Spontaneous gender categorization in masking and priming studies: key for distinguishing Jane from John Doe but not Madonna from Sinatra

Facial recognition is key to social interaction, however with unfamiliar faces only generic information, in the form of facial stereotypes such as gender and age is available. Therefore is generic information more prominent in unfamiliar versus familiar face processing? In order to address the question we tapped into two relatively disparate stages of face processing. At the early stages of encoding, we employed perceptual masking to reveal that only perception of unfamiliar face targets is affected by the gender of the facial masks. At the semantic end; using a priming paradigm, we found that while to-be-ignored unfamiliar faces prime lexical decisions to gender congruent stereotypic words, familiar faces do not. Our findings indicate that gender is a more salient dimension in unfamiliar relative to familiar face processing, both in early perceptual stages as well as later semantic stages of person construal.     

Familiar Face Detection in 180ms

The visual system is tuned for rapid detection of faces, with the fastest choice saccade to a face at 100ms. Familiar faces have a more robust representation than do unfamiliar faces, and are detected faster in the absence of awareness and with reduced attentional resources. Faces of family and close friends become familiar over a protracted period involving learning the unique visual appearance, including a view-invariant representation, as well as person knowledge. We investigated the effect of personal familiarity on the earliest stages of face processing by using a saccadic-choice task to measure how fast familiar face detection can happen. Subjects made correct and reliable saccades to familiar faces when unfamiliar faces were distractors at 180ms—very rapid saccades that are 30 to 70ms earlier than the earliest evoked potential modulated by familiarity. By contrast, accuracy of saccades to unfamiliar faces with familiar faces as distractors did not exceed chance. Saccades to faces with object distractors were even faster (110 to 120 ms) and equivalent for familiar and unfamiliar faces, indicating that familiarity does not affect ultra-rapid saccades. We propose that detectors of diagnostic facial features for familiar faces develop in visual cortices through learning and allow rapid detection that precedes explicit recognition of identity.     

Effect of Familiarity on Reward Anticipation in Children with and without Autism Spectrum Disorders

Background

Previous research on the reward system in autism spectrum disorders (ASD) suggests that children with ASD anticipate and process social rewards differently than typically developing (TD) children—but has focused on the reward value of unfamiliar face stimuli. Children with ASD process faces differently than their TD peers. Previous research has focused on face processing of unfamiliar faces, but less is known about how children with ASD process familiar faces. The current study investigated how children with ASD anticipate rewards accompanied by familiar versus unfamiliar faces.

Methods

The stimulus preceding negativity (SPN) of the event-related potential (ERP) was utilized to measure reward anticipation. Participants were 6- to 10-year-olds with (N = 14) and without (N = 14) ASD. Children were presented with rewards accompanied by incidental face or non-face stimuli that were either familiar (caregivers) or unfamiliar. All non-face stimuli were composed of scrambled face elements in the shape of arrows, controlling for visual properties.

Results

No significant differences between familiar versus unfamiliar faces were found for either group. When collapsing across familiarity, TD children showed larger reward anticipation to face versus non-face stimuli, whereas children with ASD did not show differential responses to these stimulus types. Magnitude of reward anticipation to faces was significantly correlated with behavioral measures of social impairment in the ASD group.

Conclusions

The findings do not provide evidence for differential reward anticipation for familiar versus unfamiliar face stimuli in children with or without ASD. These findings replicate previous work suggesting that TD children anticipate rewards accompanied by social stimuli more than rewards accompanied by non-social stimuli. The results do not support the idea that familiarity normalizes reward anticipation in children with ASD. Our findings also suggest that magnitude of reward anticipation to faces is correlated with levels of social impairment for children with ASD.     

Human face processing is tuned to sexual age preferences

Human faces can motivate nurturing behaviour or sexual behaviour when adults see a child or an adult face, respectively. This suggests that face processing is tuned to detecting age cues of sexual maturity to stimulate the appropriate reproductive behaviour: either caretaking or mating. In paedophilia, sexual attraction is directed to sexually immature children. Therefore, we hypothesized that brain networks that normally are tuned to mature faces of the preferred gender show an abnormal tuning to sexual immature faces in paedophilia. Here, we use functional magnetic resonance imaging (fMRI) to test directly for the existence of a network which is tuned to face cues of sexual maturity. During fMRI, participants sexually attracted to either adults or children were exposed to various face images. In individuals attracted to adults, adult faces activated several brain regions significantly more than child faces. These brain regions comprised areas known to be implicated in face processing, and sexual processing, including occipital areas, the ventrolateral prefrontal cortex and, subcortically, the putamen and nucleus caudatus. The same regions were activated in paedophiles, but with a reversed preferential response pattern.     

Directed cortical information flow during human object recognition: analyzing induced EEG gamma-band responses in brain's source space

The increase of induced gamma-band responses (iGBRs; oscillations >30 Hz) elicited by familiar (meaningful) objects is well established in electroencephalogram (EEG) research. This frequency-specific change at distinct locations is thought to indicate the dynamic formation of local neuronal assemblies during the activation of cortical object representations. As analytically power increase is just a property of a single location, phase-synchrony was introduced to investigate the formation of large-scale networks between spatially distant brain sites. However, classical phase-synchrony reveals symmetric, pair-wise correlations and is not suited to uncover the directionality of interactions. Here, we investigated the neural mechanism of visual object processing by means of directional coupling analysis going beyond recording sites, but rather assessing the directionality of oscillatory interactions between brain areas directly. This study is the first to identify the directionality of oscillatory brain interactions in source space during human object recognition and suggests that familiar, but not unfamiliar, objects engage widespread reciprocal information flow. Directionality of cortical information-flow was calculated based upon an established Granger-Causality coupling-measure (partial-directed coherence; PDC) using autoregressive modeling. To enable comparison with previous coupling studies lacking directional information, phase-locking analysis was applied, using wavelet-based signal decompositions. Both, autoregressive modeling and wavelet analysis, revealed an augmentation of iGBRs during the presentation of familiar objects relative to unfamiliar controls, which was localized to inferior-temporal, superior-parietal and frontal brain areas by means of distributed source reconstruction. The multivariate analysis of PDC evaluated each possible direction of brain interaction and revealed widespread reciprocal information-transfer during familiar object processing. In contrast, unfamiliar objects entailed a sparse number of only unidirectional connections converging to parietal areas. Considering the directionality of brain interactions, the current results might indicate that successful activation of object representations is realized through reciprocal (feed-forward and feed-backward) information-transfer of oscillatory connections between distant, functionally specific brain areas.     

Abnormal FMRI adaptation to unfamiliar faces in a case of developmental prosopamnesia

In rare cases, damage to the temporal lobe causes a selective impairment in the ability to learn new faces, a condition known as prosopamnesia [1]. Here we present the case of an individual with prosopamnesia in the absence of any acquired structural lesion. "C" shows intact processing of simple and complex nonface objects, but her ability to learn new faces is severely impaired. We used a neural marker of perceptual learning known as repetition suppression to examine functioning within C's fusiform face area (FFA), a region of cortex involved in face perception [2]. For comparison, we examined repetition suppression in the scene-selective parahippocampal place area (PPA) [3]. As expected, normal controls showed significant region-specific attenuation of neural activity across repetitions of each stimulus class. C also showed normal attenuation within the PPA to familiar and unfamiliar scenes, and within the FFA to familiar faces. Critically, however, she failed to show any adaptive change within the FFA for repeated unfamiliar faces, despite a face-specific blood-oxygen-dependent response (BOLD) response in her FFA during viewing of face stimuli. Our findings suggest that in developmental prosopamnesia, the FFA cannot maintain stable representations of new faces for subsequent recall or recognition.     

Effects of Caricaturing in Shape or Color on Familiarity Decisions for Familiar and Unfamiliar Faces

Recent evidence suggests that while reflectance information (including color) may be more diagnostic for familiar face recognition, shape may be more diagnostic for unfamiliar face identity processing. Moreover, event-related potential (ERP) findings suggest an earlier onset for neural processing of facial shape compared to reflectance. In the current study, we aimed to explore specifically the roles of facial shape and color in a familiarity decision task using pre-experimentally familiar (famous) and unfamiliar faces that were caricatured either in shape-only, color-only, or both (full; shape + color) by 15%, 30%, or 45%. We recorded accuracies, mean reaction times, and face-sensitive ERPs. Performance data revealed that shape caricaturing facilitated identity processing for unfamiliar faces only. In the ERP data, such effects of shape caricaturing emerged earlier than those of color caricaturing. Unsurprisingly, ERP effects were accentuated for larger levels of caricaturing. Overall, our findings corroborate the importance of shape for identity processing of unfamiliar faces and demonstrate an earlier onset of neural processing for facial shape compared to color.     

Identification and classification of facial familiarity in directed lying: an ERP study

Recognizing familiar faces is essential to social functioning, but little is known about how people identify human faces and classify them in terms of familiarity. Face identification involves discriminating familiar faces from unfamiliar faces, whereas face classification involves making an intentional decision to classify faces as "familiar" or "unfamiliar." This study used a directed-lying task to explore the differentiation between identification and classification processes involved in the recognition of familiar faces. To explore this issue, the participants in this study were shown familiar and unfamiliar faces. They responded to these faces (i.e., as familiar or unfamiliar) in accordance with the instructions they were given (i.e., to lie or to tell the truth) while their EEG activity was recorded. Familiar faces (regardless of lying vs. truth) elicited significantly less negative-going N400f in the middle and right parietal and temporal regions than unfamiliar faces. Regardless of their actual familiarity, the faces that the participants classified as "familiar" elicited more negative-going N400f in the central and right temporal regions than those classified as "unfamiliar." The P600 was related primarily with the facial identification process. Familiar faces (regardless of lying vs. truth) elicited more positive-going P600f in the middle parietal and middle occipital regions. The results suggest that N400f and P600f play different roles in the processes involved in facial recognition. The N400f appears to be associated with both the identification (judgment of familiarity) and classification of faces, while it is likely that the P600f is only associated with the identification process (recollection of facial information). Future studies should use different experimental paradigms to validate the generalizability of the results of this study.     

The 170ms Response to Faces as Measured by MEG (M170) Is Consistently Altered in Congenital Prosopagnosia

Modularity of face processing is still a controversial issue. Congenital prosopagnosia (cPA), a selective and lifelong impairment in familiar face recognition without evidence of an acquired cerebral lesion, offers a unique opportunity to support this fundamental hypothesis. However, in spite of the pronounced behavioural impairment, identification of a functionally relevant neural alteration in congenital prosopagnosia by electrophysiogical methods has not been achieved so far. Here we show that persons with congenital prosopagnosia can be distinguished as a group from unimpaired persons using magnetoencephalography. Early face-selective MEG-responses in the range of 140 to 200ms (the M170) showed prolonged latency and decreased amplitude whereas responses to another category (houses) were indistinguishable between subjects with congenital prosopagnosia and unimpaired controls. Latency and amplitude of face-selective EEG responses (the N170) which were simultaneously recorded were statistically indistinguishable between subjects with cPA and healthy controls which resolves heterogeneous and partly conflicting results from existing studies. The complementary analysis of categorical differences (evoked activity to faces minus evoked activity to houses) revealed that the early part of the 170ms response to faces is altered in subjects with cPA. This finding can be adequately explained in a common framework of holistic and part-based face processing. Whereas a significant brain-behaviour correlation of face recognition performance and the size of the M170 amplitude is found in controls a corresponding correlation is not seen in subjects with cPA. This indicates functional relevance of the alteration found for the 170ms response to faces in cPA and pinpoints the impairment of face processing to early perceptual stages.     

A specific and rapid neural signature for parental instinct

Darwin originally pointed out that there is something about infants which prompts adults to respond to and care for them, in order to increase individual fitness, i.e. reproductive success, via increased survivorship of one's own offspring. Lorenz proposed that it is the specific structure of the infant face that serves to elicit these parental responses, but the biological basis for this remains elusive. Here, we investigated whether adults show specific brain responses to unfamiliar infant faces compared to adult faces, where the infant and adult faces had been carefully matched across the two groups for emotional valence and arousal, as well as size and luminosity. The faces also matched closely in terms of attractiveness. Using magnetoencephalography (MEG) in adults, we found that highly specific brain activity occurred within a seventh of a second in response to unfamiliar infant faces but not to adult faces. This activity occurred in the medial orbitofrontal cortex (mOFC), an area implicated in reward behaviour, suggesting for the first time a neural basis for this vital evolutionary process. We found a peak in activity first in mOFC and then in the right fusiform face area (FFA). In mOFC the first significant peak (p<0.001) in differences in power between infant and adult faces was found at around 130 ms in the 10-15 Hz band. These early differences were not found in the FFA. In contrast, differences in power were found later, at around 165 ms, in a different band (20-25 Hz) in the right FFA, suggesting a feedback effect from mOFC. These findings provide evidence in humans of a potential brain basis for the "innate releasing mechanisms" described by Lorenz for affection and nurturing of young infants. This has potentially important clinical applications in relation to postnatal depression, and could provide opportunities for early identification of families at risk.     

Stable face representations

Photographs are often used to establish the identity of an individual or to verify that they are who they claim to be. Yet, recent research shows that it is surprisingly difficult to match a photo to a face. Neither humans nor machines can perform this task reliably. Although human perceivers are good at matching familiar faces, performance with unfamiliar faces is strikingly poor. The situation is no better for automatic face recognition systems. In practical settings, automatic systems have been consistently disappointing. In this review, we suggest that failure to distinguish between familiar and unfamiliar face processing has led to unrealistic expectations about face identification in applied settings. We also argue that a photograph is not necessarily a reliable indicator of facial appearance, and develop our proposal that summary statistics can provide more stable face representations. In particular, we show that image averaging stabilizes facial appearance by diluting aspects of the image that vary between snapshots of the same person. We review evidence that the resulting images can outperform photographs in both behavioural experiments and computer simulations, and outline promising directions for future research.     

Cortical responses to invisible faces: dissociating subsystems for facial-information processing

Perceiving faces is critical for social interaction. Evidence suggests that different neural pathways may be responsible for processing face identity and expression information. By using functional magnetic resonance imaging (fMRI), we measured brain responses when observers viewed neutral, fearful, and scrambled faces, either visible or rendered invisible through interocular suppression. The right fusiform face area (FFA), the right superior temporal sulcus (STS), and the amygdala responded strongly to visible faces. However, when face images became invisible, activity in FFA to both neutral and fearful faces was much reduced, although still measurable; activity in the STS was robust only to invisible fearful faces but not to neutral faces. Activity in the amygdala was equally strong in both the visible and invisible conditions to fearful faces but much weaker in the invisible condition for the neutral faces. In the invisible condition, amygdala activity was highly correlated with that of the STS but not with FFA. The results in the invisible condition support the existence of dissociable neural systems specialized for processing facial identity and expression information. When images are invisible, cortical responses may reflect primarily feed-forward visual-information processing and thus allow us to reveal the distinct functions of FFA and STS.     

Face pictures reduce behavioural, autonomic, endocrine and neural indices of stress and fear in sheep

Faces are highly emotive stimuli and we find smiling or familiar faces both attractive and comforting, even as young babies. Do other species with sophisticated face recognition skills, such as sheep, also respond to the emotional significance of familiar faces? We report that when sheep experience social isolation, the sight of familiar sheep face pictures compared with those of goats or inverted triangles significantly reduces behavioural (activity and protest vocalizations), autonomic (heart rate) and endocrine (cortisol and adrenaline) indices of stress. They also increase mRNA expression of activity-dependent genes (c-fos and zif/268) in brain regions specialized for processing faces (temporal and medial frontal cortices and basolateral amygdala) and for emotional control (orbitofrontal and cingulate cortex), and reduce their expression in regions associated with stress responses (hypothalamic paraventricular nucleus) and fear (central and lateral amygdala). Effects on face recognition, emotional control and fear centres are restricted to the right brain hemisphere. Results provide evidence that face pictures may be useful for relieving stress caused by unavoidable social isolation in sheep, and possibly other animal species, including humans. The finding that sheep, like humans, appear to have a right brain hemisphere involvement in the control of negative emotional experiences also suggests that functional lateralization of brain emotion systems may be a general feature in mammals.     

Transcranial Direct Current Stimulation of the Dorsolateral Prefrontal Cortex Modulates Repetition Suppression to Unfamiliar Faces: An ERP Study

Repeated visual processing of an unfamiliar face suppresses neural activity in face-specific areas of the occipito-temporal cortex. This "repetition suppression" (RS) is a primitive mechanism involved in learning of unfamiliar faces, which can be detected through amplitude reduction of the N170 event-related potential (ERP). The dorsolateral prefrontal cortex (DLPFC) exerts top-down influence on early visual processing. However, its contribution to N170 RS and learning of unfamiliar faces remains unclear. Transcranial direct current stimulation (tDCS) transiently increases or decreases cortical excitability, as a function of polarity. We hypothesized that DLPFC excitability modulation by tDCS would cause polarity-dependent modulations of N170 RS during encoding of unfamiliar faces. tDCS-induced N170 RS enhancement would improve long-term recognition reaction time (RT) and/or accuracy rates, whereas N170 RS impairment would compromise recognition ability. Participants underwent three tDCS conditions in random order at ∼72 hour intervals: right anodal/left cathodal, right cathodal/left anodal and sham. Immediately following tDCS conditions, an EEG was recorded during encoding of unfamiliar faces for assessment of P100 and N170 visual ERPs. The P3a component was analyzed to detect prefrontal function modulation. Recognition tasks were administered ∼72 hours following encoding. Results indicate the right anodal/left cathodal condition facilitated N170 RS and induced larger P3a amplitudes, leading to faster recognition RT. Conversely, the right cathodal/left anodal condition caused N170 amplitude and RTs to increase, and a delay in P3a latency. These data demonstrate that DLPFC excitability modulation can influence early visual encoding of unfamiliar faces, highlighting the importance of DLPFC in basic learning mechanisms.     

Neural representations of personally familiar and unfamiliar faces in the anterior inferior temporal cortex of monkeys

To investigate the neural representations of faces in primates, particularly in relation to their personal familiarity or unfamiliarity, neuronal activities were chronically recorded from the ventral portion of the anterior inferior temporal cortex (AITv) of macaque monkeys during the performance of a facial identification task using either personally familiar or unfamiliar faces as stimuli. By calculating the correlation coefficients between neuronal responses to the faces for all possible pairs of faces given in the task and then using the coefficients as neuronal population-based similarity measures between the faces in pairs, we analyzed the similarity/dissimilarity relationship between the faces, which were potentially represented by the activities of a population of the face-responsive neurons recorded in the area AITv. The results showed that, for personally familiar faces, different identities were represented by different patterns of activities of the population of AITv neurons irrespective of the view (e.g., front, 90° left, etc.), while different views were not represented independently of their facial identities, which was consistent with our previous report. In the case of personally unfamiliar faces, the faces possessing different identities but presented in the same frontal view were represented as similar, which contrasts with the results for personally familiar faces. These results, taken together, outline the neuronal representations of personally familiar and unfamiliar faces in the AITv neuronal population.     

Facial Recognition in a Group-Living Cichlid Fish

The theoretical underpinnings of the mechanisms of sociality, e.g. territoriality, hierarchy, and reciprocity, are based on assumptions of individual recognition. While behavioural evidence suggests individual recognition is widespread, the cues that animals use to recognise individuals are established in only a handful of systems. Here, we use digital models to demonstrate that facial features are the visual cue used for individual recognition in the social fish Neolamprologus pulcher. Focal fish were exposed to digital images showing four different combinations of familiar and unfamiliar face and body colorations. Focal fish attended to digital models with unfamiliar faces longer and from a further distance to the model than to models with familiar faces. These results strongly suggest that fish can distinguish individuals accurately using facial colour patterns. Our observations also suggest that fish are able to rapidly (≤ 0.5 sec) discriminate between familiar and unfamiliar individuals, a speed of recognition comparable to primates including humans.     

Neurophysiological mechanisms underlying face processing within and beyond the temporal cortical visual areas.

The ways in which information about faces is represented and stored in the temporal lobe visual areas of primates, as shown by recordings from single neurons in macaques, are considered. Some neurons that respond primarily to faces are found in the cortex in the anterior part of the superior temporal sulcus (in which neurons are especially likely to be tuned to facial expression and to face movement involved in gesture), and in the TE areas more ventrally forming the inferior temporal gyrus (in which neurons are more likely to have responses related to the identity of faces). Quantitative studies of the responses of the neurons that respond differently to the faces of different individuals show that information about the identity of the individual is represented by the responses of a population of neurons, that is, ensemble encoding rather than 'grandmother cell' encoding is used. It is argued that this type of tuning is a delicate compromise between very fine tuning, which has the advantage of low interference in neuronal network operations but the disadvantage of losing the useful properties (such as generalization, completion and graceful degradation) of storage in neuronal networks, and broad tuning, which has the advantage of allowing these properties of neuronal networks to be realized but the disadvantage of leading to interference between the different memories stored in an associative network. There is evidence that the responses of some of these neurons are altered by experience so that new stimuli become incorporated in the network. It is shown that the representation that is built in temporal cortical areas shows considerable invariance for size, contrast, spatial frequency and translation. Thus the representation is in a form which is particularly useful for storage and as an output from the visual system. It is also shown that one of the representations that is built is object based, which is suitable for recognition and as an input to associative memory, and that another is viewer centred, which is appropriate for conveying information about gesture. Ways are considered in which such cortical representations might be built by competitive self-organization aided by back projections in the multi-stage cortical processing hierarchy which has convergence from stage to stage.     

Asymmetrical activation in the human brain during processing of fearful faces

Traditional split-field studies and patient research indicate a privileged role for the right hemisphere in emotional processing [1-7], but there has been little direct fMRI evidence for this, despite many studies on emotional-face processing [8-10](see Supplemental Background). With fMRI, we addressed differential hemispheric processing of fearful versus neutral faces by presenting subjects with faces bilaterally [11-13]and orthogonally manipulating whether each hemifield showed a fearful or neutral expression prior to presentation of a checkerboard target. Target discrimination in the left visual field was more accurate after a fearful face was presented there. Event-related fMRI showed right-lateralized brain activations for fearful minus neutral left-hemifield faces in right visual areas, as well as more activity in the right than in the left amygdala. These activations occurred regardless of the type of right-hemifield face shown concurrently, concordant with the behavioral effect. No analogous behavioral or fMRI effects were observed for fearful faces in the right visual field (left hemisphere). The amygdala showed enhanced functional coupling with right-middle and anterior-fusiform areas in the context of a left-hemifield fearful face. These data provide behavioral and fMRI evidence for right-lateralized emotional processing during bilateral stimulation involving enhanced coupling of the amygdala and right-hemispheric extrastriate cortex.     

Multivoxel Patterns in Fusiform Face Area Differentiate Faces by Sex and Race

Although prior research suggests that fusiform gyrus represents the sex and race of faces, it remains unclear whether fusiform face area (FFA)–the portion of fusiform gyrus that is functionally-defined by its preferential response to faces–contains such representations. Here, we used functional magnetic resonance imaging to evaluate whether FFA represents faces by sex and race. Participants were scanned while they categorized the sex and race of unfamiliar Black men, Black women, White men, and White women. Multivariate pattern analysis revealed that multivoxel patterns in FFA–but not other face-selective brain regions, other category-selective brain regions, or early visual cortex–differentiated faces by sex and race. Specifically, patterns of voxel-based responses were more similar between individuals of the same sex than between men and women, and between individuals of the same race than between Black and White individuals. By showing that FFA represents the sex and race of faces, this research contributes to our emerging understanding of how the human brain perceives individuals from two fundamental social categories.     

Recognizing faces

Face recognition is an area where research has increased considerably in recent years, yet theoretical progress has been slow. Here it is argued that by considering the perception and recognition of familiar faces, as well as episodic memory for unfamiliar faces, a functional framework for face recognition can be developed. Experiments using faces, that include tasks analogous to 'visual search' and 'lexical decision' are described, and the processes in operation are compared with those occurring in word recognition. The results allow us to distinguish a number of possible subcomponents for a functional model of face recognition.