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.     

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.     

Early and persistent motor difficulties in infants at-risk of developing autism spectrum disorder: A prospective study

Analyses were conducted in order to investigate motor development in younger siblings of children diagnosed with autism spectrum disorder (ASD). Infants at familial risk and low risk of developing ASD were tested longitudinally between the ages of 7 and 36 months. Data were analysed from motor scales on the Mullen Scales of Early Learning and the Vineland Adaptive Behaviour Scales at each age point. Significantly lower motor scores in at-risk infants were evident from the age of 7 months compared to the low-risk group. Infants who were later diagnosed with ASD demonstrated significantly poorer Fine Motor skills at 36 months than at-risk infants without any developmental difficulties. In addition, Gross Motor scores were highly correlated across the two measures for low-risk infants and infants who later developed ASD. Early motor difficulties may be an early indicator of a number of neurodevelopmental disorders, including ASD.     

Associations between attentional biases to fearful faces and social-emotional development in infants with and without an older sibling with autism

During the first year of life, infants become increasingly attuned to facial emotion, with heightened sensitivity to faces conveying threat observed by age seven months as illustrated through attentional biases (e.g., slower shifting away from fearful faces). Individual differences in these cognitive attentional biases have been discussed in relation to broader social-emotional functioning, and the current study examines these associations in infants with an older sibling with autism spectrum disorder (ASD), a group with an elevated likelihood of a subsequent ASD diagnosis (ELA; n = 33), and a group of infants with no family history of ASD who are at low likelihood of ASD (LLA; n = 24). All infants completed a task measuring disengagement of attention from faces at 12 months (fearful, happy, neutral), and caregivers completed the Infant-Toddler Social and Emotional Assessment at 12, 18, and/or 24 months. For the full sample, greater fear bias in attention disengagement at 12 months related to more internalizing behaviors at 18 months, and this was driven by the LLA infants. When examining groups separately, findings revealed that LLA with a greater fear bias had more difficult behaviors at 12, 18, and 24 months; in contrast, ELA showed the opposite pattern, and this was most pronounced for ELA who later received an ASD diagnosis. These preliminary group-level findings suggest that heightened sensitivity to fearful faces might serve an adaptive function in children who later receive an ASD diagnosis, but in infants with no family history of ASD, increased biases might reflect a marker of social-emotional difficulties.     

Additive effects of social and non‐social attention during infancy relate to later autism spectrum disorder

Emerging findings from studies with infants at familial high risk for autism spectrum disorder (ASD), owing to an older sibling with a diagnosis, suggest that those who go on to develop ASD show early impairments in the processing of stimuli with both social and non‐social content. Although ASD is defined by social‐communication impairments and restricted and repetitive behaviours, the majority of cognitive theories of ASD posit a single underlying factor, which over development has secondary effects across domains. This is the first high‐risk study to statistically differentiate theoretical models of the development of ASD in high‐risk siblings using multiple risk factors. We examined the prediction of ASD outcome by attention to social and non‐social stimuli: gaze following and attentional disengagement assessed at 13 months in low‐risk controls and high‐risk ASD infants (who were subsequently diagnosed with ASD at 3 years). When included in the same regression model, these 13‐month measures independently predicted ASD outcome at 3 years of age. The data were best described by an additive model, suggesting that non‐social attention, disengagement, and social attention as evidenced by gaze following, have a cumulative impact on ASD risk. These data argue against cognitive theories of ASD which propose that a single underlying factor has cascading effects across early development leading to an ASD outcome, and support multiple impairment models of ASD that are more consistent with recent genetic and neurobiological evidence.     

Does culture shape face perception in autism? Cross‐cultural evidence of the own‐race advantage from the UK and Japan

Autism spectrum disorders (ASD) are associated with face perception atypicalities, and atypical experience with faces has been proposed as an underlying explanation. Studying the own‐race advantage (ORA) for face recognition can reveal the effect of experience on face perception in ASD, although the small number of studies in the area present mixed findings. This study probed the ORA in ASD by comparing two cultural groups simultaneously for the first time. Children with ASD in the UK (N = 16) and Japan (N = 26) were compared with age‐ and ability‐matched typically developing (TD) children in the UK (N = 16) and Japan (N = 26). Participants completed a two‐alternative forced‐choice task, whereby they had to recognize a just seen face from a foil which was manipulated in one of four ways (IC: identity change; EE: easy eyes; HE: hard eyes; HM: hard mouth). Face stimuli were Asian and Caucasian, and thus the same stimuli were own and other race depending on the cultural group. The ASD groups in the UK and Japan did not show impaired face recognition abilities, or impairments with recognizing faces depending on manipulations to the eye region, and importantly they showed an ORA. There was considerable heterogeneity in the presence of the ORA in ASD and TD and also across cultures. Children in Japan had higher accuracy than children in the UK, and TD children in Japan did not show an ORA. This cross‐cultural study challenges the view that atypical experiences with faces lead to a reduced/absent ORA in ASD.     

Unfamiliar face recognition in children with autistic spectrum disorders

We investigated unfamiliar face recognition in low‐functioning children with autistic spectrum disorders (ASD) using a ‘part‐of‐face’ method. This method has not previously been used for unfamiliar faces with this population. The ‘part‐of‐face’ procedure provides measures of both face recognition accuracy and of processing style. We compared the performance of the children with ASD with three control groups: children with developmental delay (DD), typically developing (TD) children matched for verbal cognitive ability and TD children matched for chronological age (CA). Compared to the DD group, the ASD group showed similar processing in recognition accuracy and processing style. Compared to the TD children, the ASD group did not show the same level of accuracy as controls of the same CA, instead showing similar performance to younger TD children. However, as both children with ASD and DD showed the same performance, no ASD‐specific deficit was found. Copyright © 2009 John Wiley & Sons, Ltd.     

Neonatal imitation predicts how infants engage with faces

In human infants, neonatal imitation and preferences for eyes are both associated with later social and communicative skills, yet the relationship between these abilities remains unexplored. Here we investigated whether neonatal imitation predicts facial viewing patterns in infant rhesus macaques. We first assessed infant macaques for lipsmacking (a core affiliative gesture) and tongue protrusion imitation in the first week of life. When infants were 10–28 days old, we presented them with an animated macaque avatar displaying a still face followed by lipsmacking or tongue protrusion movements. Using eye tracking technology, we found that macaque infants generally looked equally at the eyes and mouth during gesture presentation, but only lipsmacking‐imitators showed significantly more looking at the eyes of the neutral still face. These results suggest that neonatal imitation performance may be an early measure of social attention biases and might potentially facilitate the identification of infants at risk for atypical social development.     

Word comprehension mediates the link between gesture and word production: Examining language development in infant siblings of children with autism spectrum disorder

Children's gesture production precedes and predicts language development, but the pathways linking these domains are unclear. It is possible that gesture production assists in children's developing word comprehension, which in turn supports expressive vocabulary acquisition. The present study examines this mediation pathway in a population with variability in early communicative abilities—the younger siblings of children with autism spectrum disorder (ASD; high‐risk infants, HR). Participants included 92 HR infants and 28 infants at low risk (LR) for ASD. A primary caregiver completed the MacArthur‐Bates Communicative Development Inventory (Fenson, et al., 1993) at 12, 14, and 18 months, and HR infants received a diagnostic evaluation for ASD at 36 months. Word comprehension at 14 months mediated the relationship between 12‐month gesture and 18‐month word production in LR and HR infants (ab = 0.263; p < 0.01). For LR infants and HR infants with no diagnosis or language delay, gesture was strongly associated with word comprehension (as = 0.666; 0.646; 0.561; ps < 0.01). However, this relationship did not hold for infants later diagnosed with ASD (a = 0.073; p = 0.840). This finding adds to a growing literature suggesting that children with ASD learn language differently. Furthermore, this study provides an initial step toward testing the developmental pathways by which infants transition from early actions and gestures to expressive language.     

Social and attention‐to‐detail subclusters of autistic traits differentially predict looking at eyes and face identity recognition ability

This study distinguished between different subclusters of autistic traits in the general population and examined the relationships between these subclusters, looking at the eyes of faces, and the ability to recognize facial identity. Using the Autism Spectrum Quotient (AQ) measure in a university‐recruited sample, we separate the social aspects of autistic traits (i.e., those related to communication and social interaction; AQ‐Social) from the non‐social aspects, particularly attention‐to‐detail (AQ‐Attention). We provide the first evidence that these social and non‐social aspects are associated differentially with looking at eyes: While AQ‐Social showed the commonly assumed tendency towards reduced looking at eyes, AQ‐Attention was associated with increased looking at eyes. We also report that higher attention‐to‐detail (AQ‐Attention) was then indirectly related to improved face recognition, mediated by increased number of fixations to the eyes during face learning. Higher levels of socially relevant autistic traits (AQ‐Social) trended in the opposite direction towards being related to poorer face recognition (significantly so in females on the Cambridge Face Memory Test). There was no evidence of any mediated relationship between AQ‐Social and face recognition via reduced looking at the eyes. These different effects of AQ‐Attention and AQ‐Social suggest face‐processing studies in Autism Spectrum Disorder might similarly benefit from considering symptom subclusters. Additionally, concerning mechanisms of face recognition, our results support the view that more looking at eyes predicts better face memory.     

Exploring cortical activation and connectivity in infants with and without familial risk for autism during naturalistic social interactions: A preliminary study

Behavioral signs of Autism Spectrum Disorder (ASD) are typically observable by the second year of life and a reliable diagnosis of ASD is possible by 2 to 3 years of age. Studying infants with familial risk for ASD allows for the investigation of early signs of ASD risk within the first year. Brain abnormalities such as hyper-connectivity within the first year may precede the overt signs of ASD that emerge later in life. In this preliminary study, we use functional near-infrared spectroscopy (fNIRS), an infant-friendly neuroimaging tool that is relatively robust against motion artifacts, to examine functional activation and connectivity during naturalistic social interactions in 9 high-risk (HR; older sibling with ASD) and 6 low-risk (LR; no family history of ASD) infants from 6 to 9 months of age. We obtained two 30-second baseline periods and a 5-minute social interaction period. HR infants showed reduced right and left-hemispheric activation compared to LR infants based on oxy (HbO₂) and deoxy (HHb) signal trends. HR infants also had greater functional connectivity than LR infants during the pre- and post-social periods and showed a drop in connectivity during the social period. Our findings are consistent with previous work suggesting early differences in cortical activation associated with familial risk for ASD, and highlight the promise of fNIRS in evaluating potential markers of ASD risk during naturalistic social contexts.     

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).     

The neural correlates of processing newborn and adult faces in 3‐year‐old children

The current study examines the processing of upright and inverted faces in 3‐year‐old children (n = 35). Event‐related potentials (ERPs) were recorded during a passive looking paradigm including adult and newborn face stimuli. We observed three face‐sensitive components, the P1, the N170 and the P400. Inverted faces elicited shorter P1 latency and larger P400 amplitude. P1 and N170 amplitudes were larger for adult faces. To examine the role of experience in the development of face processing, the processing of adult and newborn faces was compared for children with a younger sibling (n = 23) and children without a younger sibling (n = 12). Age of sibling at test correlated negatively with P1 amplitude for adult and newborn faces. This may indicate more efficient processing of different face ages in children with a younger sibling and potentially reflects a more flexible face representation.     

Neural correlates of facial emotion processing in infancy

In the present study we examined the neural correlates of facial emotion processing in the first year of life using ERP measures and cortical source analysis. EEG data were collected cross‐sectionally from 5‐ (N = 49), 7‐ (N = 50), and 12‐month‐old (N = 51) infants while they were viewing images of angry, fearful, and happy faces. The N290 component was found to be larger in amplitude in response to fearful and happy than angry faces in all posterior clusters and showed largest response to fear than the other two emotions only over the right occipital area. The P400 and Nc components were found to be larger in amplitude in response to angry than happy and fearful faces over central and frontal scalp. Cortical source analysis of the N290 component revealed greater cortical activation in the right fusiform face area in response to fearful faces. This effect started to emerge at 5 months and became well established at 7 months, but it disappeared at 12 months. The P400 and Nc components were primarily localized to the PCC/Precuneus where heightened responses to angry faces were observed. The current results suggest the detection of a fearful face in infants’ brain can happen shortly (~200–290 ms) after the stimulus onset, and this process may rely on the face network and develop substantially between 5 to 7 months of age. The current findings also suggest the differential processing of angry faces occurred later in the P400/Nc time window, which recruits the PCC/Precuneus and is associated with the allocation of infants’ attention.     

Biracial and monoracial infant own‐race face perception: an eye tracking study

We know that early experience plays a crucial role in the development of face processing, but we know little about how infants learn to distinguish faces from different races, especially for non‐Caucasian populations. Moreover, it is unknown whether differential processing of different race faces observed in typically studied monoracial infants extends to biracial infants as well. Thus, we investigated 3‐month‐old Caucasian, Asian and biracial (Caucasian‐Asian) infants’ ability to distinguish Caucasian and Asian faces. Infants completed two within‐subject, infant‐controlled habituation sequences and test trials as an eye tracker recorded looking times and scanning patterns. Examination of individual differences revealed significant positive correlations between own‐race novelty preference and scanning frequency between eye and mouth regions of own‐race habituation stimuli for Caucasian and Asian infants, suggesting that facility in own‐race face discrimination stems from active inspection of internal facial features in these groups. Biracial infants, however, showed the opposite effect: An ‘own‐race’ novelty preference was associated with reduced scanning between eye and mouth regions of ‘own‐race’ habituation stimuli, suggesting that biracial infants use a distinct approach to processing frequently encountered faces. Future directions for investigating face processing development in biracial populations are discussed. A video abstract of this article can be viewed at http://youtu.be/a_dDXfFuEfY     

Impairments in monkey and human face recognition in 2-year-old toddlers with Autism Spectrum Disorder and Developmental Delay

Face recognition impairments are well documented in older children with Autism Spectrum Disorders (ASD); however, the developmental course of the deficit is not clear. This study investigates the progressive specialization of face recognition skills in children with and without ASD. Experiment 1 examines human and monkey face recognition in 2-year-old children with ASD, matched for nonverbal mental age (NVMA) with developmentally delayed (DD) children, and typically developing children (TD), using the Visual Paired Comparison (VPC) paradigm. Results indicate that, consistent with the other-species effect, TD controls show enhanced recognition of human but not monkey faces; however, neither the ASD nor the DD group show evidence of face recognition regardless of the species. Experiment 2 examines the same question in a group of older 3- to 4-year-old developmentally disabled (ASD and DD) children as well as in typical controls. In this experiment, both human and monkey faces are recognized by all three groups. The results of Experiments 1 and 2 suggest that difficulties in face processing, as measured by the VPC paradigm, are common in toddlers with ASD as well as DD, but that these deficits tend to disappear by early preschool age. In addition, the experiments show that higher efficacy of incidental encoding and recognition of facial identity in a context of passive exposure is positively related to nonverbal cognitive skills and age, but not to overall social interaction skills or greater attention to faces exhibited in naturalistic contexts.     

Fine motor skill predicts expressive language in infant siblings of children with autism

We investigated whether fine motor and expressive language skills are related in the later‐born siblings of children with autism (heightened‐risk, HR infants) who are at increased risk for language delays. We observed 34 HR infants longitudinally from 12 to 36 months. We used parent report and standardized observation measures to assess fine motor skill from 12 to 24 months in HR infants (Study 1) and its relation to later expressive vocabulary at 36 months in HR infants (Study 2). In Study 1, we also included 25 infants without a family history of autism to serve as a normative comparison group for a parent‐report fine motor measure. We found that HR infants exhibited fine motor delays between 12 and 24 months and expressive vocabulary delays at 36 months. Further, fine motor skill significantly predicted expressive language at 36 months. Fine motor and expressive language skills are related early in development in HR infants, who, as a group, exhibit risk for delays in both. Our findings highlight the importance of considering fine motor skill in children at risk for language impairments and may have implications for early identification of expressive language difficulties.     

Infant motor skill predicts later expressive language and autism spectrum disorder diagnosis

Motor difficulties may be an early Autism Spectrum Disorder (ASD) risk indicator and may predict subsequent expressive language skills. Further understanding of motor functioning in the first year of life in children with ASD is needed. We examined motor skills in 6-month-olds (n = 140) at high and low familial risk for ASD using the Peabody Developmental Motor Scales (Grasping, Visual-Motor Integration, and Stationary subscales). In Study 1, motor skill at 6 months predicted ASD status at 24–36 months; ASD was associated with poorer infant motor skills. In Study 2, motor skill at 6 months predicted expressive language at 30 and 36 months. Findings provide evidence that vulnerability in motor function early in development is present in ASD. Findings highlight the importance of developmental monitoring in high-risk infants and possible cascading effects of early disruption in motor development.     

See and be seen: Infant–caregiver social looking during locomotor free play

Face‐to‐face interaction between infants and their caregivers is a mainstay of developmental research. However, common laboratory paradigms for studying dyadic interaction oversimplify the act of looking at the partner's face by seating infants and caregivers face to face in stationary positions. In less constrained conditions when both partners are freely mobile, infants and caregivers must move their heads and bodies to look at each other. We hypothesized that face looking and mutual gaze for each member of the dyad would decrease with increased motor costs of looking. To test this hypothesis, 12‐month‐old crawling and walking infants and their parents wore head‐mounted eye trackers to record eye movements of each member of the dyad during locomotor free play in a large toy‐filled playroom. Findings revealed that increased motor costs decreased face looking and mutual gaze: Each partner looked less at the other's face when their own posture or the other's posture required more motor effort to gain visual access to the other's face. Caregivers mirrored infants' posture by spending more time down on the ground when infants were prone, perhaps to facilitate face looking. Infants looked more at toys than at their caregiver's face, but caregivers looked at their infant's face and at toys in equal amounts. Furthermore, infants looked less at toys and faces compared to studies that used stationary tasks, suggesting that the attentional demands differ in an unconstrained locomotor task. Taken together, findings indicate that ever‐changing motor constraints affect real‐life social looking.     

Visual configural processing in adults born at extremely low birth weight

Being born at extremely low birth weight (ELBW; ≤1,000 g) is associated with enduring visual impairments. We tested for long‐term, higher order visual processing problems in the oldest known prospectively followed cohort of ELBW survivors. Configural processing (spacing among features of an object) was examined in 62 adults born at ELBW (M_age = 31.9 years) and 82 adults born at normal birth weight (NBW; ≥2,500 g: M_age = 32.5 years). Pairs of human faces, monkey faces, or houses were presented in a delayed match‐to‐sample task, where non‐matching stimuli differed only in the spacing of their features. Discrimination accuracy for each stimulus type was compared between birth weight groups, adjusting for neurosensory impairment, visual acuity, binocular fusion ability, IQ, and sex. Both groups were better able to discriminate human faces than monkey faces (p < .001). However, the ELBW group discriminated between human faces (p < .001), between monkey faces (p < .001), and to some degree, between houses (p < .06), more poorly than NBW control participants, suggesting a general deficit in perceptual processing. Human face discrimination was related to performance IQ (PIQ) across groups, but especially among ELBW survivors. Coding (a PIQ subtest) also predicted human face discrimination in ELBW survivors, consistent with previously reported links between visuo‐perceptive difficulties and regional slowing of cortical activity in individuals born preterm. Correlations with Coding suggested ELBW survivors may have used a feature‐matching approach to processing human faces. Future studies could examine brain‐based anatomical and functional evidence for altered face processing, as well as the social and memory consequences of face‐processing deficits in ELBW survivors.