Infant Neural Sensitivity to Dynamic Eye Gaze Is Associated with Later Emerging Autism

Centre for Brain and Cognitive Development, Birkbeck College, University of London, London WC1E 7HX, UK.
Current biology: CB (Impact Factor: 9.57). 02/2012; 22(4):338-42. DOI: 10.1016/j.cub.2011.12.056
Source: PubMed


Autism spectrum disorders (henceforth autism) are diagnosed in around 1% of the population [1]. Familial liability confers risk for a broad spectrum of difficulties including the broader autism phenotype (BAP) [2, 3]. There are currently no reliable predictors of autism in infancy, but characteristic behaviors emerge during the second year, enabling diagnosis after this age [4, 5]. Because indicators of brain functioning may be sensitive predictors, and atypical eye contact is characteristic of the syndrome [6-9] and the BAP [10, 11], we examined whether neural sensitivity to eye gaze during infancy is associated with later autism outcomes [12, 13]. We undertook a prospective longitudinal study of infants with and without familial risk for autism. At 6-10 months, we recorded infants' event-related potentials (ERPs) in response to viewing faces with eye gaze directed toward versus away from the infant [14]. Longitudinal analyses showed that characteristics of ERP components evoked in response to dynamic eye gaze shifts during infancy were associated with autism diagnosed at 36 months. ERP responses to eye gaze may help characterize developmental processes that lead to later emerging autism. Findings also elucidate the mechanisms driving the development of the social brain in infancy.

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    • "With the first overt behavioural symptoms appearing only toward the end of the first year of life, affected infants will typically not be routinely diagnosed before their third birthday (E.J.H. Jones et al., 2014). However, results from infant sibling studies suggest that the underlying differences in brain function that later on give rise to the behavioural symptoms may already be evident during the first year of life (Elsabbagh et al., 2012; Lloyd-Fox et al., 2013). Despite this, to our knowledge, no studies have directly investigated brain response to human vocal sounds in infants at high risk of ASD. "
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    ABSTRACT: Adults diagnosed with autism spectrum disorder (ASD) show a reduced sensitivity (degree of selective response) to social stimuli such as human voices. In order to determine whether this reduced sensitivity is a consequence of years of poor social interaction and communication or is present prior to significant experience, we used functional MRI to examine cortical sensitivity to auditory stimuli in infants at high familial risk for later emerging ASD (HR group, N = 15), and compared this to infants with no family history of ASD (LR group, N = 18). The infants (aged between 4 and 7 months) were presented with voice and environmental sounds while asleep in the scanner and their behaviour was also examined in the context of observed parent-infant interaction. Whereas LR infants showed early specialisation for human voice processing in right temporal and medial frontal regions, the HR infants did not. Similarly, LR infants showed stronger sensitivity than HR infants to sad vocalisations in the right fusiform gyrus and left hippocampus. Also, in the HR group only, there was an association between each infant's degree of engagement during social interaction and the degree of voice sensitivity in key cortical regions. These results suggest that at least some infants at high-risk for ASD have atypical neural responses to human voice with and without emotional valence. Further exploration of the relationship between behaviour during social interaction and voice processing may help better understand the mechanisms that lead to different outcomes in at risk populations. Copyright © 2015 The Authors. Published by Elsevier Ltd.. All rights reserved.
    Cortex 06/2015; 71. DOI:10.1016/j.cortex.2015.06.015 · 5.13 Impact Factor
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    • "In contrast to typically developing children, those who develop ASD show slower face processing [90], lack of differentiation of gaze direction toward vs away [91], decreased attention to social scenes [92] [93], and no quickened response to an object cued by eye gaze [94], signifying a defect in joint attention. We suggest that the non-social AV brain specialization alters the response to social experience, consistent with the finding that children with ASD are effective processors of nonhuman AV stimuli, but they exhibit lower processing scores than typical when faces and voices are involved [95]. "
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    ABSTRACT: Earliest identifiable findings in autism indicate that the autistic brain develops differently from the typical brain in the first year of life, after a period of typical development. Twin studies suggest that autism has an environmental component contributing to causation. Increased availability of audiovisual (AV) materials and viewing practices of infants parallel the time frame of the rise in prevalence of autism spectrum disorder (ASD). Studies have shown an association between ASD and increased TV/cable screen exposure in infancy, suggesting AV exposure in infancy as a possible contributing cause of ASD. Infants are attracted to the saliency of AV materials, yet do not have the experience to recognize these stimuli as socially relevant. The authors present a developmental model of autism in which exposure to screen-based AV input in genetically susceptible infants stimulates specialization of non-social sensory processing in the brain. Through a process of neuroplasticity, the autistic infant develops the skills that are driven by the AV viewing. The AV developed neuronal pathways compete with preference for social processing, negatively affecting development of social brain pathways and causing global developmental delay. This model explains atypical face and speech processing, as well as preference for AV synchrony over biological motion in ASD. Neural hyper-connectivity, enlarged brain size and special abilities in visual, auditory and motion processing in ASD are also explained by the model. Positive effects of early intervention are predicted by the model. Researchers studying causation of autism have largely overlooked AV exposure in infancy as a potential contributing factor. The authors call for increased public awareness of the association between early screen viewing and ASD, and a concerted research effort to determine the extent of causal relationship. Copyright © 2015. Published by Elsevier Ltd.
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    • "This also suggests that the later developing principles might be more malleable, whereas the early developing principles might be more influenced by the infants' biological predispositions and thus be under greater genetic control (McCall, 1981; Zwaigenbaum et al., 2005). This notion receives support from work on neurodevelopmental disorders that affect social behavior such as autism, showing that autism is associated with impaired self-relevance detection and joint engagement (Charman, 2003; Elsabbagh et al., 2012). In fact, these impairments have been argued to be some of the earliest warning signs for autism, detectable in infants' behavior by the end of the first year of life (Zwaigenbaum et al., 2005). "
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    ABSTRACT: One fundamental question in psychology is what makes humans such intensely social beings. Probing the developmental and neural origins of our social capacities is a way of addressing this question. In the last 10 years the field of social-cognitive development has witnessed a surge in studies using neuroscience methods to elucidate the development of social information processing during infancy. While the use of electroencephalography (EEG)/event-related brain potentials (ERPs) and functional near-infrared spectroscopy (fNIRS) has revealed a great deal about the timing and localization of the cortical processes involved in early social cognition, the principles underpinning the early development of social brain functioning remain largely unexplored. Here I provide a framework that delineates the essential processes implicated in the early development of the social brain. In particular, I argue that the development of social brain functions in infancy is characterized by the following key principles: (a) self-relevance, (b) joint engagement, (c) predictability, (d) categorization, (e) discrimination, and (f) integration. For all of the proposed principles, I provide empirical examples to illustrate when in infancy they emerge. Moreover, I discuss to what extent they are in fact specifically social in nature or share properties with more domain-general developmental principles. Taken together, this article provides a conceptual integration of the existing EEG/ERPs and fNIRS work on infant social brain function and thereby offers the basis for a principle-based approach to studying the neural correlates of early social cognition. (PsycINFO Database Record (c) 2015 APA, all rights reserved).
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