The breakdown of social looking.

Individual differences in social looking are commonly believed to reflect one single heritable dimension tightly linked to autism. Yet, recent data suggest that in human infants, looking to eyes (rather than mouth) and preference for faces (versus non-social objects) reflect distinct genetic influences, and neither appear to have a clear-cut relation to autism.

Sustained looking at faces at 5 months of age is associated with socio-communicative skills in the second year of life.

Efficiently processing information from faces in infancy is foundational for nonverbal communication. We studied individual differences in 5-month-old infants' (N = 517) sustained attention to faces and preference for emotional faces. We assessed the contribution of genetic and environmental influences to individual differences in these gaze behaviors, and the association between these traits and other concurrent and later phenotypes. We found an association between the mean duration of looking at a face (before looking away from it) at 5 months and socio-communicative abilities at 14 months (ß = 0.17, 95% CI: 0.08; 0.26, p < 0.001). Sustained attention to faces predicted socio-communicative abilities over and above variance captured by mean fixation duration. We also found a statistically significant but weak tendency to prefer looking at smiling faces (relative to neutral faces), but no indication that variability in this behavior was explained by genetic effects. Moderate heritability was found for sustained attention to faces (A = 0.23, CI: 0.06; 0.38), while shared environmental influences were non-significant for both phenotypes. These findings suggest that sustained looking at individual faces before looking away is a developmentally significant 'social attention' phenotype in infancy, characterized by moderate heritability and a specific relation to later socio-communicative abilities.

Genetic and environmental contributions to gaze lateralization across social and non-social stimuli in human infants.

A tendency to look at the left side of faces from the observer's point of view has been found in older children and adults, but it is not known when this face-specific left gaze bias develops and what factors may influence individual differences in gaze lateralization. Therefore, the aims of this study were to estimate gaze lateralization during face observation and to more broadly estimate lateralization tendencies across a wider set of social and non-social stimuli, in early infancy. In addition, we aimed to estimate the influence of genetic and environmental factors on lateralization of gaze. We studied gaze lateralization in 592 5-month-old twins (282 females, 330 monozygotic twins) by recording their gaze while viewing faces and two other types of stimuli that consisted of either collections of dots (non-social stimuli) or faces interspersed with objects (mixed stimuli). A right gaze bias was found when viewing faces, and this measure was moderately heritable (A = 0.38, 95% CI 0.24; 0.50). A left gaze bias was observed in the non-social condition, while a right gaze bias was found in the mixed condition, suggesting that there is no general left gaze bias at this age. Genetic influence on individual differences in gaze lateralization was only found for the tendency to look at the right versus left side of faces, suggesting genetic specificity of lateralized gaze when viewing faces.

A field test of computer-vision-based gaze estimation in psychology.

Computer-vision-based gaze estimation refers to techniques that estimate gaze direction directly from video recordings of the eyes or face without the need for an eye tracker. Although many such methods exist, their validation is often found in the technical literature (e.g., computer science conference papers). We aimed to (1) identify which computer-vision-based gaze estimation methods are usable by the average researcher in fields such as psychology or education, and (2) evaluate these methods. We searched for methods that do not require calibration and have clear documentation. Two toolkits, OpenFace and OpenGaze, were found to fulfill these criteria. First, we present an experiment where adult participants fixated on nine stimulus points on a computer screen. We filmed their face with a camera and processed the recorded videos with OpenFace and OpenGaze. We conclude that OpenGaze is accurate and precise enough to be used in screen-based experiments with stimuli separated by at least 11 degrees of gaze angle. OpenFace was not sufficiently accurate for such situations but can potentially be used in sparser environments. We then examined whether OpenFace could be used with horizontally separated stimuli in a sparse environment with infant participants. We compared dwell measures based on OpenFace estimates to the same measures based on manual coding. We conclude that OpenFace gaze estimates may potentially be used with measures such as relative total dwell time to sparse, horizontally separated areas of interest, but should not be used to draw conclusions about measures such as dwell duration.

Infants' looking preferences for social versus non-social objects reflect genetic variation.

To what extent do individual differences in infants' early preference for faces versus non-facial objects reflect genetic and environmental factors? Here in a sample of 536 5-month-old same-sex twins, we assessed attention to faces using eye tracking in two ways: initial orienting to faces at the start of the trial (thought to reflect subcortical processing) and sustained face preference throughout the trial (thought to reflect emerging attention control). Twin model fitting suggested an influence of genetic and unique environmental effects, but there was no evidence for an effect of shared environment. The heritability of face orienting and preference were 0.19 (95% confidence interval (CI) 0.04 to 0.33) and 0.46 (95% CI 0.33 to 0.57), respectively. Face preference was associated positively with later parent-reported verbal competence (ß = 0.14, 95% CI 0.03 to 0.25, P = 0.014, R2 = 0.018, N = 420). This study suggests that individual differences in young infants' selection of perceptual input-social versus non-social-are heritable, providing a developmental perspective on gene-environment interplay occurring at the level of eye movements.

Manipulation of phasic arousal by auditory cues is associated with subsequent changes in visual orienting to faces in infancy.

This eye-tracking study investigated the effect of sound-induced arousal on social orienting under different auditory cue conditions in 5-month-old (n = 25; n = 13 males) and 10-month-old infants (n = 21; n = 14 males) participating in a spontaneous visual search task. Results showed: (1) larger pupil dilation discriminating between high and low volume (b = 0.02, p = 0.007), but not between social and non-social sounds (b = 0.004, p = 0.64); (2) faster visual orienting (b = - 0.09, p < 0.001) and better social orienting at older age (b = 0.94, p < 0.001); (3) a fast habituation effect on social orienting after high-volume sounds (χ2(2) = 7.39, p = 0.025); (4) a quadratic association between baseline pupil size and target selection (b = - 1.0, SE = 0.5, χ2(1) = 4.04, p = 0.045); (5) a positive linear association between pupil dilation and social orienting (b = 0.09, p = 0.039). Findings support adaptive gain theories of arousal, extending the link between phasic pupil dilation and task performance to spontaneous social orienting in infancy.

Remote, tablet-based assessment of gaze following: a nationwide infant twin study.

Introduction: Much of our understanding of infant psychological development relies on an in-person, laboratory-based assessment. This limits research generalizability, scalability, and equity in access. One solution is the development of new, remotely deployed assessment tools that do not require real-time experimenter supervision. Methods: The current nationwide (Sweden) infant twin study assessed participants remotely via their caregiver's tablets (N = 104, ages 3 to 17 months). To anchor our findings in previous research, we used a gaze-following task where experimental and age effects are well established. Results: Closely mimicking results from conventional eye tracking, we found that a full head movement elicited more gaze following than isolated eye movements. Furthermore, predictably, we found that older infants followed gaze more frequently than younger infants. Finally, while we found no indication of genetic contributions to gaze-following accuracy, the latency to disengage from the gaze cue and orient toward a target was significantly more similar in monozygotic twins than in dizygotic twins, an indicative of heritability. Discussion: Together, these results highlight the potential of remote assessment of infants' psychological development, which can improve generalizability, inclusion, and scalability in developmental research.

Infant responses to direct gaze and associations to autism: A live eye-tracking study.

LAY ABSTRACT: When other people look directly towards us, we often respond by looking back at them, and such direct-gaze responses are important for establishing eye contact. Atypical eye contact is common in autism, but how and when this aspect of autism develops is not well understood. Here, we studied whether how much and how quickly infants respond to others' direct gaze is associated with autism in toddlerhood. We did this by measuring direct-gaze responses in a playful social interaction using live eye tracking. The study included 169 infants, of whom 129 had an elevated likelihood of developing autism due to having a first-degree family member with the condition, and 40 with typical likelihood of autism. In the elevated likelihood group, 35 were diagnosed with autism spectrum disorder at 3 years of age, and 94 were not. The results showed that infants in all three groups tended to increase their looking towards the adult's face after the adult looked directly at them. However, neither how much nor how quickly the infants responded to direct gaze by looking back at the adult reliably differentiated the infants with or without subsequent autism. While infants in the elevated likelihood of autism and subsequent diagnosis group tended to look away quicker from faces with direct gaze than infants in the typical likelihood group, this measure did not differentiate between the two elevated likelihood groups. We interpret the results as supporting the view that atypical direct-gaze responses are not early markers of autism.

How 18-month-olds with Later Autism Look at Other Children Interacting: The Timing of Gaze Allocation.

When observing other people during naturally paced and dynamic interactions, it is essential to look at specific locations at the right time to extract a maximum of socially informative content. In this study, we aimed to investigate the looking behavior of typically developing toddlers and toddlers later diagnosed with autism when observing other children interact. The sample consisted of 98 toddlers; 22 in a low-likelihood of autism group, 60 in an elevated likelihood of autism group who did not receive a subsequent diagnosis, and 16 in an elevated likelihood group who did receive an autism diagnosis. Participants performed an eye tracking task at 18 months of age and were assessed for diagnostic outcome at 36 months. The video stimuli consisted of two children interacting, where a boy reaches out for a toy and a girl refuses to give it to him. The low likelihood group showed an expected increase in ratio of looking at the girl's face after the boy requested the toy, as compared to before (t(21) = -3.337, p = .003). Toddlers with later autism showed a significantly lower ratio of looking at the girl's face during this time window, as compared to the other groups (F(2,91) = 3.698, p = .029). These findings provide new leads on how social gaze may be different in children with autism in everyday life (e.g., kindergarten), and highlight the need of studying the dynamics of gaze on short time scales.

Stable eye versus mouth preference in a live speech-processing task.

Looking at the mouth region is thought to be a useful strategy for speech-perception tasks. The tendency to look at the eyes versus the mouth of another person during speech processing has thus far mainly been studied using screen-based paradigms. In this study, we estimated the eye-mouth-index (EMI) of 38 adult participants in a live setting. Participants were seated across the table from an experimenter, who read sentences out loud for the participant to remember in both a familiar (English) and unfamiliar (Finnish) language. No statistically significant difference in the EMI between the familiar and the unfamiliar languages was observed. Total relative looking time at the mouth also did not predict the number of correctly identified sentences. Instead, we found that the EMI was higher during an instruction phase than during the speech-processing task. Moreover, we observed high intra-individual correlations in the EMI across the languages and different phases of the experiment. We conclude that there are stable individual differences in looking at the eyes versus the mouth of another person. Furthermore, this behavior appears to be flexible and dependent on the requirements of the situation (speech processing or not).

Early-life differences in the gut microbiota composition and functionality of infants at elevated likelihood of developing autism spectrum disorder.

Evidence from cross-sectional human studies, and preliminary microbial-based intervention studies, have implicated the microbiota-gut-brain axis in the neurobiology of autism spectrum disorder (ASD). Using a prospective longitudinal study design, we investigated the developmental profile of the fecal microbiota and metabolome in infants with (n = 16) and without (n = 19) a family history of ASD across the first 36 months of life. In addition, the general developmental levels of infants were evaluated using the Mullen Scales of Early Learning (MSEL) test at 5 and 36 months of age, and with ADOS-2 at 36 months of age. At 5 months of age, infants at elevated-likelihood of ASD (EL) harbored less Bifidobacterium and more Clostridium and Klebsiella species compared to the low-likelihood infants (LL). Untargeted metabolic profiling highlighted that LL infants excreted a greater amount of fecal γ-aminobutyric acid (GABA) at 5 months, which progressively declined with age. Similar age-dependent patterns were not observed in the EL group, with GABA being consistently low across all timepoints. Integrated microbiome-metabolome analysis showed a positive correlation between GABA and Bifidobacterium species and negative associations with Clostridium species. In vitro experiments supported these observations demonstrating that bifidobacteria can produce GABA while clostridia can consume it. At the behavioral level, there were no significant differences between the EL and LL groups at 5 months. However, at 36 months of age, the EL group had significantly lower MSEL and ADOS-2 scores compared to the LL group. Taken together, the present results reveal early life alterations in gut microbiota composition and functionality in infants at elevated-likelihood of ASD. These changes occur before any behavioral impairments can be detected, supporting a possible role for the gut microbiota in emerging behavioral variability later in life.

Pre-pragmatic language use in toddlerhood: Developmental antecedents, aetiological factors, and associations to autism.

Background: Pragmatic language is key for adaptive communication, but often compromised in neurodevelopmental conditions such as autism spectrum disorder (ASD). Decontextualized language-to talk about events and things beyond here and now-develops early in childhood and can be seen as a pre-pragmatic ability. Little is known about the factors that contribute to decontextualized language use in toddlers and whether these are different from factors contributing to general language development. Methods: We studied longitudinal associations between parent-rated core language and non-verbal socio-communicative abilities at 14 months of age, and decontextualized language use at 24 months of age in children with typical and elevated likelihood of ASD (total N = 303). Using twin modelling, we also investigated genetic and environmental contributions on decontextualized language and grammar use in two-year-old twin pairs (total N = 374). Results: Core language ability was a strong predictor of later decontextualized language use in both children with and without an elevated likelihood of ASD. In contrast, social communication was only a significant predictor of decontextualized language use for children with low levels of core language. This pattern was specific to decontextualized language, and not replicated in prediction of concurrent grammatical ability. Further, there was a large genetic influence on decontextualized language at 2 years of age, which mostly overlapped with the genetic influences on grammatical ability. Shared environment influences were significant for grammatical ability, but not found on decontextualized language. In children with an elevated likelihood of ASD, decontextualized language use was negatively associated with autistic symptoms. Conclusions: This study suggests that decontextualized language is developmentally associated with, yet dissociable from, more general language development measured as grammatical ability. Already at 2 years of age, parental ratings of decontextualized language is associated to clinician-rated symptoms of ASD.

Using the Infant Sibling-Design to Explore Associations Between Autism and ADHD Traits in Probands and Temperament in the Younger Siblings.

The purpose of the current study was to use the infant sibling design to explore whether proband traits of autism and ADHD could provide information about their infant sibling's temperament. This could help us to gain information about the extent to which infant temperament traits are differentially associated with autism and ADHD traits. We used parent-ratings of autistic traits and ADHD traits (CRS-3) in older siblings diagnosed with autism (age range 4 to 19 years), and their infant siblings' temperament traits (IBQ) at 9 months of age in 216 sibling pairs from two sites (BASIS, UK, and EASE, Sweden) to examine associations across siblings. We found specific, but modest, associations across siblings after controlling for sex, age, developmental level and site. Proband autistic traits were specifically related to low levels of approach in the infant siblings, with infant developmental level explaining part of the variance in infant approach. Proband ADHD traits were specifically related to high levels of infant activity even after controlling for covariates. Our findings suggest that proband traits of autism and ADHD carry information for infant sibling's temperament, indicating that inherited liability may influence early emerging behaviours in infant siblings. The impact of sex, age, developmental level and site are discussed.

Global motion processing in infants' visual cortex and the emergence of autism.

Autism is a heritable and common neurodevelopmental condition, with behavioural symptoms typically emerging around age 2 to 3 years. Differences in basic perceptual processes have been documented in autistic children and adults. Specifically, data from many experiments suggest links between autism and alterations in global visual motion processing (i.e., when individual motion information is integrated to perceive an overall coherent pattern). Yet, no study has investigated whether a distinctive organization of global motion processing precede the emergence of autistic symptoms in early childhood. Here, using a validated infant electroencephalography (EEG) experimental paradigm, we first establish the normative activation profiles for global form, global motion, local form, and local motion in the visual cortex based on data from two samples of 5-month-old infants (total n = 473). Further, in a sample of 5-month-olds at elevated likelihood of autism (n = 52), we show that a different topographical organization of global motion processing is associated with autistic symptoms in toddlerhood. These findings advance the understanding of neural organization of infants' basic visual processing, and its role in the development of autism.

Social Attention: Developmental Foundations and Relevance for Autism Spectrum Disorder.

The use of the term "social attention" (SA) in the cognitive neuroscience and developmental psychopathology literature has increased exponentially in recent years, in part motivated by the aim to understand the early development of autism spectrum disorder (ASD). Unfortunately, theoretical discussions around the term have lagged behind its various uses. Here, we evaluate SA through a review of key candidate SA phenotypes emerging early in life, from newborn gaze cueing and preference for face-like configurations to later emerging skills such as joint attention. We argue that most of the considered SA phenotypes are unlikely to represent unique socioattentional processes and instead have to be understood in the broader context of bottom-up and emerging top-down (domain-general) attention. Some types of SA behaviors (e.g., initiation of joint attention) are linked to the early development of ASD, but this may reflect differences in social motivation rather than attention per se. Several SA candidates are not linked to ASD early in life, including the ones that may represent uniquely socioattentional processes (e.g., orienting to faces, predicting others' manual action goals). Although SA may be a useful superordinate category under which one can organize certain research questions, the widespread use of the term without proper definition is problematic. Characterizing gaze patterns and visual attention in social contexts in infants at elevated likelihood of ASD may facilitate early detection, but conceptual clarity regarding the underlying processes at play is needed to sharpen research questions and identify potential targets for early intervention.

Preferential looking to eyes versus mouth in early infancy: heritability and link to concurrent and later development.

BACKGROUND: From birth, infants orient preferentially to faces, and when looking at the face, they attend primarily to eyes and mouth. These areas convey different types of information, and earlier research suggests that genetic factors influence the preference for one or the other in young children. METHODS: In a sample of 535 5-month-old infant twins, we assessed eye (relative to mouth) preference in early infancy, i.e., before neural systems for social communication and language are fully developed. We investigated the contribution of genetic and environmental factors to the preference for looking at eyes, and the association with concurrent traits and follow-up measures. RESULTS: Eye preference was independent from all other concurrent traits measured, and had a moderate-to-high contribution from genetic influences (A = 0.57; 95% CI: 0.45, 0.66). Preference for eyes at 5 months was associated with higher parent ratings of receptive vocabulary at 14 months. No statistically significant association with later autistic traits was found. Preference for eyes was strikingly stable across different stimulus types (e.g., dynamic vs. still), suggesting that infants' preference at this age does not reflect sensitivity to low-level visual cues. CONCLUSIONS: These results suggest that individual differences in infants' preferential looking to eyes versus mouth to a substantial degree reflect genetic variation. The findings provide new leads on both the perceptual basis and the developmental consequences of these attentional biases.

Infants' sense of approximate numerosity: Heritability and link to other concurrent traits.

The ability to perceive approximate numerosity is present in many animal species, and emerges early in human infants. Later in life, it is moderately heritable and associated with mathematical abilities, but the etiology of the Approximate Number System (ANS) and its degree of independence from other cognitive abilities in infancy is unknown. Here, we assessed the phenotypic specificity as well as the influence of genetic and environmental factors on the ANS in a sample of 5-month-old twins (N = 514). We found a small-to-moderate but statistically significant effect of genetic factors on ANS acuity (heritability = 0.18, 95% CI: 0.02, 0.33), but only when differences in numerosity were relatively large (1:4 ratio). Non-verbal ability assessed with the Mullen Scales of Early Learning (MSEL) was found to be heritable (0.47; 95% CI: 0.34, 0.57) and the phenotypic association between ANS acuity and non-verbal ability performance was close to zero. Similarly, we found no association between ANS acuity and general attention during the task. An unexpected weak but statistically significant negative association between ANS acuity and scores on the receptive language scale of the MSEL was found. These results suggest that early ANS function may be largely independent from other aspects of non-verbal development. Further, variability in ANS in infancy seems to, to some extent, reflect genotypic differences in the population. HIGHLIGHTS: Assessing 514 infant twins with eye tracking, we found that infants' sense of approximate numerosity is heritable and not positively associated with concurrent attentional, cognitive or motor abilities. These results have implications for our understanding of development of mathematical ability and the link between cognitive abilities early in postnatal life.

Autistic Children Quickly Orient Away from Both Eyes and Mouths During Face Observation.

Studies have supported two different hypotheses of reduced eye gaze in people with ASD; gaze avoidance and gaze indifference, while less is known about the role of anxiety. We tested these hypotheses using an eye-tracking paradigm that cued the eyes or mouth of emotional faces. Autistic children (n = 12, mean age 7 years) looked faster away from both eyes and mouths than controls (n = 22). This effect was not explained by anxiety symptoms. No difference was found in latency towards either area. These results indicate that attentional avoidance of autistic children is not specific to eyes, and that they do not show attentional indifference to eyes compared to controls. Atypicalities in visual scanning in ASD are possibly unrelated to specific facial areas.