Reduced Alternating Gaze During Social Interaction in Infancy is Associated with Elevated Symptoms of Autism in Toddlerhood

In typical development, infants often alternate their gaze between their interaction partners and interesting stimuli, increasing the probability of joint attention toward surrounding objects and creating opportunities for communication and learning. Children with Autism Spectrum Disorder (ASD) have been found to engage less in behaviors that can initiate joint attention compared to typically developing children, but the role of such atypicalities in the development of ASD during infancy is not fully understood. Here, using eye tracking technology in a live setting, we show that 10-month-olds at high familial risk for ASD engage less in alternating gaze during interaction with an adult compared to low risk infants. These differences could not be explained by low general social preference or slow visual disengagement, as the groups performed similarly in these respects. We also found that less alternating gaze at 10 months was associated with more social ASD symptoms and less showing and pointing at 18 months. These relations were similar in both the high risk and the low risk groups, and remained when controlling for general social preference and disengagement latencies. This study shows that atypicalities in alternating gaze in infants at high risk for ASD emerge already during the first 10 months of life - a finding with theoretical as well as potential practical implications.     

自闭症谱系障碍个体的注意解离

注意解离是注意定向网络的重要组成部分, 指在注意转移过程中对原来刺激进行注意分离的过程。自闭症个体注意解离的早期受损会直接影响其它重要功能的发展, 尤其是唤醒调节和共同注意发展。采用间隙重叠范式的研究发现, 自闭症个体注意解离能力是否异常还存在争议, 被试年龄及取样、测量指标和刺激特征可能是影响的因素; 其神经机制可能涉及额叶、顶叶、小脑和胼胝体等脑区。未来应从脑机制研究入手, 综合考虑被试特征、研究方法和刺激特征对注意解离结果的影响, 明确其在自闭症早期预测和识别中的作用。     

The control of social attention from 1 to 4 months

The control of social attention during early infancy was investigated in two studies. In both studies, an adult turned towards one of two targets within the infant's immediate visual field. We tested: (a) whether infants were able to follow the direction of the adult's head turn; and (b) whether following a head turn was accompanied by further gaze shifts between experimenter and target. In the first study, 1‐month‐olds did not demonstrate attention following at the group level. In addition, those infants who turned towards the same target remained fixed on it and did not shift attention again. In Study 2, we tested infants longitudinally at 2–4 months. At the group level, infants followed the adult's head turn at 3 and 4 months but not at 2 months. Those infants who turned towards the same target at 3 and 4 months also shifted gaze back and forth between experimenter and target. By 3 months, infants seem able to capitalize on the social environment to disengage and distribute attention more flexibly. The results support the claim that the control of social attention begins in early infancy, and are consistent with the hypothesis that following the attention of other people is dependent on the development of disengagement skills.     

Initiation of joint attention and related visual attention processes in infants with autism spectrum disorder: Literature review

Autism spectrum disorder (ASD) represents a group of neurodevelopmental disabilities that can be difficult to identify before the age of 2 or 3 years, the age when the full range of behavioral symptoms has emerged in most cases. Initiation of joint attention is an important developmental function in which impairments are already observable before the second birthday and can predict children’s ASD symptomatology. In the first part of this review, we summarize results pertaining to retrospective studies of initiation of joint attention in children with ASD and prospective studies of infants at high risk for ASD during the first 2 years, when this behavior is becoming more complex in terms of frequency, quality, and variety. We will also discuss the implications of impairments in dyadic engagement, a precursor of joint attention behavior, for the early development of joint attention. Finally, the early development of initiation of joint attention has been related to specific visual attention mechanisms such as social orienting and visual disengagement. In the second part of this review, we provide an overview of the relationship between those visual attention mechanisms and subsequent social-communication impairments. Clinical and research implications of these findings for both early detection and early intervention will be discussed.     

婴幼儿面孔注意偏向：先天倾向与发展轨迹——来自正常和孤独症婴幼儿的证据

正常发展(Typically developing, TD)婴儿的先天面孔注意倾向稳定地存在于不同发展阶段不同刺激情景中, 且在生命第一年内呈现短暂下降后快速增强的发展趋势。TD婴幼儿的视觉注意在第4至6周之间发生由皮下控制向皮层控制的关键性转变之后, 伴随面孔视觉经验的不断积累, 逐渐形成的面孔特异性皮层网络对面孔的优先选择性反应逐渐增强。而孤独症谱系(Autism Spectrum Disorder, ASD)婴幼儿具备初始的面孔注意先天倾向, 但在面孔皮层发育关键期内逐渐偏离正常轨道, 在1岁左右表现出面孔注意障碍。该群体先天的感知注意损伤或社会动机缺失可能导致其在关键性转变期内的面孔视觉经验输入不足, 进而阻碍面孔特异性皮层网络的正常发展。未来研究可考虑采用生物遗传学方法和近红外脑成像技术探索新生儿面孔注意先天倾向的起源, 系统考察社会场景中感知觉特征和社会性特征对ASD高危婴儿面孔注意发展轨迹尤其是关键性转变期的影响作用。     

Visual disengagement in young infants in relation to age,sex, SES,developmental level and adaptive functioning

Visual attention plays a key role in infants’ interaction with the environment, and shapes their behavioral and brain development. As such, early problems with flexibly switching gaze from one stimulus to another (visual disengagement) have been hypothesized to lead to developmental difficulties (e.g. joint attention and social skills) over time. This study aimed to identify cross-sectional associations between performance in the Gap task (gaze shift latencies and visual attention disengagement) and measures of development and adaptive behavior in conjunction to any sex or socioeconomic status effects in infancy. We measured visual attention disengagement in 436 5-month-old infants and calculated its association with cognitive developmental level, adaptive behaviours, socioeconomic status (SES) and biological sex. In the Gap task, participants must redirect their gaze from a central stimulus to an appearing peripheral stimulus. The three experimental conditions of the task (Gap, Baseline and Overlap) differ on the timepoint when the central stimuli disappears in relation to the appearance of the peripheral stimulus: 200 ms before the peripheral stimulus appears (Gap), simultaneously to its appearance (Baseline), or with peripheral stimulus offset (Overlap). The data from the experimental conditions showed the expected pattern, with average latencies being the shortest in the Gap and longest in the Overlap condition. Females were faster (p = .004) than males in the Gap condition, which could indicate that arousal-related effects differ as a function of biological sex. Infants from higher SES were slower (p = .031) in the Overlap condition compared to lower SES infants. This suggests that basic visual attention may differ by socio-cultural background, and should be considered when studying visual attention and its developmental correlates. We observed no significant association to concurrent developmental level or adaptive function. Given its large sample size, this study provides a useful reference for future studies of visual disengagement in early infancy.     

Altered lateralization of dorsal language tracts in 6‐week‐old infants at risk for autism

Altered structural connectivity has been identified as a possible biomarker of autism spectrum disorder (ASD) risk in the developing brain. Core features of ASD include impaired social communication and early language delay. Thus, examining white matter tracts associated with language may lend further insight into early signs of ASD risk and the mechanisms that underlie language impairments associated with the disorder. Evidence of altered structural connectivity has previously been detected in 6‐month‐old infants at high familial risk for developing ASD. However, as language processing begins in utero, differences in structural connectivity between language regions may be present in the early infant brain shortly after birth. Here we investigated key white matter pathways of the dorsal language network in 6‐week‐old infants at high (HR) and low (LR) risk for ASD to identify atypicalities in structural connectivity that may predict altered developmental trajectories prior to overt language delays and the onset of ASD symptomatology. Compared to HR infants, LR infants showed higher fractional anisotropy (FA) in the left superior longitudinal fasciculus (SLF); in contrast, in the right SLF, HR infants showed higher FA than LR infants. Additionally, HR infants showed more rightward lateralization of the SLF. Across both groups, measures of FA and lateralization of these pathways at 6 weeks of age were related to later language development at 18 months of age as well as ASD symptomatology at 36 months of age. These findings indicate that early differences in the structure of language pathways may provide an early predictor of future language development and ASD risk.     

Can infants’ orientation to social stimuli predict later joint attention skills?

From the moment infants are born, they seem to prefer orienting to social stimuli, over objects and non‐social stimuli. This preference lasts throughout adulthood and is believed to play a crucial role in social‐communicative development. By following up a group of infants at the age of 6, 8, and 12 months, this study explored the role of social orienting in the early development of joint attention skills. The expected association between social orienting and joint attention was partially confirmed. Social orienting in real‐life photographs of everyday situations was not related to later joint attention skills, however fixation to the eyes in a neutral face was related to response to joint attention skills, and fixation to the eyes in a dynamic video clip of a talking person was predictive of initiating joint attention skills. Several alternative interpretations of the results are discussed.     

Face scanning distinguishes social from communication impairments in autism

How closely related are the social and communicative impairments in Autism Spectrum Disorder (ASD)? Recent findings in typically developing children suggest that both types of impairment are highly heritable but have only moderate behavioural and genetic overlap. So far, their respective roles in social perception are poorly understood. Here we show that when looking at other people’s faces, children with ASD who are better at socio‐emotional behaviours than non‐verbal communication look more at the eyes, while those with the opposite profile look more at the mouth (Study 1). For the mouth area, a similar pattern was observed for inverted faces, suggesting that information from this area is perceived on a featural basis. In Study 2, we found that when shown a person performing manual actions, ‘eye‐lookers’ from Study 1 tended to look most at the face of the actor, while ‘mouth‐lookers’ from Study 1 tended to look at the action itself (hand/objects). This result was found in both ASD and typical development. In Study 3, the main finding in Study 1 was replicated in a new sample. Taken together, we interpret these results as supporting the view that the neural systems underlying socio‐emotional versus non‐verbal communication skills are separable, a finding that has important theoretical and clinical implications. The results also suggest that a similar differentiation of looking behaviour may operate in normal development.     

Unimpaired attentional disengagement in toddlers with autism spectrum disorder

A prominent hypothesis holds that ‘sticky’ attention early in life in children with autism spectrum disorder (ASD) limits their ability to explore and learn about the world. Under this hypothesis, the core clinical symptoms of ASD – restricted interests, repetitive behaviors and impaired social/communication abilities – could all result from impaired attentional disengagement during development. However, the existence of disengagement deficits in children with ASD is controversial, and a recent study found no deficit in 5‐ to 12‐year‐olds with ASD. Nonetheless, the possibility remains that disengagement is impaired earlier in development in children with ASD, altering their developmental trajectory even if the attentional deficit itself is remediated or compensated for by the time children with ASD reach school age. Here, we tested this possibility by characterizing attentional disengagement in a group of toddlers just diagnosed with ASD (age 21 to 37 months). We found strikingly similar performance between the ASD and age‐matched typically developing (TD) toddlers, and no evidence of impaired attentional disengagement. These results show that even at a young age when the clinical symptoms of ASD are first emerging, disengagement abilities are intact. Sticky attention is not a fundamental characteristic of ASD, and probably does not play a causal role in its etiology.     

Imitation from 12 to 24 months in autism and typical development: a longitudinal Rasch analysis

The development of imitation during the second year of life plays an important role in domains of sociocognitive development such as language and social learning. Deficits in imitation ability in persons with autism spectrum disorder (ASD) from toddlerhood into adulthood have also been repeatedly documented, raising the possibility that early disruptions in imitation contribute to the onset of ASD and the deficits in language and social interaction that define the disorder. This study prospectively examined the development of imitation between 12 and 24 months of age in 154 infants at familial risk for ASD and 78 typically developing infants who were all later assessed at 36 months for ASD or other developmental delays. The study established a developmental measure of imitation ability and examined group differences over time, using an analytic Rasch measurement model. Results revealed a unidimensional latent construct of imitation and verified a reliable sequence of imitation skills that was invariant over time for all outcome groups. Results also showed that all groups displayed similar significant linear increases in imitation ability between 12 and 24 months and that these increases were related to individual growth in both expressive language and ratings of social engagement but not in fine motor development. The group of children who developed ASD by age 3 years exhibited delayed imitation development compared with the low-risk typical outcome group across all time-points, but were indistinguishable from other high-risk infants who showed other cognitive delays not related to ASD.     

Sluggish cognitive tempo in children and adolescents with higher functioning autism spectrum disorders: Social impairments and internalizing symptoms

Sluggish cognitive tempo (SCT) was introduced in 1980s in the field of attention deficit hyperactivity disorder (ADHD). Studies indicate that symptoms of SCT are separate from symptoms of ADHD and independently associated with multiple domains of functioning in clinical groups and in typical development. We assessed whether similar pattern would apply to higher functioning autism spectrum disorders (ASD). Children with higher functioning ASD (N = 55; 5?15 years) were divided into the ASD+High SCT (n = 17), the ASD+Medium SCT (n = 18) and the ASD+Low SCT (n = 20) groups based on parent‐rated daydreaming and slowness on the Five to Fifteen questionnaire (FTF). The groups were compared on SCT‐related impairments found in previous studies: social skills, academic functioning, psychiatric symptoms, and processing speed. Assessment methods were the FTF, the Development and Well‐Being Assessment, and the Coding subtest of the WISC‐III. The ADHD symptoms were statistically controlled due to the overlap between SCT and ADHD. The ASD+High SCT and ASD+Medium SCT groups were significantly more likely to have the most pronounced social impairments, and the ASD+High SCT group had significantly higher rate of internalizing disorders compared to the ASD+Low SCT group. Our results suggest that children with higher functioning ASD and high or medium levels of SCT symptoms could be at higher risk for psychosocial impairments than children with higher functioning ASD with low levels of SCT symptoms. Co‐occurring ADHD symptoms do not explain the finding. Recognizing SCT symptoms in higher functioning ASD would be important to targeting preventive support.     

Gaze aversion during social interaction in preterm infants: a function of attention skills?

Preterm infants avert their gaze more often and for longer periods in early social interactions compared to full term infants. In previous studies this finding is interpreted as being a function of the higher degree of parental stimulation that is often found in parents of preterm children. The current study explores an additional hypothesis. Since the development of general visual attention abilities is found to be less optimal in preterm children, it is possible that less optimal maturation of attention abilities partially explains the elevated gaze aversion in a social context. Therefore, the current study investigated the association between gaze aversion in a social context and the ability to disengage and shift visual attention in a non-social context in 20 preterm and 42 full term infants aged 4 and 6 months. Results confirm that preterm infants are slower to shift their attention in a non-social context and that they avert their gaze more often in a social context compared to full term children. Furthermore, more frequent gaze aversion during social interaction at 6 months was related to longer disengagement and the shifting of attention at 4 and 6 months, but only within the preterm group. The results suggest that attention maturation is less optimal in preterm children; this can be observed in a non-social as well as a social context. Less attention maturation in preterm children can negatively influence the amount of time they can stay actively involved in social interaction.     

Leveraging epigenetics to examine differences in developmental trajectories of social attention: A proof-of-principle study of DNA methylation in infants with older siblings with autism

Preliminary evidence suggests that changes in DNA methylation, a widely studied epigenetic mechanism, contribute to the etiology of Autism Spectrum Disorder (ASD). However, data is primarily derived from post-mortem brain samples or peripheral tissue from adults. Deep-phenotyped longitudinal infant cohorts are essential to understand how epigenetic modifications relate to early developmental trajectories and emergence of ASD symptoms. We present a proof-of-principle study designed to evaluate the potential of prospective epigenetic studies of infant siblings of children with ASD.Illumina genome-wide 450 K DNA methylation data from buccal swabs was generated for 63 male infants at multiple time-points from 8 months to 2 years of age (total N = 107 samples). 11 of those infants received a diagnosis of ASD at 3 years. We conducted a series of analyses to characterize DNA methylation signatures associated with categorical outcome and neurocognitive measures from parent-report questionnaire, eye-tracking and electro-encephalography.Effects observed across the entire genome (epigenome-wide association analyses) suggest that collecting DNA methylation samples within infant-sibling designs allows for the detection of meaningful signals with smaller sample sizes than previously estimated. Mapping networks of co-methylated probes associated with neural correlates of social attention implicated enrichment of pathways involved in brain development. Longitudinal modelling found covariation between phenotypic traits and DNA methylation levels in the proximity of genes previously associated with cognitive development, although larger samples and more complete datasets are needed to obtain generalizable results.In conclusion, assessment of DNA methylation profiles at multiple time-points in infant-sibling designs is a promising avenue to comprehend developmental origins and mechanisms of ASD.     

Enhanced gaze‐following behavior in Deaf infants of Deaf parents

Gaze following plays a role in parent–infant communication and is a key mechanism by which infants acquire information about the world from social input. Gaze following in Deaf infants has been understudied. Twelve Deaf infants of Deaf parents (DoD) who had native exposure to American Sign Language (ASL) were gender‐matched and age‐matched (±7 days) to 60 spoken‐language hearing control infants. Results showed that the DoD infants had significantly higher gaze‐following scores than the hearing infants. We hypothesize that in the absence of auditory input, and with support from ASL‐fluent Deaf parents, infants become attuned to visual‐communicative signals from other people, which engenders increased gaze following. These findings underscore the need to revise the ‘deficit model’ of deafness. Deaf infants immersed in natural sign language from birth are better at understanding the signals and identifying the referential meaning of adults’ gaze behavior compared to hearing infants not exposed to sign language. Broader implications for theories of social‐cognitive development are discussed. A video abstract of this article can be viewed at https://youtu.be/QXCDK_CUmAI     

What are you looking at? Infants’ neural processing of an adult's object‐directed eye gaze

Previous research suggests that by 4 months of age infants use the eye gaze of adults to guide their attention and facilitate processing of environmental information. Here we address the question of how infants process the relation between another person and an external object. We applied an ERP paradigm to investigate the neural processes underlying the perception of the direction of an adult's eye gaze in 4-month-old infants. Infants showed differential processing of an adult's eye gaze, which was directed at a simultaneously presented object compared to non-object-directed eye gaze. This distinction was evident in two ERP components: The Negative component, reflecting attentional processes, and the positive slow wave, which is involved in memory encoding. The implications of these findings for the development of joint attention and related social cognitive functions are discussed.     

Attachment security differs by later autism spectrum disorder: A prospective study

Although difficulties with social relationships are key to autism spectrum disorder (ASD), no previous study has examined infant attachment security prior to ASD diagnosis. We prospectively assessed attachment security at 15 months in high‐risk infants with later ASD (high‐risk/ASD, n = 16), high‐risk infants without later ASD (high‐risk/no‐ASD, n = 40), and low‐risk infants without later ASD (low‐risk/no‐ASD, n = 39) using the Strange Situation Procedure. High‐risk/ASD infants were disproportionately more likely to be classified as insecure (versus secure) and more likely to be classified as insecure‐resistant (versus secure or avoidant) than high‐risk/no‐ASD and low‐risk/no‐ASD infants. High‐risk infants with insecure‐resistant attachments were over nine times more likely to receive an ASD diagnosis than high‐risk infants with secure attachments. Insecure‐resistant attachment in high‐risk infants suggests a propensity toward negative affect with the parent in conditions of stress. Insecure‐resistant attachment may prove useful as a potential early index of propensity toward ASD diagnosis in high‐risk siblings, while insecure‐resistant attachment in the context of emergent autism may contribute to difficulties experienced by children with ASD and their families.     

A direct link between gaze perception and social attention

How information is exchanged between the cognitive mechanisms responsible for gaze perception and social attention is unclear. These systems could be independent; the "gaze cueing" effect could emerge from the activation of a general-purpose attentional mechanism that is ignorant of the social nature of the gaze cue. Alternatively, orienting to social gaze direction might be directly determined by the operation of cognitive mechanisms specifically dedicated to gaze perception. This second notion is the dominant assumption in the literature, but there is little direct support for this account. Here, we systematically manipulated observers' perception of gaze direction by implementing a gaze adaptation paradigm. Gaze cueing was reduced only in conditions where perception of specific averted gaze stimuli was impaired (Experiment 1). Adaptation to a pointing stimulus failed to impact gaze cueing (Experiment 2). Overall, these data suggest a direct link between the specific operation of gaze perception mechanisms and the consequential orienting of attention.     

The social foundation of executive function

In this study, we propose that infant social cognition may ‘bootstrap' the successive development of domain‐general cognition in line with the cultural intelligence hypothesis. Using a longitudinal design, 6‐month‐old infants (N = 118) were assessed on two basic social cognitive tasks targeting the abilities to share attention with others and understanding other peoples' actions. At 10 months, we measured the quality of the child's social learning environment, indexed by parent's abilities to provide scaffolding behaviors during a problem‐solving task. Eight months later, the children were followed up with a cognitive test‐battery, including tasks of inhibitory control and working memory. Our results showed that better infant social action understanding interacted with better parental scaffolding skills in predicting simple inhibitory control in toddlerhood. This suggests that infants' who are better at understanding other's actions are also better equipped to make the most of existing social learning opportunities, which in turn may benefit future non‐social cognitive outcomes.     

Attenuation of change blindness in children with autism spectrum disorders

Change blindness refers to the difficulty most people find in detecting a difference between two pictures when these are presented successively, with a brief interruption between. Attention at the site of the change is required for detection. A number of studies have investigated change blindness in adults and children with autism spectrum disorders (ASD). Some have produced evidence that people with ASD find changes to social stimuli harder to detect and changes to non‐social stimuli easier to detect, relative to comparison participants. However, other studies have produced entirely contradictory findings. There is a need for consistency in methodology to aid understanding of change blindness and attentional processes in ASD. Here, we replicate a change blindness study previously carried out with typically developing (TD) children and adults and with adults with ASD. Results reveal attenuated change blindness for non‐social stimuli in children with ASD relative to TD norms. Our results are interpreted, alongside others' findings, as potentially indicative of a complex relationship between different influences on attention over time.