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.

An investigation on the face inversion effect in deaf children.

The face inversion effect is an important indicator of holistic face perception and reflects the developmental level of face processing. This study examined the face inversion effect in deaf or hard of hearing (DHH) children aged 7-17 using the face dimensions task. This task uses photographic images of a face, in which configural and featural information in the eye and mouth regions have been parametrically and independently manipulated. The study aimed to discuss the effect of face inversion on facial processing in DHH children, including two aspects of information processing types (configural versus featural) and processing regions (eyes versus mouth) and compared the results with hearing children. The results revealed that DHH children aged 7-17 years exhibit significant face inversion effect, with disruptions observed in both the featural and configural processing of eyes and mouths when faces were inverted. Configural processing was more affected by inversion than featural processing in all children, with larger differences observed in DHH children than in hearing children. This supports the dual-mode hypothesis of holistic face processing. Age correlations were observed in the sensitivity of DHH children to face inversion effect but not among hearing children. The inversion effect of configural mouth processing decreases with age in DHH children.

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.

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.

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.

Bayesian estimation of ERP components from multicondition and multichannel EEG.

Extraction and separation of functionally different event-related potentials (ERPs) from electroencephalography (EEG) is a long-standing problem in cognitive neuroscience. In this paper, we propose a Bayesian spatio-temporal model for estimating ERP components from multichannel EEG recorded under multiple experimental conditions. The model isolates the spatially and temporally overlapping ERP components by utilizing their phase-locking structure and the inter-condition non-stationarity structure of their amplitudes and latencies. Critically, unlike in previous multilinear algorithms, the non-phase-locked background EEGs are modeled as spatially correlated and non-isotropic signals. A variational algorithm was developed for approximate Bayesian inference of the proposed model, with the effective number of ERP components automatically determined as a part of the algorithm. The utility of the algorithm is demonstrated with applications to synthetic data and the EEG data collected from 13 subjects during a face inversion experiment. The results show that our algorithm more accurately and reliably estimates the spatio-temporal patterns, amplitudes, and latencies of the underlying ERP components in comparison with several state-of-the-art algorithms.

The face inversion effect in infants is driven by high, and not low, spatial frequencies.

To investigate the mechanisms underlying development of upright face preferences in infants, the current study measured inversion effects for faces that were spatial frequency (SF) filtered, into low SF and high SF, with the notion that different SFs are analyzed by different visual mechanisms. For comparison to faces, we used object stimuli that consisted of pictures of strollers. In 4 month olds, 8 month olds, and adults, we measured the strength of the selective face inversion effect (sFIE), operationally defined as an upright over inverted looking preference that is greater for faces than objects. In Study 1, we employed unfiltered stimuli, and found a clear sFIE in both infants and adults. To determine what drove this sFIE, in Study 2, the sFIE was measured for low-SF and high-SF stimuli, with all stimuli being equated for visibility. For adults, the sFIE was equally strong for low-SF and high-SF stimuli. A different pattern was seen for infants. Infants exhibited a significantly greater sFIE for high-SF, than for low-SF, stimuli (and only for high SF was the sFIE significant). In fact, the strength of infants' upright face preference for high-SF stimuli was indistinguishable from that observed for unfiltered faces, indicating that in natural (unfiltered) stimuli, high SFs are sufficient to account for infants' upright face preferences.

Face inversion does not affect the reversed congruency effect of gaze.

In a spatial Stroop task, the eye-gaze target produces the reversed congruency effect-responses become shorter when the gaze direction and its location are incongruent than when they are congruent. The present study examined the face inversion effect on the gaze spatial Stroop task to clarify whether the holistic face processing or part-based processing of the eyes is responsible for the reversed congruency effect. In Experiment 1, participants judged the gaze direction of the upright or inverted face with a neutral expression presented either in the left or right visual field. In Experiment 2, we examined whether face inversion interacted with facial expressions (i.e., angry, happy, neutral, and sad). Face inversion disrupted holistic face processing, slowing down the overall performance relative to the performance with upright faces. However, face inversion did not affect the reversed congruency effect. These results further support the parts-based processing account and suggest that while faces are processed holistically, the reversed congruency effect, relying on the extracted local features (i.e., eyes), may be processed in a part-based manner.

The face inversion effect or the face upright effect?

The face inversion effect (FIE) refers to the observation that presenting stimuli upside-down impairs the processing of faces disproportionally more than other mono-oriented objects. This has been taken as evidence that processing of faces and objects differ qualitatively. However, nearly all FIE studies are based on comparing individuation of upright faces, which most people are rather good at, with individuation of objects most people are much less familiar with individuating (e.g., radios and airplanes). Consequently, the FIE may mainly reflect differences between categories in how they are processed prior to inversion, with within-category discrimination of upright faces being a much more familiar task than within-category discrimination among members belonging to other object classes. We tested this hypothesis by comparing inversion effects for faces and objects using object recognition tasks that do not require within-category discrimination (object decision and old/new recognition memory tasks). In all tasks (seven with objects and two with faces) we find credible inversion effects, but in no instance were these effects significantly larger for faces than for objects. This suggests that the FIE can be a product of familiarity with the type of identification process required in the upright conditions rather than some process that is selectively affected for faces when stimuli are inverted.

Qualitative differences in the spatiotemporal brain states supporting configural face processing emerge in adolescence in autism.

BACKGROUND: Studying the neural processing of faces can illuminate the mechanisms of compromised social expertise in autism. To resolve a longstanding debate, we examined whether differences in configural face processing in autism are underpinned by quantitative differences in the activation of typical face processing pathways, or the recruitment of non-typical neural systems. METHODS: We investigated spatial and temporal characteristics of event-related EEG responses to upright and inverted faces in a large sample of children, adolescents, and adults with and without autism. We examined topographic analyses of variance and global field power to identify group differences in the spatial and temporal response to face inversion. We then examined how quasi-stable spatiotemporal profiles - microstates - are modulated by face orientation and diagnostic group. RESULTS: Upright and inverted faces produced distinct profiles of topography and strength in the topographical analyses. These topographical profiles differed between diagnostic groups in adolescents, but not in children or adults. In the microstate analysis, the autistic group showed differences in the activation strength of normative microstates during early-stage processing at all ages, suggesting consistent quantitative differences in the operation of typical processing pathways; qualitative differences in microstate topographies during late-stage processing became prominent in adults, suggesting the increasing involvement of non-typical neural systems with processing time and over development. CONCLUSIONS: These findings suggest that early difficulties with configural face processing may trigger later compensatory processes in autism that emerge in later development.

Do facially disfiguring features influence attention and perception of faces? Evidence from an antisaccade task.

Facial disfigurements can influence how observers attend to and interact with the person, leading to disease-avoidance behaviour and emotions (disgust, threat, fear for contagion). However, it is unclear whether this behaviour is reflected in the effect of the facial stigma on attention and perceptual encoding of facial information. We addressed this question by measuring, in a mixed antisaccade task, observers' speed and accuracy of orienting of visual attention towards or away from peripherally presented upright and inverted unfamiliar faces that had either a realistic looking disease-signalling feature (a skin discolouration), a non-disease-signalling control feature, or no added feature. The presence of a disfiguring or control feature did not influence the orienting of attention (in terms of saccadic latency) towards upright faces, suggesting that avoidance responses towards facial stigma do not occur during covert attention. However, disfiguring and control features significantly reduced the effect of face inversion on saccadic latency, thus suggesting an impact on the holistic processing of facial information. The implications of these findings for the encoding and appraisal of facial disfigurements are discussed.