Interhemispheric cooperation for familiar but not unfamiliar face processing

Evidence for interhemispheric cooperation during language processing has been demonstrated for words, but not for meaningless pseudowords. Specifically, responses were found to be faster and more accurate when identical copies of a word were presented bilaterally to both hemispheres, relative to unilateral single presentations. This bilateral advantage for words seems to be a robust effect in normals. The present study addressed the question of whether the bilateral advantage is restricted to lexical material or whether it is a more global phenomenon occurring for meaningful material in general. Thirty healthy participants performed a familiarity decision in which one copy of familiar and unfamiliar faces was presented tachistoscopically to the right visual hemifield (RVF), the left visual hemifield (LVF) or simultaneously to both visual hemifields (bilateral condition, BVF). We obtained a highly significant familiarity by visual field interaction(P < 0.006) showing that only for familiar faces, a bilateral advantage was obtained. Unfamiliar face processing did not yield a bilateral advantage. We conclude that interhemispheric cooperation only occurs for meaningful material for which cortical representations can be assumed.     

Asymmetry in face processing during childhood measured with chimeric faces

Studies with adults have found a left bias in their perception of faces, which suggests a right hemisphere specialisation in processing facial information. Hemispheric asymmetry is observed during the first year of life but it is still unclear at what age such specialisation becomes adult-like during the prolonged period of face-processing development through childhood. In the present study we investigated the development of children's perceptions of gender and emotion using chimeric faces. Our results demonstrate that a right hemisphere bias, similar to that found in adults, is observed from 5 years of age. The results are discussed within a framework of developmental studies and we conclude that although children may be less efficient than adults at encoding faces, their basic manner of encoding is not fundamentally different from that of adults.     

Shyness and the first 100 ms of emotional face processing

Although shyness is presumed to be related to an increased sensitivity to detect motivationally salient social stimuli, we know little of how shyness affects the early perception of facial emotions. We demonstrate here that individual differences in normative shyness were related to brain responses to some emotional faces as early as the P1 electrocortical component, 80–130 ms after stimulus onset. High-shy individuals showed reduced P1 amplitude for fearful faces compared to neutral faces. Low-shy individuals processed happy faces faster than other emotions and showed increased P1 amplitudes for happy faces over neutral faces. Regardless of shyness level, participants showed increased amplitudes in the N170 component (130–200 ms) for all emotions over neutral conditions, particularly for the emotion of fear. This study presents the first evidence that shyness is related to early electrocortical responses to the processing of fearful faces, consistent with a fast-path amygdala sensitivity model.     

Faster, stronger, lateralized: low spatial frequency information supports face processing

Distinct visual pathways are selectively tuned for processing specific spatial frequencies. Recently, Awasthi, Friedman, and Williams (2011) reported fast categorisation of faces at periphery, arguing for primacy of low spatial frequency (LSF) information in face processing. However, previous studies have also documented rapid categorization of places and natural scenes. Here, we tested if the LSF advantage is face specific or also involved in place perception. We used visually guided reaching as a continuous behavioral measure to examine the processing of LSF and high spatial frequency (HSF) hybrids, presented at the periphery. Subjects reached out and touched targets and their movements were recorded. The trajectories revealed that LSF interference was both 95 ms earlier and stronger for faces than places and was lateralized to the left visual field. The early processing of LSF information supports the assumption that faces are prioritised and provides a (neural) framework for such specialised processing.     

Interhemispheric cooperation for face recognition but not for affective facial expressions

Interhemispheric cooperation can be indicated by enhanced performance when stimuli are presented to both visual fields relative to one visual field alone. This "bilateral gain" is seen for words but not pseudowords in lexical decision tasks, and has been attributed to the operation of interhemispheric cell assemblies that exist only for meaningful words with acquired cortical representations. Recently, a bilateral gain has been reported for famous but not unfamiliar faces in a face recognition task [Neuropsychologia 40 (2002) 1841]. In Experiment 1 of the present paper, participants performed familiarity decisions for faces that were presented to the left (LVF), the right (RVF), or to both visual fields (BVF). An advantage for BVF relative to both LVF and RVF stimuli was seen in reaction times (RTs) to famous faces, but this bilateral advantage was absent for unfamiliar faces. In Experiment 2, participants classified the expression (happy or neutral) of unfamiliar faces. No bilateral advantage was seen for expressions, although a right hemisphere superiority was seen in terms of higher accuracy for LVF and BVF trials relative to the RVF. Recognition of famous faces (but not of facial expressions) require access to acquired memory representations that may be instantiated via cortical cell assemblies, and it is suggested that interhemispheric cooperation depends on these acquired cortical representations.     

The bilateral advantage for famous faces: interhemispheric communication or competition?

The bilateral advantage for the perception of famous faces was investigated using a redundant target procedure. In experiment 1 we compared simultaneous presentation of stimuli (a) bilaterally and (b) one above the other in the central field. Results showed a redundancy advantage, but only when faces were presented bilaterally. This result lends support to the notion of interhemispheric communication using cross-hemisphere representations. Experiment 2 examined the nature of such communication by comparing bilateral presentation of identical face images, with bilateral presentation of different images of the same person. When asked to make a familiar/unfamiliar face judgement, participants showed evidence for a redundancy advantage under both bilateral conditions. This suggests that the nature of the information shared in interhemispheric communication is abstract, rather than being tied to superficial stimulus properties.     

Dissociation between face perception and face memory in adults,but not children,with developmental prosopagnosia

Cognitive models propose that face recognition is accomplished through a series of discrete stages, including perceptual representation of facial structure, and encoding and retrieval of facial information. This implies that impaired face recognition can result from failures of face perception, face memory, or both. Studies of acquired prosopagnosia, autism spectrum disorders, and the development of normal face recognition support the idea that face perception and face memory are distinct processes, yet this distinction has received little attention in developmental prosopagnosia (DP). To address this issue, we tested the face perception and face memory of children and adults with DP. By definition, face memory is impaired in DP, so memory deficits were present in all participants. However, we found that all children, but only half of the adults had impaired face perception. Thus, results from adults indicate that face perception and face memory are dissociable, while the results from children provide no evidence for this division. Importantly, our findings raise the possibility that DP is qualitatively different in childhood versus adulthood. We discuss theoretical explanations for this developmental pattern and conclude that longitudinal studies are necessary to better understand the developmental trajectory of face perception and face memory deficits in DP.     

An event-related brain potential study of explicit face recognition

To determine the time course of face recognition and its links to face-sensitive event-related potential (ERP) components, ERPs elicited by faces of famous individuals and ERPs to non-famous control faces were compared in a task that required explicit judgements of facial identity. As expected, the face-selective N170 component was unaffected by the difference between famous and non-famous faces. In contrast, the occipito-temporal N250 component was linked to face recognition, as it was selectively triggered by famous faces. Importantly, this component was present for famous faces that were judged to be definitely known relative to famous faces that just appeared familiar, demonstrating that it is associated with the explicit identification of a particular face. The N250 is likely to reflect early perceptual stages of face recognition where long-term memory traces of familiar faces in ventral visual cortex are activated by matching on-line face representations. Famous faces also triggered a broadly distributed longer-latency positivity (P600f) that showed a left-hemisphere bias and was larger for definitely known faces, suggesting links between this component and name generation. These results show that successful face recognition is predicted by ERP components over face-specific visual areas that emerge within 230 ms after stimulus onset.     

Perceptual and anatomic patterns of selective deficits in facial identity and expression processing

Whether a single perceptual process or separate and possibly independent processes support facial identity and expression recognition is unclear. We used a morphed-face discrimination test to examine sensitivity to facial expression and identity information in patients with occipital or temporal lobe damage, and structural and functional MRI to correlate behavioral deficits with damage to the core regions of the face-processing network. We found selective impairments of identity perception in two patients with right inferotemporal lesions and two prosopagnosic patients with damage limited to the anterior temporal lobes. Of these four patients one exhibited damage to the right fusiform and occipital face areas, while the remaining three showed sparing of these regions. Thus impaired identity perception can occur with damage not only to the fusiform and occipital face areas, but also to other medial occipitotemporal structures that likely form part of a face recognition network. Impaired expression perception was seen in the fifth patient with damage affecting the face-related portion of the posterior superior temporal sulcus. This subject also had difficulty in discriminating identity when irrelevant variations in expression needed to be discounted. These neuropsychological and neuroimaging data provide evidence to complement models which address the separation of expression and identity perception within the face-processing network.     

Inverted face processing in body dysmorphic disorder

Individuals with body dysmorphic disorder (BDD) are preoccupied with perceived defects in appearance. Preliminary evidence suggests abnormalities in global and local visual information processing. The objective of this study was to compare global and local processing in BDD subjects and healthy controls by testing the face inversion effect, in which inverted (upside-down) faces are recognized more slowly and less accurately relative to upright faces. Eighteen medication-free subjects with BDD and 17 matched, healthy controls performed a recognition task with sets of upright and inverted faces on a computer screen that were either presented for short duration (500 ms) or long duration (5000 ms). Response time and accuracy rates were analyzed using linear and logistic mixed effects models, respectively. Results indicated that the inversion effect for response time was smaller in BDD subjects than controls during the long duration stimuli, but was not significantly different during the short duration stimuli. Inversion effect on accuracy rates did not differ significantly between groups during either of the two durations. Lesser inversion effect in BDD subjects may be due to greater detail-oriented and piecemeal processing for long duration stimuli. Similar results between groups for short duration stimuli suggest that they may be normally engaging configural and holistic processing for brief presentations. Abnormal visual information processing in BDD may contribute to distorted perception of appearance; this may not be limited to their own faces, but to others’ faces as well.     

Familiarity facilitates the corticocortical processing of face perception

The visual evoked potentials elicited by mosaic pictures were used to elucidate the initial step of face perception. Three different mosaic levels (subthreshold, threshold, suprathreshold) for familiar and unfamiliar faces and objects were randomly presented for 250 ms. The latencies of occipital N1 and posterior-temporal N2 were shortened by decreasing the mosaic levels of faces but not for object. The N2 amplitude significantly increased at threshold and suprathreshold levels for familiar and unfamiliar faces. The latency difference between N1 and N2 at threshold level for a familiar face was significantly shortened compared with that for an unfamiliar face. Our findings suggest the initial step of face perception is already set in the primary visual cortex, and familiarity can facilitate the corticocortical processing of face information.     

Whole not hole: Expert face recognition requires holistic perception

Face recognition is an important ability of the human brain, yet its underlying mechanisms are still poorly understood. Two opposite views have been proposed to account for human face recognition expertise: the ability to extract the most diagnostic local information, feature-by feature (analytical view), or the ability to process all features at once over the whole face (holistic view). To help clarifying this debate, we used an original gaze-contingent stimulus presentation method to compare normal observers and a brain-damaged patient specifically impaired at face recognition (prosopagnosia). When a single central facial feature was revealed at a time through a gaze-contingent window, normal observers’ performance at an individual face matching task decreased to the patient level. However, when only the central feature was masked, forcing normal observers to rely on the whole face but the fixated feature, their performance was almost not affected. In contrast, the prosopagnosic patient's performance decreased dramatically in this latter condition. These results were independent of the absolute size of the face and window/mask. This dissociation indicates that expertise in face recognition does not rest on the ability to analyze diagnostic local detailed features sequentially but rather on the ability to see the individual features of a face all at once, a function that is critically impaired in acquired prosopagnosia.     

Disconnection in prosopagnosia and face processing

Face perception is a function with significant complexity, reflected in cognitive models that propose a hierarchy of parallel and serial processing stages. Current neuroimaging data also show that face perception involves a core processing network of cortical modules, which are likely specialized for different functions involved in face processing. The core face processing network is further linked to an extended face processing network which is not solely involved in the perception of faces, but rather contains modules mediating the processing of semantic, biographic and emotional information about people. The segregation of these processes within discrete anatomic regions creates the potential for disconnection between regions to generate neuropsychological deficits involving faces. In this review we consider the types of disconnection possible both within the core face processing system and between the core and extended systems, the pattern of deficits that would be considered as evidence of such disconnections, the potential anatomy of lesions that would create them, and whether any cases exist that meet these criteria.     

Temporal dynamics of face repetition suppression

Single-unit recordings and functional brain imaging studies have shown reduced neural responses to repeated stimuli in the visual cortex. Using MEG, we compared responses evoked by repetitions of neutral faces to those evoked by fearful faces, which were either task relevant (targets) or irrelevant (distracters). Faces evoked a bi-phasic response in extrastriate cortex, peaking at 160–185 ms and at 220–250 ms, with stronger responses to neutral faces at the earlier interval and stronger responses to fearful faces at the later interval. At both latencies, repetitions of neutral and fearful targets resulted in reduced amplitude of the MEG signal. Additionally, we found that the context in which targets were presented affected their processing: fearful distracters increased the responses evoked by both neutral and fearful targets. Our data indicate that valence enhancement and context effects can be detected in extrastriate visual cortex within 250 ms and that these processes likely reflect feedback from other regions.     

Examining the relationship between face processing and social interaction behavior in children with and without autism spectrum disorder

Background

Children with autism spectrum disorder (ASD) show impairment in reciprocal social communication, which includes deficits in social cognition and behavior. Since social cognition and social behavior are considered to be interdependent, it is valuable to examine social processes on multiple levels of analysis. Neuropsychological measures of face processing often reveal deficits in social cognition in ASD including the ability to identify and remember facial information. However, the extent to which neuropsychological measures are associated with or predictive of real-world social behavior is unclear.

Methods

The study investigated 66 children (ASD 34, typically developing (TD) 32) using neuropsychological measures of face processing (identity, affect, and memory). Children also participated in a peer interaction paradigm, which allowed observation and coding of natural social interaction behaviors during play with peers (e.g., Self-Play, Cooperative Play, Verbal Bout). ANCOVA, regression, and correlation models analyzed between-group differences, the ability of neuropsychological measures to predict social behavior, and the strength of the associations.

Results

Between-group differences were shown on Memory for Faces Delayed and the peer interaction variables Self-Play and Verbal Bout. Regression models indicated that Memory for Faces Delayed predicted the amount of Self-Play, Equipment use alone, and Cooperative Play with peers on the playground. Autism symptomology only predicted verbal exchange with peers.

Conclusions

Face memory strongly predicts relevant social engagement patterns in both children with and without ASD. Impairment in facial memory is associated with reduced ‘real-world’ social interaction and more self-play, whereas higher performance in face memory predicts more cooperative play. Results highlight the strong connection between face memory and reciprocal social interaction, suggesting that improvement in one may benefit the other.     

EEG correlates of categorical and graded face perception

Face perception is a critical social ability and identifying its neural correlates is important from both basic and applied perspectives. In EEG recordings, faces elicit a distinct electrophysiological signature, the N170, which has a larger amplitude and shorter latency in response to faces compared to other objects. However, determining the face specificity of any neural marker for face perception hinges on finding an appropriate control stimulus. We used a novel stimulus set consisting of 300 images that spanned a continuum between random patches of natural scenes and genuine faces, in order to explore the selectivity of face-sensitive ERP responses with a model-based parametric stimulus set. Critically, our database contained “false alarm” images that were misclassified as face by computational face-detection system and varied in their image-level similarity to real faces. High-density (128-channel) event-related potentials (ERPs) were recorded while 23 adult subjects viewed all 300 images in random order, and determined whether each image was a face or non-face. The goal of our analyses was to determine the extent to which a gradient of sensitivity to face-like structure was evident in the ERP signal. Traditional waveform analyses revealed that the N170 component over occipitotemporal electrodes was larger in amplitude for faces compared to all non-faces, even those that were high in image similarity to faces, suggesting strict selectivity for veridical face stimuli. By contrast, single-trial classification of the entire waveform measured at the same sensors revealed that misclassifications of non-face patterns as faces increased with image-level similarity to faces. These results suggest that individual components may exhibit steep selectivity, but integration of multiple waveform features may afford graded information regarding stimulus appearance.     

Two neural pathways of face processing: A critical evaluation of current models

The neural basis of face processing has been extensively studied in the past two decades. The current dominant neural model proposed by Haxby et al. (2000); Gobbini and Haxby (2007) suggests a division of labor between the fusiform face area (FFA), which processes invariant facial aspects, such as identity, and the posterior superior temporal sulcus (pSTS), which processes changeable facial aspects, such as expression. An extension to this model for the processing of dynamic faces proposed by O’Toole et al. (2002) highlights the role of the pSTS in the processing of identity from dynamic familiar faces. To evaluate these models, we reviewed recent neuroimaging studies that examined the processing of identity and expression with static and dynamic faces. Based on accumulated data we propose an updated model, emphasizing the dissociation between form and motion as the primary functional division between a ventral stream that goes through the FFA and a dorsal stream that goes through the STS, respectively. We also encourage future studies to expand their research to the processing of dynamic faces.     

The asymmetry of the fusiform face area is a stable individual characteristic that underlies the left-visual-field superiority for faces

Recognition of faces is better when faces are presented in the left than right-visual-field. Furthermore, this perceptual asymmetry is a stable individual characteristic. Although it has been commonly assumed that the right hemispheric dominance for face processing underlies this left-visual-field superiority in face recognition, this neural-behavioral association has never been directly demonstrated. Here we applied functional MRI (fMRI) to measure the magnitude of the asymmetric response to faces for each subject. To determine whether the asymmetric neural response to faces is stable across sessions, subjects returned for a second fMRI session. In addition, subjects performed a behavioral experiment outside the scanner where they had to recognize centrally presented chimeric faces, which presented different identities in the right- and left-visual-field. This task yielded a measure of the magnitude of the left-visual-field bias for each subject. Our findings show that the magnitude of the asymmetry of the face-selective area in the fusiform gyrus (FFA) is highly consistent for each individual across scans. We then show that the behavioral left-visual-field asymmetry, measured outside the scanner, was strongly and specifically correlated with the asymmetry of the FFA across subjects, but not with other face-specific or nearby object-general regions. Our findings provide the first empirical evidence for the prevalent idea that perceptual asymmetries in face recognition are associated with the well-known hemispheric asymmetry for faces. We conclude that the FFA asymmetry is a highly stable individual characteristic that underlies the well-established left-visual-field superiority for face recognition.     

Neurophysiological correlates of face gender processing in humans

Event-related potentials (ERPs) were recorded while subjects were involved in three gender-processing tasks based on human faces and on human hands. In one condition all stimuli were only of one gender, preventing any gender discrimination. In a second condition, faces (or hands) of men and women were intermixed but the gender was irrelevant for the subject's task; hence gender discrimination was assumed to be incidental. In the third condition, the task required explicit gender discrimination; gender processing was therefore assumed to be intentional. Gender processing had no effect on the occipito-temporal negative potential at approximately 170 ms after stimulation (N170 component of the ERP), suggesting that the neural mechanisms involved in the structural encoding of faces are different from those involved in the extraction of gender-related facial features. In contrast, incidental and intentional processing of face (but not hand) gender affected the ERPs between 145 and 185 ms from stimulus onset at more anterior scalp locations. This effect was interpreted as evidence for the direct visual processing of faces as described in Bruce and Young's model [Bruce, V. & Young, A. (1986) Br. J. Psychol., 77, 305-327]. Additional gender discrimination effects were observed for both faces and hands at mid-parietal sites around 45-85 ms latency, in the incidental task only. This difference was tentatively assumed to reflect an early mechanism of coarse visual categorization. Finally, intentional (but not incidental) gender processing affected the ERPs during a later epoch starting from approximately 200 ms and ending at approximately 250 ms for faces, and approximately 350 ms for hands. This later effect might be related to attention-based gender categorization or to a more general categorization activity.     

Impaired holistic processing in congenital prosopagnosia

It has long been argued that face processing requires disproportionate reliance on holistic or configural processing, relative to that required for non-face object recognition, and that a disruption of such holistic processing may be causally implicated in prosopagnosia. Previously, we demonstrated that individuals with congenital prosopagnosia (CP) did not show the normal face inversion effect (better performance for upright compared to inverted faces) and evinced a local (rather than the normal global) bias in a compound letter global/local (GL) task, supporting the claim of disrupted holistic processing in prosopagnosia. Here, we investigate further the nature of holistic processing impairments in CP, first by confirming, in a large sample of CP individuals, the absence of the normal face inversion effect and the presence of the local bias on the GL task, and, second, by employing the composite face paradigm, often regarded as the gold standard for measuring holistic face processing. In this last task, we show that, in contrast with controls, the CP group perform equivalently with aligned and misaligned faces and was impervious to (the normal) interference from the task-irrelevant bottom part of faces. Interestingly, the extent of the local bias evident in the composite task is correlated with the abnormality of performance on diagnostic face processing tasks. Furthermore, there is a significant correlation between the magnitude of the local bias in the GL and performance on the composite task. These results provide further evidence for impaired holistic processing in CP and, moreover, corroborate the critical role of this type of processing for intact face recognition.