Controlling attention to gaze and arrows in childhood: an fMRI study of typical development and Autism Spectrum Disorders

Functional magnetic resonance imaging was used to examine functional anatomy of attention to social (eye gaze) and nonsocial (arrow) communicative stimuli in late childhood and in a disorder defined by atypical processing of social stimuli, Autism Spectrum Disorders (ASD). Children responded to a target word ('LEFT'/'RIGHT') in the context of a distracting arrow or averted gaze pointing in a direction that was congruent, incongruent, or neutral (bar without arrowheads, central gaze) relative to the target word. Despite being irrelevant to the target task, both arrow and averted gaze facilitated responses (Congruent vs. Neutral trials) to the same extent in the two groups and led to interference (Incongruent vs. Congruent trials), which was greater from arrows in ASD than control children. In the brain, interaction between group and distracter-domain was observed in frontal-temporal regions during facilitation and frontal-striatal regions during interference. During facilitation, regions associated with attention to gaze in control children (left superior temporal sulcus, premotor) were associated with attention to arrows in ASD children; gaze was associated with medial temporal involvement in ASD children. During interference, regions associated with arrows in control children (anterior cingulate, right caudate) were activated in response to gaze in ASD children; further, left dorsolateral prefrontal cortex, a region not observed in control children, was activated during gaze-interference in ASD children. Thus, functional anatomy was atypical in ASD children during spontaneous processing of social and nonsocial communicative cues.     

A study of impaired judgment of eye-gaze direction and related face-processing deficits in autism spectrum disorders

The purpose of this study was to examine whether individuals with autism spectrum disorders (ASD) use the same cognitive strategies as typically developing individuals when processing eye-gaze direction. Subjects viewed pictures of whole faces, the eye region alone, and pairs of arrows presented for 40, 70, or 100 ms, and responded according to the direction the eyes were looking or the arrows pointing (left, right, or straight ahead). Experiment 1 demonstrated that typically developing adults (n = 41) were more accurate and showed shorter reaction times when judging direction of averted eye gaze in the context of the whole face than when only the eyes were visible (eye-region-alone condition). Furthermore, in the eye-region-alone condition participants were more accurate and faster at judging direct eye gaze than averted eye gaze. The same task was used in experiment 2 to compare the performance of a group of individuals with ASD (n = 24) with that of a group of IQ-matched typically developing individuals (n = 26). The performance of the control participants was identical to that observed in experiment 1. Individuals with ASD were able to judge eye-gaze direction accurately at short exposure duration; however, they failed to show the typical advantage for judging averted gaze in whole faces and the increased sensitivity to direct gaze in the eye-region-alone condition. The findings are discussed in terms of impairments to discrete gaze-processing and face-processing mechanisms, and the connectivity between these mechanisms.     

自闭症谱系障碍儿童在多重线索下习得词语的眼动研究

本文利用眼动追踪技术在基线、一致和矛盾3种实验条件下考察感知觉线索和社会性线索在自闭症谱系障碍儿童词语习得中的相对作用。行为数据结果表明, 此类儿童在矛盾条件下选择枯燥物体作为新异词语的所指对象, 这说明社会性线索较之于感知觉线索具有优势作用; 而他们在基线和一致条件下选择有趣物体作为新异词语的所指对象, 且一致条件的词语习得成绩优于基线条件, 这说明社会性线索较之于感知觉线索具有促进作用。眼动数据结果表明, 此类儿童在脸部注视模式和视线追随行为上与普通儿童存在差异。这说明, 虽然社会性线索在此类儿童与普通儿童的词语习得中具有相同的相对作用, 但他们获取社会性信息的方式与普通儿童存在差异。     

Perceiving gaze from head and eye rotations: An integrative challenge for children and adults

Gaze is an emergent visual feature. A person's gaze direction is perceived not just based on the rotation of their eyes, but also their head. At least among adults, this integrative process appears to be flexible such that one feature can be weighted more heavily than the other depending on the circumstances. Yet it is unclear how this weighting might vary across individuals or across development. When children engage emergent gaze, do they prioritize cues from the head and eyes similarly to adults? Is the perception of gaze among individuals with autism spectrum disorder (ASD) emergent, or is it reliant on a single feature? Sixty adults (M = 29.86 years‐of‐age), thirty‐seven typically developing children and adolescents (M = 9.3 years‐of‐age; range = 7–15), and eighteen children with ASD (M = 9.72 years‐of‐age; range = 7–15) viewed faces with leftward, rightward, or direct head rotations in conjunction with leftward or rightward pupil rotations, and then indicated whether the face was looking leftward or rightward. All individuals, across development and ASD status, used head rotation to infer gaze direction, albeit with some individual differences. However, the use of pupil rotation was heavily dependent on age. Finally, children with ASD used pupil rotation significantly less than typically developing (TD) children when inferring gaze direction, even after accounting for age. Our approach provides a novel framework for understanding individual and group differences in gaze as it is actually perceived—as an emergent feature. Furthermore, this study begins to address an important gap in ASD literature, taking the first look at emergent gaze perception in this population.     

Facial expression coding in children and adolescents with autism: Reduced adaptability but intact norm-based coding

Individuals with autism spectrum disorder (ASD) can have difficulty recognizing emotional expressions. Here, we asked whether the underlying perceptual coding of expression is disrupted. Typical individuals code expression relative to a perceptual (average) norm that is continuously updated by experience. This adaptability of face-coding mechanisms has been linked to performance on various face tasks. We used an adaptation aftereffect paradigm to characterize expression coding in children and adolescents with autism. We asked whether face expression coding is less adaptable in autism and whether there is any fundamental disruption of norm-based coding. If expression coding is norm-based, then the face aftereffects should increase with adaptor expression strength (distance from the average expression). We observed this pattern in both autistic and typically developing participants, suggesting that norm-based coding is fundamentally intact in autism. Critically, however, expression aftereffects were reduced in the autism group, indicating that expression-coding mechanisms are less readily tuned by experience. Reduced adaptability has also been reported for coding of face identity and gaze direction. Thus, there appears to be a pervasive lack of adaptability in face-coding mechanisms in autism, which could contribute to face processing and broader social difficulties in the disorder.     

自闭症谱系障碍儿童对面孔加工的同龄偏向效应

采用视觉追踪技术,探讨自闭症谱系障碍(autism spectrum disorders, ASD)儿童面孔加工的同龄偏向效应。实验1选取19名ASD儿童和23名生理年龄匹配的普通儿童(typically developing, TD)为被试,通过自由观看同龄和异龄中性面孔,探讨ASD儿童是否存在面孔加工的同龄偏向效应;实验2选取22名ASD儿童和生理年龄匹配的25名TD儿童,通过自由观看快乐、愤怒和恐惧面孔,探讨情绪对ASD儿童面孔加工同龄偏向的影响。结果发现,(1)ASD儿童对同龄中性面孔的注视时间显著大于异龄中性面孔;(2)ASD儿童在愤怒和恐惧情绪下对同龄面孔的注视时间显著大于异龄面孔,而在快乐情绪下同龄和异龄的注视时间则无显著差异。这表明ASD儿童对面孔的注视加工存在同龄偏向效应,且受情绪的影响。     

孤独症儿童的情绪共情能力及情绪表情注意方式

研究探讨了孤独症儿童的情绪共情能力及情绪表情注意方式的特点。各选取15名孤独症儿童以及作为对照组的智力障碍儿童和普通儿童各15名, 完成情绪共情实验, 同时使用生物反馈仪记录自主生理反应, 眼动仪记录眼动轨迹。结果发现孤独症儿童对情绪表情的自动模仿及感知能力显著低于智力障碍儿童与普通儿童; 对面孔的总注视时间、总注视点数均显著少于智力障碍儿童、普通儿童; 对眼部、嘴部的注视时间比及注视点数比均显著低于普通儿童; 对高兴和悲伤表情的注意较多而对恐惧则较少。这提示孤独症儿童的情绪共情能力不足、对情绪表情的注意方式异常。     

Does perceived direct gaze boost detection in adults and children with and without autism? The stare-in-the-crowd effect revisited

This study extended that of von Grünau and Anston (1995) and explored whether perceived direct gaze is easily detected by individuals with and without autism, utilizing a visual-search paradigm. Participants detected target faces with either direct gaze or averted gaze. Laterally averted faces were used to eliminate the involvement of lower perceptual characteristics such as symmetry, which were inherent with the “straight gaze” used by von Grünau and Anston. Both typically developed adults and children detected targets with direct gaze more quickly than those with averted gaze, but face inversion distorted this asymmetrical performance, suggesting the contribution of configurative facial processing. In contrast, children with autism were not affected by the gaze direction presented by realistic facial stimuli. They were, however, faster to detect straight gaze defined solely by local features, which suggests that their impairment might be specific to the detection of direct gaze presented within a facial context.     

The eye gaze direction of an observed person can bias perception,memory, and attention in adolescents with and without autism spectrum disorder

The reported experiments aimed to investigate whether a person and his or her gaze direction presented in the context of a naturalistic scene cause perception, memory, and attention to be biased in typically developing adolescents and high-functioning adolescents with autism spectrum disorder (ASD). A novel computerized image manipulation program presented a series of photographic scenes, each containing a person. The program enabled participants to laterally maneuver the scenes behind a static window, the borders of which partially occluded the scenes. The gaze direction of the person in the scenes spontaneously cued attention of both groups in the direction of gaze, affecting judgments of preference (Experiment 1a) and causing memory biases (Experiment 1b). Experiment 2 showed that the gaze direction of a person cues visual search accurately to the exact location of gaze in both groups. These findings suggest that biases in preference, memory, and attention are caused by another person’s gaze direction when viewed in a complex scene in adolescents with and without ASD     

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.     

Links between social and linguistic processing of speech in preschool children with autism: behavioral and electrophysiological measures

Data on typically developing children suggest a link between social interaction and language learning, a finding of interest both to theories of language and theories of autism. In this study, we examined social and linguistic processing of speech in preschool children with autism spectrum disorder (ASD) and typically developing chronologically matched (TDCA) and mental age matched (TDMA) children. The social measure was an auditory preference test that pitted 'motherese' speech samples against non-speech analogs of the same signals. The linguistic measure was phonetic discrimination assessed with mismatch negativity (MMN), an event-related potential (ERP). As a group, children with ASD differed from controls by: (a) demonstrating a preference for the non-speech analog signals, and (b) failing to show a significant MMN in response to a syllable change. When ASD children were divided into subgroups based on auditory preference, and the ERP data reanalyzed, ASD children who preferred non-speech still failed to show an MMN, whereas ASD children who preferred motherese did not differ from the controls. The data support the hypothesis of an association between social and linguistic processing in children with ASD.     

Learning new faces in typically developing children and children on the autistic spectrum

As faces become familiar, recognition becomes easier but the style of processing also changes. Here, twenty-one typically developing (TD) children and twenty-one children with autism spectrum disorder (ASD) were familiarised with 6 identities over 3 days. Next, they completed a 4-alternative forced-choice matching test in which targets were the 6 familiarised faces and 6 unfamiliar faces. The TD group showed a significant advantage for familiarised faces when matching whole faces and both internal and external facial regions. The ASD group showed similar familiarisation effects for whole and external faces, but not for internal regions. The ASD group was also impaired at matching eyes and mouths of familiarised faces. Results suggest the process of acquiring familiarity with faces differs from ASD and TD children.     

Intact and impaired mechanisms of action understanding in autism

Typically developing children understand and predict others' behavior by extracting and processing relevant information such as the logic of their actions within the situational constraints and the intentions conveyed by their gaze direction and emotional expressions. Children with autism have difficulties understanding and predicting others' actions. With the use of eye tracking and behavioral measures, we investigated action understanding mechanisms used by 18 children with autism and a well-matched group of 18 typically developing children. Results showed that children with autism (a) consider situational constraints in order to understand the logic of an agent's action and (b) show typical usage of the agent's emotional expressions to infer his or her intentions. We found (c) subtle atypicalities in the way children with autism respond to an agent's direct gaze and (d) marked impairments in their ability to attend to and interpret referential cues such as a head turn for understanding an agent's intentions.     

双通路理论视角下孤独症谱系障碍者的视线加工障碍

临床行为观察发现, 孤独症谱系障碍个体普遍存在不能与他人建立视线接触, 不能追随他人视线看向目标物体等视线加工(gaze processing)障碍。然而已有实验研究发现该群体在实验情境中普遍存在视线接触(eye contact)异常, 但其视线追随行为(gaze following)则存在正常与异常并存的现象。基于视线加工双通路理论的启示, 该障碍可能是由于视线加工皮下通路先天功能异常而皮层通路后天发展异常所致。然而, 该理论尚缺乏皮下通路先天功能异常是视线接触障碍潜在神经机制的直接证据, 还需进一步考察皮下通路先天功能异常对视线追随障碍的影响作用, 以及皮层通路后天发展异常即其补偿机制的神经回路及早期形成过程。     

Patterns of language and discourse comprehension skills in school‐aged children with autism spectrum disorders

Åsberg, J. (2010). Patterns of language and discourse comprehension skills in school‐aged children with autism spectrum disorders. Scandinavian Journal of Psychology 51, 534–539. The present study examined patterns of language and discourse comprehension skills in Swedish school‐aged children with autism spectrum disorders (ASD) (n = 16) as compared to a slightly younger group of typically developing children (n = 16) matched for non‐verbal cognitive ability. Results suggested significantly lower abilities in narrative discourse comprehension for the ASD group, but not in oral receptive vocabulary or reception of grammar. This difficulty with discourse‐level comprehension appeared to be of a general nature, as no evidence was found for the hypothesis that participants with ASD would find comprehension of inferential discourse information disproportionally more difficult than stated information, or for the hypothesis that discourse processing in ASD would be characterized by an elevated processing of explicitly stated narrative details. The study has clinical and educational implications, as the findings suggest that children with ASD would benefit from being offered specific support for discourse‐level comprehension.     

Young children with autism show atypical brain responses to fearful versus neutral facial expressions of emotion

Evidence suggests that autism is associated with impaired emotion perception, but it is unknown how early such impairments are evident. Furthermore, most studies that have assessed emotion perception in children with autism have required verbal responses, making results difficult to interpret. This study utilized high-density event-related potentials (ERPs) to investigate whether 3-4-year-old children with autism spectrum disorder (ASD) show differential brain activity to fear versus neutral facial expressions. It has been shown that normal infants as young as 7 months of age show differential brain responses to faces expressing different emotions. ERPs were recorded while children passively viewed photos of an unfamiliar woman posing a neutral and a prototypic fear expression. The sample consisted of 29 3-4-year-old children with ASD and 22 chronological age-matched children with typical development. Typically developing children exhibited a larger early negative component (N300) to the fear than to the neutral face. In contrast, children with ASD did not show the difference in amplitude of this early ERP component to the fear versus neutral face. For a later component, typically developing children exhibited a larger negative slow wave (NSW) to the fear than to the neutral face, whereas children with autism did not show a differential NSW to the two stimuli. In children with ASD, faster speed of early processing (i. e. N300 latency) of the fear face was associated with better performance on tasks assessing social attention (social orienting, joint attention and attention to distress). These data suggest that children with ASD, as young as 3 years of age, show a disordered pattern of neural responses to emotional stimuli.     

场景的年龄特征会影响自闭症谱系障碍儿童的注视模式

为了探讨场景年龄特征对ASD儿童场景注视模式的影响,选取14名自闭症谱系障碍（ASD）儿童和19名与其智力年龄匹配的正常发育（TD）儿童为被试,在被试对儿童场景和成人场景图片进行自由观看的同时记录其眼动。结果发现,ASD儿童对全图、面部、眼部和嘴部的访问均显著少于TD儿童,对背景区域的访问显著大于TD儿童;ASD和TD儿童对面部和身体的访问时间比都显著大于前景与背景兴趣区;ASD儿童对儿童场景中面部、眼部和嘴部兴趣区的访问时间比大于成人场景,而TD儿童则相反;两组儿童都表现出对儿童场景中背景的偏好。结果表明,在场景注视中,ASD与TD儿童具有相似的社会性注意倾向,对社会性信息给予更多注视,但ASD儿童表现更弱;场景的年龄特征会影响ASD儿童与TD儿童的场景注视模式,相对于成人场景,ASD儿童更偏向于注视儿童场景中的面孔和背景。     

Out of mind,out of sight? Investigating abnormal face scanning in autism spectrum disorder using gaze‐contingent paradigm

Diminished social motivation is hypothesized to explain abnormal face scanning pattern in individuals with autism spectrum disorder (ASD), especially reduced eye‐looking time in ASDs than typically developing (TD) people. Here, we tested an alternative explanation that children with ASD may use a compensatory strategy to avoid direct eye contact by processing the eyes through peripheral vision. We compared the face scanning patterns of children with and without ASD in two conditions: in the clear condition, the face was completely visible; in the blur condition, by using the gaze‐contingent paradigm, the whole face was blurred except for a small region being fixated at, thus children could not rely on the peripheral information to process the eyes. We found that children with ASD fixated less on the eyes than TD children in both conditions. Temporal‐course analyses further revealed the possible motivation‐based guidance of attention to process the eyes in the TD group but not in the ASD group. Additionally, we found that children with ASD scanned faces more randomly and less strategically than TD children. These results have ruled out the alternative hypothesis that the abnormal face scanning pattern in ASDs was due to their compensatory strategy to process eyes through peripheral vision, furthering our understanding of the mechanisms underlying their abnormal face scanning.     

Neural bases of Theory of Mind in children with autism spectrum disorders and children with conduct problems and callous‐unemotional traits

Individuals with autism spectrum disorders (ASD) have difficulty understanding other minds (Theory of Mind; ToM), with atypical processing evident at both behavioural and neural levels. Individuals with conduct problems and high levels of callous‐unemotional (CU) traits (CP/HCU) exhibit reduced responsiveness to others' emotions and difficulties interacting with others, but nonetheless perform normally in experimental tests of ToM. The present study aimed to examine the neural underpinnings of ToM in children (aged 10–16) with ASD (N = 16), CP/HCU (N = 16) and typically developing (TD) controls (N = 16) using a non‐verbal cartoon vignette task. Whilst individuals with ASD were predicted to show reduced fMRI responses across regions involved in ToM processing, CP/HCU individuals were predicted to show no differences compared with TD controls. The analyses indicated that neural responses did not differ between TD and CP/HCU groups during ToM. TD and CP/HCU children exhibited significantly greater medial prefrontal cortex responses during ToM than did the ASD group. Within the ASD group, responses in medial prefrontal cortex and right temporoparietal junction (TPJ) correlated with symptom severity as measured by the Autism Diagnostic Observation Schedule (ADOS). Findings suggest that although both ASD and CP/HCU are characterized by social difficulties, only children with ASD display atypical neural processing associated with ToM.     

Comparing Attention to Socially-Relevant Stimuli in Autism Spectrum Disorder and Developmental Coordination Disorder

Difficulties with social interaction have been reported in both children with an autism spectrum disorder (ASD) and children with developmental coordination disorder (DCD), although these disorders have very different diagnostic characteristics. To date, assessment of social skills in a DCD population has been limited to paper-based assessment or parent report. The present study employed eye tracking methodology to examine how children attend to socially-relevant stimuli, comparing 28 children with DCD, 28 children with ASD and 26 typically-developing (TD) age-matched controls (aged 7–10). Eye movements were recorded while children viewed 30 images, half of which were classed as ‘Individual’ (one person in the scene, direct gaze) and the other half were ‘Social’ (more naturalistic scenes showing an interaction). Children with ASD spent significantly less time looking at the face/eye regions in the images than TD children, but children with DCD performed between the ASD and TD groups in this respect. Children with DCD demonstrated a reduced tendency to follow gaze, in comparison to the ASD group. Our findings confirm that social atypicalities are present in both ASD and to a lesser extent DCD, but follow a different pattern. Future research would benefit from considering the developmental nature of the observed findings and their implications for support.