Exploring face perception in disorders of development: Evidence from Williams syndrome and autism

Individuals with Williams syndrome (WS) and autism are characterized by different social phenotypes but have been said to show similar atypicalities of face‐processing style. Although the structural encoding of faces may be similarly atypical in these two developmental disorders, there are clear differences in overall face skills. The inclusion of both populations in the same study can address how the profile of face skills varies across disorders. The current paper explored the processing of identity, eye‐gaze, lip‐reading, and expressions of emotion using the same participants across face domains. The tasks had previously been used to make claims of a modular structure to face perception in typical development. Participants with WS (N=15) and autism (N=20) could be dissociated from each other, and from individuals with general developmental delay, in the domains of eye‐gaze and expression processing. Individuals with WS were stronger at these skills than individuals with autism. Even if the structural encoding of faces appears similarly atypical in these groups, the overall profile of face skills, as well as the underlying architecture of face perception, varies greatly. The research provides insights into typical and atypical models of face perception in WS and autism.     

Finding a face in the crowd: testing the anger superiority effect in Asperger Syndrome

Social threat captures attention and is processed rapidly and efficiently, with many lines of research showing involvement of the amygdala. Visual search paradigms looking at social threat have shown angry faces 'pop-out' in a crowd, compared to happy faces. Autism and Asperger Syndrome (AS) are neurodevelopmental conditions characterised by social deficits, abnormal face processing, and amygdala dysfunction. We tested adults with high-functioning autism (HFA) and AS using a facial visual search paradigm with schematic neutral and emotional faces. We found, contrary to predictions, that people with HFA/AS performed similarly to controls in many conditions. However, the effect was reduced in the HFA/AS group when using widely varying crowd sizes and when faces were inverted, suggesting a difference in face-processing style may be evident even with simple schematic faces. We conclude there are intact threat detection mechanisms in AS, under simple and predictable conditions, but that like other face-perception tasks, the visual search of threat faces task reveals atypical face-processing in HFA/AS.     

Face engagement during infancy predicts later face recognition ability in younger siblings of children with autism

Face recognition difficulties are frequently documented in children with autism spectrum disorders (ASD). It has been hypothesized that these difficulties result from a reduced interest in faces early in life, leading to decreased cortical specialization and atypical development of the neural circuitry for face processing. However, a recent study by our lab demonstrated that infants at increased familial risk for ASD, irrespective of their diagnostic status at 3 years, exhibit a clear orienting response to faces. The present study was conducted as a follow‐up on the same cohort to investigate how measures of early engagement with faces relate to face‐processing abilities later in life. We also investigated whether face recognition difficulties are specifically related to an ASD diagnosis, or whether they are present at a higher rate in all those at familial risk. At 3 years we found a reduced ability to recognize unfamiliar faces in the high‐risk group that was not specific to those children who received an ASD diagnosis, consistent with face recognition difficulties being an endophenotype of the disorder. Furthermore, we found that longer looking at faces at 7 months was associated with poorer performance on the face recognition task at 3 years in the high‐risk group. These findings suggest that longer looking at faces in infants at risk for ASD might reflect early face‐processing difficulties and predicts difficulties with recognizing faces later in life.     

高功能自闭症个体对威胁性情绪面孔的注意偏向

高功能自闭症(High-Functioning Autism, HFA)个体智力正常, 但也面临着严重的社会功能障碍。对威胁性情绪面孔的注意偏向与HFA个体社会功能的发展密切相关。梳理相关研究发现, HFA个体在自动加工阶段和情绪目标参与阶段, 不存在威胁性情绪面孔注意偏向; 而在任务与情绪无关的控制加工阶段, 存在威胁性情绪面孔注意偏向。针对HFA个体威胁性情绪面孔注意偏向的理论解释主要有杏仁核理论、强烈世界理论和执行功能理论等。神经生理机制方面, HFA个体对威胁性情绪面孔的注意偏向可能与其异常的皮下及皮层通路功能有关, 同时可能会受5-羟色胺系统基因及催产素水平等的影响。未来研究可在综合考虑研究方法及个体因素的基础上, 进一步探究其加工特征及神经生物机制, 着力开发科学有效的干预策略。     

Face processing in adolescents with autistic disorder: the inversion and composite effects

Two experiments with upright and inverted face and object images were carried out to investigate whether face processing in autism is more feature-based than in individuals with typical development. Participants were 17 high-ability adolescents with autistic disorder (16-24 years), 24 typically developing children (9-10 years) and 16 adults (18-33 years). In Experiment 1, a normal inversion effect was found for the adolescents with autism in a standard face recognition paradigm with reduced memory demands, except for a subgroup with low social intelligence who were not better in recognizing upright relative to inverted photographs of faces. In Experiment 2, the group with autism did not show the composite effect like the adult group did: they recognized face halves as well in aligned composite faces as in non-aligned composite faces. The results on the inversion task suggest that most adolescents with autism form a normal configuration-based face representation, but the absence of the composite effect indicates that they are less prone to use the contextual information of the face in a visual-search task.     

Neural bases and development of face recognition in autism

This paper critically examines the literature on face recognition in autism, including a discussion of the neural correlates of this ability. The authors begin by selectively reviewing the behavioral and cognitive neuroscience research on whether faces are represented by a "special" behavioral and neural system-one distinct from object processing. The authors then offer a neuroconstructivist model that attempts to account for the robust finding that certain regions in the inferior temporal cortex are recruited in the service of face recognition. This is followed by a review of the evidence supporting the view that face recognition is atypical in individuals with autism. This face-recognition deficit may indicate a continued risk for the further development of social impairments. The authors conclude by speculating on the role of experience in contributing to this atypical developmental pattern and its implications for normal development of face processing.     

Neural recruitment related to threat perception differs as a function of adolescent sleep

Detecting threat cues in the environment is an important aspect of social functioning. This is particularly true for adolescents as social threats become more salient and they navigate increasingly complex relationships outside of the family. Sleep relates to socioemotional processing throughout development, but the neurobiological relevance of sleep for threat perceptions in adolescence remains unknown. In the present study, 46 human adolescents (aged 14–18 years; 26 female) made judgments while undergoing a brain scan about whether unfamiliar, affectively neutral, computer‐generated faces were threatening. Prior to the scan, several indices of sleep were assessed nightly for two‐weeks using actigraphy. Sleep duration and poor sleep quality (defined as less efficiency, more awakenings, longer awakenings), factors influenced by biological and psychosocial changes during adolescence, elicited distinct neural activation patterns. Sleep duration was positively associated with activation in visual and face processing regions (occipital cortex, occipital fusiform gyrus), and this activation was linked to increased threat detection during the threat perception task. Sleep quality was negatively related to dorsolateral prefrontal cortex activation, which moderated the relation between reaction time (RT) and exposure to faces. Findings suggest reduced threat perception for adolescents with shorter sleep durations and more impulsive responding (as evinced by less consistent RT) for adolescents experiencing worse quality sleep. This study identifies an association between sleep and neural functioning relevant for socioemotional decision making during adolescence, a time when these systems undergo significant development.     

Neural correlates of perceptual narrowing in cross‐species face‐voice matching

Integrating the multisensory features of talking faces is critical to learning and extracting coherent meaning from social signals. While we know much about the development of these capacities at the behavioral level, we know very little about the underlying neural processes. One prominent behavioral milestone of these capacities is the perceptual narrowing of face–voice matching, whereby young infants match faces and voices across species, but older infants do not. In the present study, we provide neurophysiological evidence for developmental decline in cross‐species face–voice matching. We measured event‐related brain potentials (ERPs) while 4‐ and 8‐month‐old infants watched and listened to congruent and incongruent audio‐visual presentations of monkey vocalizations and humans mimicking monkey vocalizations. The ERP results indicated that younger infants distinguished between the congruent and the incongruent faces and voices regardless of species, whereas in older infants, the sensitivity to multisensory congruency was limited to the human face and voice. Furthermore, with development, visual and frontal brain processes and their functional connectivity became more sensitive to the congruence of human faces and voices relative to monkey faces and voices. Our data show the neural correlates of perceptual narrowing in face–voice matching and support the notion that postnatal experience with species identity is associated with neural changes in multisensory processing ( Lewkowicz & Ghazanfar, 2009 ).     

Is anyone looking at me? Direct gaze detection in children with and without autism

Atypical processing of eye contact is one of the significant characteristics of individuals with autism, but the mechanism underlying atypical direct gaze processing is still unclear. This study used a visual search paradigm to examine whether the facial context would affect direct gaze detection in children with autism. Participants were asked to detect target gazes presented among distracters with different gaze directions. The target gazes were either direct gaze or averted gaze, which were either presented alone (Experiment 1) or within facial context (Experiment 2). As with the typically developing children, the children with autism, were faster and more efficient to detect direct gaze than averted gaze, whether or not the eyes were presented alone or within faces. In addition, face inversion distorted efficient direct gaze detection in typically developing children, but not in children with autism. These results suggest that children with autism use featural information to detect direct gaze, whereas typically developing children use configural information to detect direct gaze.     

Atypical updating of face representations with experience in children with autism

Face identity aftereffects are significantly diminished in children with autism relative to typical children, which may reflect reduced perceptual updating with experience. Here, we investigated whether this atypicality also extends to non‐face stimulus categories, which might signal a pervasive visual processing difference in individuals with autism. We used a figural aftereffect task to measure directly perceptual updating following exposure to distorted upright faces, inverted faces and cars, in typical children and children with autism. A size‐change between study and test stimuli limited the likelihood that any processing atypicalities reflected group differences in adaptation to low‐level features of the stimuli. Results indicated that, relative to typical children, figural aftereffects for upright faces, but not inverted faces or cars, were significantly attenuated in children with autism. Moreover, the group difference was amplified when we isolated the ‘face‐selective’ component of the aftereffect, by partialling out the mid‐level shape adaptation common to upright and inverted face stimuli. Notably, the aftereffects of typical children were disproportionately larger for upright faces than for inverted faces and cars, but the magnitude of aftereffects of autistic children was not similarly modulated according to stimulus category. These findings are inconsistent with a pervasive adaptive coding atypicality relative to typical children, and suggest that reduced perceptual updating may constitute a high‐level, and possibly face‐selective, visual processing difference in children with autism.     

The eyes or the mouth? Feature salience and unfamiliar face processing in Williams syndrome and autism

Using traditional face perception paradigms the current study explores unfamiliar face processing in two neurodevelopmental disorders. Previous research indicates that autism and Williams syndrome (WS) are both associated with atypical face processing strategies. The current research involves these groups in an exploration of feature salience for processing the eye and mouth regions of unfamiliar faces. The tasks specifically probe unfamiliar face matching by using (a) upper or lower face features, (b) the Thatcher illusion, and (c) featural and configural face modifications to the eye and mouth regions. Across tasks, individuals with WS mirror the typical pattern of performance, with greater accuracy for matching faces using the upper than using the lower features, susceptibility to the Thatcher illusion, and greater detection of eye than mouth modifications. Participants with autism show a generalized performance decrement alongside atypicalities, deficits for utilizing the eye region, and configural face cues to match unfamiliar faces. The results are discussed in terms of feature salience, structural encoding, and the phenotypes typically associated with these neurodevelopmental disorders.     

The eyes or the mouth? Feature salience and unfamiliar face processing in Williams syndrome and autism

Using traditional face perception paradigms the current study explores unfamiliar face processing in two neurodevelopmental disorders. Previous research indicates that autism and Williams syndrome (WS) are both associated with atypical face processing strategies. The current research involves these groups in an exploration of feature salience for processing the eye and mouth regions of unfamiliar faces. The tasks specifically probe unfamiliar face matching by using (a) upper or lower face features, (b) the Thatcher illusion, and (c) featural and configural face modifications to the eye and mouth regions. Across tasks, individuals with WS mirror the typical pattern of performance, with greater accuracy for matching faces using the upper than using the lower features, susceptibility to the Thatcher illusion, and greater detection of eye than mouth modifications. Participants with autism show a generalized performance decrement alongside atypicalities, deficits for utilizing the eye region, and configural face cues to match unfamiliar faces. The results are discussed in terms of feature salience, structural encoding, and the phenotypes typically associated with these neurodevelopmental disorders.     

The lasting effects of process‐specific versus stimulus‐specific learning during infancy

The capacity to tell the difference between two faces within an infrequently experienced face group (e.g. other species, other race) declines from 6 to 9 months of age unless infants learn to match these faces with individual‐level names. Similarly, the use of individual‐level labels can also facilitate differentiation of a group of non‐face objects (strollers). This early learning leads to increased neural specialization for previously unfamiliar face or object groups. The current investigation aimed to determine whether early conceptual learning between 6 and 9 months leads to sustained behavioral advantages and neural changes in these same children at 4–6 years of age. Results suggest that relative to a control group of children with no previous training and to children with infant category‐level naming experience, children with early individual‐level training exhibited faster response times to human faces. Further, individual‐level training with a face group – but not an object group – led to more adult‐like neural responses for human faces. These results suggest that early individual‐level learning results in long‐lasting process‐specific effects, which benefit categories that continue to be perceived and recognized at the individual level (e.g. human faces).     

Functional connectivity differences in autism during face and car recognition: underconnectivity and atypical age‐related changes

Face recognition abilities improve between adolescence and adulthood over typical development (TD), but plateau in autism, leading to increasing face recognition deficits in autism later in life. Developmental differences between autism and TD may reflect changes between neural systems involved in the development of face encoding and recognition. Here, we focused on whole‐brain connectivity with the fusiform face area (FFA), a well‐established face‐preferential brain region. Older children, adolescents, and adults with and without autism completed the Cambridge Face Memory Test, and a matched car memory test, during fMRI scanning. We then examined task‐based functional connectivity between the FFA and the rest of the brain, comparing autism and TD groups during encoding and recognition of face and car stimuli. The autism group exhibited underconnectivity, relative to the TD group, between the FFA and frontal and primary visual cortices, independent of age. Underconnectivity with the medial and rostral lateral prefrontal cortex was face‐specific during encoding and recognition, respectively. Conversely, underconnectivity with the L orbitofrontal cortex was evident for both face and car encoding. Atypical age‐related changes in connectivity emerged between the FFA and the R temporoparietal junction, and R dorsal striatum for face stimuli only. Similar differences in age‐related changes in autism emerged for FFA connectivity with the amygdala across both face and car recognition. Thus, underconnectivity and atypical development of functional connectivity may lead to a less optimal face‐processing network in the context of increasing general and social cognitive deficits in autism.     

Brain activation during upright and inverted encoding of own‐ and other‐age faces: ERP evidence for an own‐age bias

We investigated the neural processing underlying own‐age versus other‐age faces among 5‐year‐old children and adults, as well as the effect of orientation on face processing. Upright and inverted faces of 5‐year‐old children, adults, and elderly adults (> 75 years of age) were presented to participants while ERPs and eye tracking patterns were recorded concurrently. We found evidence for an own‐age bias in children, as well as for predicted delayed latencies and larger amplitudes for inverted faces, which replicates earlier findings. Finally, we extend recent reports about an expert‐sensitive component (P2) to other‐race faces to account for similar effects in regard to other‐age faces. We conclude that differences in neural activity are strongly related to the amount and quality of experience that participants have with faces of various ages. Effects of orientation are discussed in relation to the holistic hypothesis and recent data that compromise this view.     

Normal perception of Mooney faces in developmental prosopagnosia: Evidence from the N170 component and rapid neural adaptation

Individuals with developmental prosopagnosia (DP) have a severe difficulty recognizing the faces of known individuals in the absence of any history of neurological damage. These recognition problems may be linked to selective deficits in the holistic/configural processing of faces. We used two‐tone Mooney images to study the processing of faces versus non‐face objects in DP when it is based on holistic information (or the facial gestalt) in the absence of obvious local cues about facial features. A rapid adaptation procedure was employed for a group of 16 DPs. Naturalistic photographs of upright faces were preceded by upright or inverted Mooney faces or by Mooney houses. DPs showed face‐sensitive N170 components in response to Mooney faces versus houses, and N170 amplitude reductions for inverted as compared to upright Mooney faces. They also showed the typical pattern of N170 adaptation effects, with reduced N170 components when upright naturalistic test faces were preceded by upright Mooney faces, demonstrating that the perception of Mooney and naturalistic faces recruits shared neural populations. Our findings demonstrate that individuals with DP can utilize global information about face configurations for categorical discriminations between faces and non‐face objects, and suggest that face processing deficits emerge primarily at more fine‐grained higher level stages of face perception.     

人类面孔早期加工特异性神经机制

在面孔识别研究领域中,大量研究探讨人类对这一类刺激的加工是否具有与其他刺激不同的认知神经机制,即面孔的加工具有领域特异性还是过程特异性？由于各类研究使用的方法各不相同,导致对这一问题的回答尚缺乏一致性。本研究假设,如果面孔刺激具有特异性,无论在何种任务被试采用何种加工方式下,人类面孔N170反应在统计值上均显著高于其他类别的N170反应;相反,面孔与其他刺激在N170上则没有统计上的差异。研究将人类面孔、动物面孔、水果／蔬菜、房屋4类刺激呈现在不同任务设置下,测量人类面孔在不同任务中与各类刺激间的早期反应差异。当前研究结果发现,人类面孔在不同任务中始终保持着比其他刺激更为显著的ERPs（Event-Related Potentials,ERPs）反应优势,表现在额中部的早期正成分VPP和右侧颞枕部负成分N170对人类面孔反应幅度显著高于其他三类刺激的。人类面孔与其他刺激的ERP间差异反应模式在不同任务下相对稳定,并末发现动物面孔有类似效应。研究结果支持人类面孔加工的领域特异性说法。     

Resolving ambiguity: a psycholinguistic approach to understanding prosody processing in high-functioning autism

Individuals with autism exhibit significant impairments in prosody production, yet there is a paucity of research on prosody comprehension in this population. The current study adapted a psycholinguistic paradigm to examine whether individuals with autism are able to use prosody to resolve syntactically ambiguous sentences. Participants were 21 adolescents with high-functioning autism (HFA), and 22 typically developing controls matched on age, IQ, receptive language, and gender. The HFA group was significantly less likely to use prosody to disambiguate syntax, but scored comparably to controls when syntax alone or both prosody and syntax indicated the correct response. These findings indicate that adolescents with HFA have difficulty using prosody to disambiguate syntax in comparison to typically developing controls, even when matched on chronological age, IQ, and receptive language. The implications of these findings for how individuals with autism process language are discussed.     

Individual differences in holistic processing predict face recognition ability

Why do some people recognize faces easily and others frequently make mistakes in recognizing faces? Classic behavioral work has shown that faces are processed in a distinctive holistic manner that is unlike the processing of objects. In the study reported here, we investigated whether individual differences in holistic face processing have a significant influence on face recognition. We found that the magnitude of face-specific recognition accuracy correlated with the extent to which participants processed faces holistically, as indexed by the composite-face effect and the whole-part effect. This association is due to face-specific processing in particular, not to a more general aspect of cognitive processing, such as general intelligence or global attention. This finding provides constraints on computational models of face recognition and may elucidate mechanisms underlying cognitive disorders, such as prosopagnosia and autism, that are associated with deficits in face recognition.     

Visual adaptation of the perception of “life”: Animacy is a basic perceptual dimension of faces

One critical component of understanding another’s mind is the perception of “life” in a face. However, little is known about the cognitive and neural mechanisms underlying this perception of animacy. Here, using a visual adaptation paradigm, we ask whether face animacy is (1) a basic dimension of face perception and (2) supported by a common neural mechanism across distinct face categories defined by age and species. Observers rated the perceived animacy of adult human faces before and after adaptation to (1) adult faces, (2) child faces, and (3) dog faces. When testing the perception of animacy in human faces, we found significant adaptation to both adult and child faces, but not dog faces. We did, however, find significant adaptation when morphed dog images and dog adaptors were used. Thus, animacy perception in faces appears to be a basic dimension of face perception that is species specific but not constrained by age categories.