, inversion effects based on regression also predicted performance with inverted faces to a similar degree as they predicted performance with upright faces. Consequently, and contrary to what is commonly assumed, inversion effects do not seem to capture effects specific to holistic processing of upright faces. While the present findings do not bring us closer to an understanding of which changes in cognitive processing are induced by inversion, they do suggest that inversion effects do not reflect a unitary construct; an implicit assumption that seems to characterize much of the research regarding face processing.

Face inversion effect on perceived cuteness of infant faces.

Research has demonstrated that attractiveness evaluations of adult faces were less accurate when faces were inverted than upright. It remains unknown, however, whether a similar effect applies to perceived cuteness of infants, which is assumed to be based on elemental facial features called the "baby schema." In this research, we studied the face inversion effect on perceived cuteness of infant faces in a rating task and a two-alternative forced-choice (2AFC) task. We also examined beauty as a control dimension. Although the rating task revealed no inversion effect, the 2AFC task showed poorer discrimination performance with inverted faces than with upright faces in both evaluations. These results indicate that infant cuteness and beauty dimensions are correlated well with each other, and their perception not only relies on elemental features that are not strongly affected by inversion but is also affected by holistic facial configurations when a detailed comparison is required.

The effect of face orientation on audiovisual speech integration in infancy: An electrophysiological study.

Humans pay special attention to faces and speech from birth, but the interplay of developmental processes leading to specialization is poorly understood. We investigated the effects of face orientation on audiovisual (AV) speech perception in two age groups of infants (younger: 5- to 6.5-month-olds; older: 9- to 10.5-month-olds) and adults. We recorded event-related potentials (ERP) in response to videos of upright and inverted faces producing /ba/ articulation dubbed with auditory syllables that were either matching /ba/ or mismatching /ga/ the mouth movement. We observed an increase in the amplitude of audiovisual mismatch response (AVMMR) to incongruent visual /ba/-auditory /ga/ syllable in comparison to other stimuli in younger infants, while the older group of infants did not show a similar response. AV mismatch response to inverted visual /ba/-auditory /ga/ stimulus relative to congruent stimuli was also detected in the right frontal areas in the younger group and the left and right frontal areas in adults. We show that face configuration affects the neural response to AV mismatch differently across all age groups. The novel finding of the AVMMR in response to inverted incongruent AV speech may potentially imply the featural face processing in younger infants and adults when processing inverted faces articulating incongruent speech. The lack of visible differential responses to upright and inverted incongruent stimuli obtained in the older group of infants suggests a likely functional cortical reorganization in the processing of AV speech.

Comparison of neuronal responses in primate inferior-temporal cortex and feed-forward deep neural network model with regard to information processing of faces.

Feed-forward deep neural networks have better performance in object categorization tasks than other models of computer vision. To understand the relationship between feed-forward deep networks and the primate brain, we investigated representations of upright and inverted faces in a convolutional deep neural network model and compared them with representations by neurons in the monkey anterior inferior-temporal cortex, area TE. We applied principal component analysis to feature vectors in each model layer to visualize the relationship between the vectors of the upright and inverted faces. The vectors of the upright and inverted monkey faces were more separated through the convolution layers. In the fully-connected layers, the separation among human individuals for upright faces was larger than for inverted faces. The Spearman correlation between each model layer and TE neurons reached a maximum at the fully-connected layers. These results indicate that the processing of faces in the fully-connected layers might resemble the asymmetric representation of upright and inverted faces by the TE neurons. The separation of upright and inverted faces might take place by feed-forward processing in the visual cortex, and separations among human individuals for upright faces, which were larger than those for inverted faces, might occur in area TE.

Reduced left visual field bias for faces in adolescents with social anxiety disorder.

Introduction: Individuals tend to explore the left side of a face first and for a longer time in comparison to the right side. This left visual field (LVF) bias is suggested to reflect right hemispheric dominance for face processing. Social anxiety disorder (SAD) is associated with maladaptive interpretations of facial expressions, but it is not known whether this is linked to an atypical LVF bias. Previous studies have reported a reduced LVF bias in autism, a condition overlapping with SAD. This pre-registered study examined the LVF bias in adolescents with SAD. Methods: Eye-tracking was used to investigate the ratio of first fixations to the left on upright and inverted face stimuli in 26 adolescents (13-17 years) with SAD and 23 healthy controls primed to look either between the eyes or at the mouth. Results: The SAD group showed a smaller LVF bias and an atypical face inversion effect when primed to look at the eyes. Autistic traits predicted a smaller LVF bias, independently of social anxiety level. Conclusions: Results suggest that SAD is associated with impaired processing of faces at an early stage of visual scanning. The findings contribute to a better understanding of SAD and its overlap with autism.

Does a cichlid fish process face holistically? Evidence of the face inversion effect.

Faces are the most important body part for differentiating among human individuals by humans. Humans read the face as a whole, rather than looking at its parts, which makes it more difficult to recognise inverted faces than upright. Some other mammals also identify each other based on the upright face and take longer to recognise inverted faces. This effect is called the face inversion effect and is considered as evidence for face-specific perception. This ability has rarely been observed in animals other than mammals, but it was recently reported that some fish species could distinguish among individuals based on the face. For example, the cichlid fish Neolamprologus pulcher rapidly recognises familiar conspecifics by faces rather than other body parts. Here, we examined the face inversion effect in N. pulcher, by showing photographs of conspecific fish faces and objects in both upright and inverted orientations. Subjects gazed at novel faces longer than familiar faces in upright presentation, whereas they did not show such a tendency for inverted faces. Although the object discrimination was difficult, we did not observe the difference between upright and inverted object photographs. Our results indicate that fish exhibits the inversion effect for faces. These findings suggest that N. pulcher may process their conspecifics' face holistically, like humans.

The Effects of Blur and Inversion on the Recognition of Ambient Face Images.

When viewing unfamiliar faces that vary in expressions, angles, and image quality, observers make many recognition errors. Specifically, in unconstrained identity-sorting tasks, observers struggle to cope with variation across different images of the same person while succeeding at telling different people apart. The use of ambient face images in this simple card-sorting task reveals the magnitude of these face recognition errors and suggests a useful platform to reexamine the nature of face processing using naturalistic stimuli. In the present study, we chose to investigate the impact of two basic stimulus manipulations (image blur and face inversion) on identity sorting with ambient images. Although these manipulations are both known to affect face processing when well-controlled, frontally viewed face images are used, examining how they affect performance for ambient images is an important step toward linking the large body of research using controlled face images to more ecologically valid viewing conditions. Briefly, we observed a high cost of image blur regardless of blur magnitude, and a strong inversion effect that affected observers' sensitivity to extrapersonal variability but did not affect the number of unique identities they estimated were present in the set of images presented to them.

Altered upright face recognition and presence of face inversion effect in temporal lobe epilepsy: An event-related potential study.

AIM: Facial recognition can be assessed by examining an event-related potential component, namely the N170. The amplitude of the N170 is larger in response to inverted faces than to upright faces. To examine facial processing in patients with temporal lobe epilepsy (TLE), we investigated the amplitude of the N170, the face inversion effect, and the association between social functioning and face-specific configuration processing. METHODS: Sixteen patients with TLE and 17 normal controls (NC) participated in this study. Event-related potentials in response to upright or inverted neutral faces and bicycles were recorded. Social functioning was assessed by the socioeconomic status of the participants using the 5-point Hollingshead-Redlich Scale. RESULTS: Compared with NC, patients with TLE had decreased N170 amplitudes. The inversion effect was observed for face stimuli in both groups; however, no inversion effect was observed for bicycle stimuli. Additionally, in TLE patients, but not in NC, socioeconomic status was significantly correlated with the N170 amplitudes in response to upright faces. CONCLUSION: In a social context, upright faces are processed as a whole. This process is impaired in TLE. Conversely, inverted faces are processed analytically. This function is normal in TLE. Abnormal face-specific configuration processing may contribute to lower social functioning in TLE.

The Bandwidth of Diagnostic Horizontal Structure for Face Identification.

Horizontally oriented spatial frequency components are a diagnostic source of face identity information, and sensitivity to this information predicts upright identification accuracy and the magnitude of the face-inversion effect. However, the bandwidth at which this information is conveyed, and the extent to which human tuning matches this distribution of information, has yet to be characterized. We designed a 10-alternative forced choice face identification task in which upright or inverted faces were filtered to retain horizontal or vertical structure. We systematically varied the bandwidth of these filters in 10° steps and replaced the orientation components that were removed from the target face with components from the average of all possible faces. This manipulation created patterns that looked like faces but contained diagnostic information in orientation bands unknown to the observer on any given trial. Further, we quantified human performance relative to the actual information content of our face stimuli using an ideal observer with perfect knowledge of the diagnostic band. We found that the most diagnostic information for face identification is conveyed by a narrow band of orientations along the horizontal meridian, whereas human observers use information from a wide range of orientations.

It's Not All About the Face: Variability Reveals Asymmetric Obligatory Processing of Faces and Bodies in Whole-Body Contexts.

Researchers have sought to understand the specialized processing of faces and bodies in isolation, but recently they have considered how face and body information interact within the context of the whole body. Although studies suggest that face and body information can be integrated, it remains an open question whether this integration is obligatory and whether contributions of face and body information are symmetrical. In a selective attention task with whole-body stimuli, we focused attention on either the face or body and tested whether variation in the irrelevant part could be ignored. We manipulated orientation to determine the extent to which inversion disrupted obligatory face and body processing. Obligatory processing was evidenced as performance changes in discrimination that depended on stimulus orientation when the irrelevant region varied. For upright but not inverted face discrimination, participants could not ignore body posture variation, even when it was not diagnostic to the task. However, participants could ignore face variation for upright body posture discrimination but not for inverted posture discrimination. The extent to which face and body information necessarily influence each other in whole-body contexts appears to depend on both domain-general attentional and face- or body-specific holistic processing mechanisms.

Inversion Impairs Expert Budgerigar Identity Recognition: A Face-Like Effect for a Nonface Object of Expertise.

The face-inversion effect is the finding that picture-plane inversion disproportionately impairs face recognition compared to object recognition and is now attributed to greater orientation-sensitivity of holistic processing for faces but not common objects. Yet, expert dog judges have showed similar recognition deficits for inverted dogs and inverted faces, suggesting that holistic processing is not specific to faces but to the expert recognition of perceptually similar objects. Although processing changes in expert object recognition have since been extensively documented, no other studies have observed the distinct recognition deficits for inverted objects-of-expertise that people as face experts show for faces. However, few studies have examined experts who recognize individual objects similar to how people recognize individual faces. Here we tested experts who recognize individual budgerigar birds. The effect of inversion on viewpoint-invariant budgerigar and face recognition was compared for experts and novices. Consistent with the face-inversion effect, novices showed recognition deficits for inverted faces but not for inverted budgerigars. By contrast, experts showed equal recognition deficits for inverted faces and budgerigars. The results are consistent with the hypothesis that processes underlying the face-inversion effect are specific to the expert individuation of perceptually similar objects.

Being BOLD: The neural dynamics of face perception.

According to a non-hierarchical view of human cortical face processing, selective responses to faces may emerge in a higher-order area of the hierarchy, in the lateral part of the middle fusiform gyrus (fusiform face area [FFA]) independently from face-selective responses in the lateral inferior occipital gyrus (occipital face area [OFA]), a lower order area. Here we provide a stringent test of this hypothesis by gradually revealing segmented face stimuli throughout strict linear descrambling of phase information [Ales et al., 2012]. Using a short sampling rate (500 ms) of fMRI acquisition and single subject statistical analysis, we show a face-selective responses emerging earlier, that is, at a lower level of structural (i.e., phase) information, in the FFA compared with the OFA. In both regions, a face detection response emerging at a lower level of structural information for upright than inverted faces, both in the FFA and OFA, in line with behavioral responses and with previous findings of delayed responses to inverted faces with direct recordings of neural activity were also reported. Overall, these results support the non-hierarchical view of human cortical face processing and open new perspectives for time-resolved analysis at the single subject level of fMRI data obtained during continuously evolving visual stimulation. Hum Brain Mapp 38:120-139, 2017. © 2016 Wiley Periodicals, Inc.

Comparing the face inversion effect in crows and humans.

Humans show impaired recognition of faces that are presented upside down, a phenomenon termed face inversion effect, which is thought to reflect the special relevance of faces for humans. Here, we investigated whether a phylogenetically distantly related avian species, the carrion crow, with similar socio-cognitive abilities to human and non-human primates, exhibits a face inversion effect. In a delayed matching-to-sample task, two crows had to differentiate profiles of crow faces as well as matched controls, presented both upright and inverted. Because crows can discriminate humans based on their faces, we also assessed the face inversion effect using human faces. Both crows performed better with crow faces than with human faces and performed worse when responding to inverted pictures in general compared to upright pictures. However, neither of the crows showed a face inversion effect. For comparative reasons, the tests were repeated with human subjects. As expected, humans showed a face-specific inversion effect. Therefore, we did not find any evidence that crows-like humans-process faces as a special visual stimulus. Instead, individual recognition in crows may be based on cues other than a conspecific's facial profile, such as their body, or on processing of local features rather than holistic processing.

Further evidence of early development of attention to dynamic facial emotions: Reply to Grossmann and Jessen.

Adults exhibit enhanced attention to negative emotions like fear, which is thought to be an adaptive reaction to emotional information. Previous research, mostly conducted with static faces, suggests that infants exhibit an attentional bias toward fearful faces only at around 7months of age. In a recent study (Journal of Experimental Child Psychology, 2016, Vol. 147, pp. 100-110), we found that 5-month-olds also exhibit heightened attention to fear when tested with dynamic face videos. This indication of an earlier development of an attention bias to fear raises questions about developmental mechanisms that have been proposed to underlie this function. However, Grossmann and Jessen (Journal of Experimental Child Psychology, 2016, Vol. 153, pp. 149-154) argued that this result may have been due to differences in the amount of movement in the videos rather than a response to emotional information. To examine this possibility, we tested a new sample of 5-month-olds exactly as in the original study (Heck, Hock, White, Jubran, & Bhatt, 2016) but with inverted faces. We found that the fear bias seen in our study was no longer apparent with inverted faces. Therefore, it is likely that infants' enhanced attention to fear in our study was indeed a response to emotions rather than a reaction to arbitrary low-level stimulus features. This finding indicates enhanced attention to fear at 5months and underscores the need to find mechanisms that engender the development of emotion knowledge early in life.

Dissociable cortical pathways for qualitative and quantitative mechanisms in the face inversion effect.

Humans' ability to recognize objects is remarkably robust across a variety of views unless faces are presented upside-down. Whether this face inversion effect (FIE) results from qualitative (distinct mechanisms) or quantitative processing differences (a matter of degree within common mechanisms) between upright and inverted faces has been intensely debated. Studies have focused on preferential responses to faces in face-specific brain areas, although face recognition also involves nonpreferential responses in non-face-specific brain areas. By using dynamic causal modeling with Bayesian model selection, here we show that dissociable cortical pathways are responsible for qualitative and quantitative mechanisms in the FIE in the distributed network for face recognition. When faces were upright, the early visual cortex (VC) and occipital and fusiform face areas (OFA, FFA) suppressed couplings to the lateral occipital cortex (LO), a primary locus of object processing. In contrast, they did not inhibit the LO when faces were inverted but increased couplings to the intraparietal sulcus, which has been associated with visual working memory. Furthermore, we found that upright and inverted face processing together involved the face network consisting of the VC, OFA, FFA, and inferior frontal gyrus. Specifically, modulatory connectivity within the common pathways (VC-OFA), implicated in the parts-based processing of faces, strongly correlated with behavioral FIE performance. The orientation-dependent dynamic reorganization of effective connectivity indicates that the FIE is mediated by both qualitative and quantitative differences in upright and inverted face processing, helping to resolve a central debate over the mechanisms of the FIE.

Gaze constancy in upright and inverted faces.

The dual-route model (Otsuka, Mareschal, Calder, & Clifford, 2014) posits that constancy in the perception of gaze direction across lateral head rotation depends on the integration of information from the eye region and information about head rotation. Incorporation of information about head rotation serves to compensate for the change in eye-region information when viewing a rotated head. We tested the ability of this model to predict the magnitude of Wollaston's effect: When eyes from a frontal pose are inserted into an angled face, the perceived direction of gaze appears attracted towards the direction of the head. The framework of the dual-route model explains Wollaston's effect as a result of the misapplication of this same integration operation without any change in eye-region information. To test this explanation, we compared the magnitude of the integration occurring for Wollaston's effect to that for normal faces. Here, participants performed categorical judgment of gaze direction across head rotation poses in three image conditions: normal face, eyes-only, and Wollaston. Integration of eye and head information was inferred by comparing the effect of pose between the eyes-only condition and the normal face condition, and by examining the effect of pose in the Wollaston condition. Consistent with the dual-route model, the magnitude of integration was similar between the normal face condition and the Wollaston condition. Further, upright and inverted faces yielded similar levels of gaze constancy, showing that the dual-route model applies to the perception of gaze direction in inverted faces as well as in upright faces.

Separable effects of inversion and contrast-reversal on face detection thresholds and response functions: a sweep VEP study.

The human brain rapidly detects faces in the visual environment. We recently presented a sweep visual evoked potential approach to objectively define face detection thresholds as well as suprathreshold response functions (Ales, Farzin, Rossion, & Norcia, 2012). Here we determined these parameters are affected by orientation (upright vs. inverted) and contrast polarity (positive vs. negative), two manipulations that disproportionately disrupt the perception of faces relative to other object categories. Face stimuli parametrically increased in visibility through phase-descrambling while alternating with scrambled images at a fixed presentation rate of 3 Hz (6 images/s). The power spectrum and mean luminance of all stimuli were equalized. As a face gradually emerged during a stimulation sequence, EEG responses at 3 Hz appeared at ≈35% phase coherence over right occipito-temporal channels, replicating previous observations. With inversion and contrast-reversal, the 3-Hz amplitude decreased by ≈20%-50% and the face detection threshold increased by ≈30%-60% coherence. Furthermore, while the 3-Hz response emerged abruptly and saturated quickly for normal faces, suggesting a categorical neural response, the response profile for inverted and negative polarity faces was shallower and more linear, indicating gradual and continuously increasing activation of the underlying neural population. These findings demonstrate that inversion and contrast-reversal increase the threshold and modulate the suprathreshold response function of face detection.