Developmental Cognitive Neuroscience : Autism Spectrum Condition – understanding sensory and social features (Janvier 2018)
Le numéro de janvier 2018 de Developmental Cognitive Neuroscience est consacré aux aspects sensoriels et sociaux de l’autisme :
Autism Spectrum Condition – understanding sensory and social features
1. Hamilton A, Pelphrey K. Sensory and social features of autism – can they be integrated ?. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:1-3.
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2. Cheung CHM, Bedford R, Johnson MH, Charman T, Gliga T. Visual search performance in infants associates with later ASD diagnosis. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:4-10.
An enhanced ability to detect visual targets amongst distractors, known as visual search (VS), has often been documented in Autism Spectrum Disorders (ASD). Yet, it is unclear when this behaviour emerges in development and if it is specific to ASD. We followed up infants at high and low familial risk for ASD to investigate how early VS abilities links to later ASD diagnosis, the potential underlying mechanisms of this association and the specificity of superior VS to ASD. Clinical diagnosis of ASD as well as dimensional measures of ASD, attention-deficit/hyperactivity disorder (ADHD) and anxiety symptoms were ascertained at 3 years. At 9 and 15 months, but not at age 2 years, high-risk children who later met clinical criteria for ASD (HR-ASD) had better VS performance than those without later diagnosis and low-risk controls. Although HR-ASD children were also more attentive to the task at 9 months, this did not explain search performance. Superior VS specifically predicted 3 year-old ASD but not ADHD or anxiety symptoms. Our results demonstrate that atypical perception and core ASD symptoms of social interaction and communication are closely and selectively associated during early development, and suggest causal links between perceptual and social features of ASD.
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3. Jones EJH, Dawson G, Webb SJ. Sensory hypersensitivity predicts enhanced attention capture by faces in the early development of ASD. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:11-20.
Sensory sensitivity is prevalent among young children with ASD, but its relation to social communication impairment is unclear. Recently, increased sensory hypersensitivity has been linked to greater activity of the neural salience network (Green et al., 2016). Increased neural sensitivity to stimuli, especially social stimuli, could provide greater opportunity for social learning and improved outcomes. Consistent with this framework, in Experiment 1 we found that parent report of greater sensory hypersensitivity at 2 years in toddlers with ASD (N=27) was predictive of increased neural responsiveness to social stimuli (larger amplitude event-related potential/ERP responses to faces at P1, P400 and Nc) at 4 years, and this in turn was related to parent report of increased social approach at 4 years. In Experiment 2, parent report of increased perceptual sensitivity at 6 months in infants at low and high familial risk for ASD (N=35) predicted larger ERP P1 amplitude to faces at 18 months. Increased sensory hypersensitivity in early development thus predicted greater attention capture by faces in later development, and this related to more optimal social behavioral development. Sensory hypersensitivity may index a child’s ability to benefit from supportive environments during development. Early sensory symptoms may not always be developmentally problematic for individuals with ASD.
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4. Vernetti A, Senju A, Charman T, Johnson MH, Gliga T. Simulating interaction : Using gaze-contingent eye-tracking to measure the reward value of social signals in toddlers with and without autism. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:21-29.
Several accounts have been proposed to explain difficulties with social interaction in autism spectrum disorder (ASD), amongst which atypical social orienting, decreased social motivation or difficulties with understanding the regularities driving social interaction. This study uses gaze-contingent eye-tracking to tease apart these accounts by measuring reward related behaviours in response to different social videos. Toddlers at high or low familial risk for ASD took part in this study at age 2 and were categorised at age 3 as low risk controls (LR), high-risk with no ASD diagnosis (HR-no ASD), or with a diagnosis of ASD (HR-ASD). When the on-demand social interaction was predictable, all groups, including the HR-ASD group, looked longer and smiled more towards a person greeting them compared to a mechanical Toy (Condition 1) and also smiled more towards a communicative over a non-communicative person (Condition 2). However, all groups, except the HR-ASD group, selectively oriented towards a person addressing the child in different ways over an invariant social interaction (Condition 3). These findings suggest that social interaction is intrinsically rewarding for individuals with ASD, but the extent to which it is sought may be modulated by the specific variability of naturalistic social interaction.
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5. Baranek GT, Woynaroski TG, Nowell S, Turner-Brown L, DuBay M, Crais ER, Watson LR. Cascading effects of attention disengagement and sensory seeking on social symptoms in a community sample of infants at-risk for a future diagnosis of autism spectrum disorder. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:30-40.
Recent work suggests sensory seeking predicts later social symptomatology through reduced social orienting in infants who are at high-risk for autism spectrum disorder (ASD) based on their status as younger siblings of children diagnosed with ASD. We drew on extant longitudinal data from a community sample of at-risk infants who were identified at 12 months using the First Year Inventory, and followed to 3–5 years. We replicate findings of Damiano et al. (in this issue) that a) high-risk infants who go on to be diagnosed with ASD show heightened sensory seeking in the second year of life relative to those who do not receive a diagnosis, and b) increased sensory seeking indirectly relates to later social symptomatology via reduced social orienting. We extend previous findings to show that sensory seeking has more clinical utility later in the second year of life (20–24 months) than earlier (13–15 months). Further, this study suggests that diminished attention disengagement at 12–15 months may precede and predict increased sensory seeking at 20–24 months. Findings add support for the notion that sensory features produce cascading effects on social development in infants at risk for ASD, and suggest that reduced attention disengagement early in life may set off this cascade.
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6. Damiano-Goodwin CR, Woynaroski TG, Simon DM, Ibañez LV, Murias M, Kirby A, Newsom CR, Wallace MT, Stone WL, Cascio CJ. Developmental sequelae and neurophysiologic substrates of sensory seeking in infant siblings of children with autism spectrum disorder. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:41-53.
It has been proposed that early differences in sensory responsiveness arise from atypical neural function and produce cascading effects on development across domains. This longitudinal study prospectively followed infants at heightened risk for autism spectrum disorder (ASD) based on their status as younger siblings of children diagnosed with ASD (Sibs-ASD) and infants at relatively lower risk for ASD (siblings of typically developing children ; Sibs-TD) to examine the developmental sequelae and possible neurophysiological substrates of a specific sensory response pattern : unusually intense interest in nonsocial sensory stimuli or “sensory seeking.” At 18 months, sensory seeking and social orienting were measured with the Sensory Processing Assessment, and a potential neural signature for sensory seeking (i.e., frontal alpha asymmetry) was measured via resting state electroencephalography. At 36 months, infants’ social symptomatology was assessed in a comprehensive diagnostic evaluation. Sibs-ASD showed elevated sensory seeking relative to Sibs-TD, and increased sensory seeking was concurrently associated with reduced social orienting across groups and resting frontal asymmetry in Sibs-ASD. Sensory seeking also predicted later social symptomatology. Findings suggest that sensory seeking may produce cascading effects on social development in infants at risk for ASD and that atypical frontal asymmetry may underlie this atypical pattern of sensory responsiveness.
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7. Vivanti G, Hocking DR, Fanning PAJ, Uljarevic M, Postorino V, Mazzone L, Dissanayake C. Attention to novelty versus repetition : Contrasting habituation profiles in Autism and Williams syndrome. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:54-60.
Background Abnormalities in habituation have been documented in Autism Spectrum Disorder (ASD) and Williams syndrome (WS). Such abnormalities have been proposed to underlie the distinctive social and non-social difficulties that define ASD, including sensory features and repetitive behaviours, and the distinctive social phenotype characterizing WS. Methods We measured habituation in 39 preschoolers with ASD, 20 peers with WS and 19 typically developing (TD) children using an eye-tracking protocol that measured participants’ duration of attention in response to a repeating stimulus and a novel stimulus presented side by side across multiple trials. Results Participants in the TD group and the WS group decreased their attention toward the repeating stimulus and increased their attention to the novel stimulus over time. Conversely, the ASD group showed a similar attentional response to the novel and repeating stimuli. Habituation was correlated with social functioning in the WS but not in the ASD group. Contrary to predictions, slower habituation in ASD was associated with lower severity of repetitive behaviours. Conclusions Habituation appears to be intact in WS and impaired in ASD. More research is needed to clarify the nature of the syndrome-specific patterns of correlations between habituation and social and non-social functioning in these neurodevelopmental disorders.
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8. Guy MW, Richards JE, Tonnsen BL, Roberts JE. Neural correlates of face processing in etiologically-distinct 12-month-old infants at high-risk of autism spectrum disorder. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:61-71.
Neural correlates of face processing were examined in 12-month-olds at high-risk for autism spectrum disorder (ASD), including 21 siblings of children with ASD (ASIBs) and 15 infants with fragile X syndrome (FXS), as well as 21 low-risk (LR) controls. Event-related potentials were recorded to familiar and novel face and toy stimuli. All infants demonstrated greater N290 amplitude to faces than toys. At the Nc component, LR infants showed greater amplitude to novel stimuli than to their mother’s face and own toy, whereas infants with FXS showed the opposite pattern of responses and ASIBs did not differentiate based on familiarity. These results reflect developing face specialization across high- and low-risk infants and reveal neural patterns that distinguish between groups at high-risk for ASD.
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9. Tavassoli T, Miller LJ, Schoen SA, Jo Brout J, Sullivan J, Baron-Cohen S. Sensory reactivity, empathizing and systemizing in autism spectrum conditions and sensory processing disorder. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:72-77.
Although the DSM-5 added sensory symptoms as a criterion for ASC, there is a group of children who display sensory symptoms but do not have ASC ; children with sensory processing disorder (SPD). To be able to differentiate these two disorders, our aim was to evaluate whether children with ASC show more sensory symptomatology and/or different cognitive styles in empathy and systemizing compared to children with SPD and typically developing (TD) children. The study included 210 participants : 68 children with ASC, 79 with SPD and 63 TD children. The Sensory Processing Scale Inventory was used to measure sensory symptoms, the Autism Spectrum Quotient (AQ) to measure autistic traits, and the Empathy Quotient (EQ) and Systemizing Quotient (SQ) to measure cognitive styles. Across groups, a greater sensory symptomatology was associated with lower empathy. Further, both the ASC and SPD groups showed more sensory symptoms than TD children. Children with ASC and SPD only differed on sensory under-reactivity. The ASD group did, however, show lower empathy and higher systemizing scores than the SPD group. Together, this suggest that sensory symptoms alone may not be adequate to differentiate children with ASC and SPD but that cognitive style measures could be used for differential diagnosis.
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10. Ropar D, Greenfield K, Smith AD, Carey M, Newport R. Body representation difficulties in children and adolescents with autism may be due to delayed development of visuo-tactile temporal binding. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:78-85.
Recent research suggests visuo-tactile binding is temporally extended in autism spectrum disorders (ASD), although it is not clear whether this specifically underlies altered body representation in this population. In the current study children and adolescents with ASD, and typically developing controls, placed their hand into mediated reality system (MIRAGE) and saw two identical live video images of their own right hand. One image was in the proprioceptively correct location (veridical hand) and the other was displaced to either side. While visuo-tactile feedback was applied via brushstroke to the participant’s (unseen) right finger, they viewed one hand image receiving synchronous brushstrokes and the other receiving brushstrokes with a temporal delay (60, 180 and 300ms). After brushing, both images disappeared from view and participants pointed to a target, with direction of movement indicating which hand was embodied. ASD participants, like younger mental aged-matched controls, showed reduced embodiment of the spatially incongruent, but temporally congruent, hand compared to chronologically age-matched controls at shorter temporal delays. This suggests development of visuo-tactile integration may be delayed in ASD. Findings are discussed in relation to atypical body representation in ASD and how this may contribute to social and sensory difficulties within this population.
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11. Ansuini C, Podda J, Battaglia FM, Veneselli E, Becchio C. One hand, two hands, two people : Prospective sensorimotor control in children with autism. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:86-96.
Where grasps are made reveals how grasps are planned. The grasp height effect predicts that, when people take hold of an object to move it to a new position, the grasp height on the object is inversely related to the height of the target position. In the present study, we used this effect as a window into the prospective sensorimotor control of children with autism spectrum disorders without accompanying intellectual impairment. Participants were instructed to grasp a vertical cylinder and move it from a table (home position) to a shelf of varying height (target position). Depending on the conditions, they performed the task using only one hand (unimanual), two hands (bimanual), or with the help of a co-actor (joint). Comparison between the performance of typically developing children and children with autism revealed no group difference across tasks. We found, however, a significant influence of IQ on grasp height modulation in both groups. These results provide clear evidence against a general prospective sensorimotor planning deficit and suggest that at least some form of higher order planning is present in autism without accompanying intellectual impairment.
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12. Karaminis T, Neil L, Manning C, Turi M, Fiorentini C, Burr D, Pellicano E. Reprint of “Investigating ensemble perception of emotions in autistic and typical children and adolescents”. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:97-107.
Ensemble perception, the ability to assess automatically the summary of large amounts of information presented in visual scenes, is available early in typical development. This ability might be compromised in autistic children, who are thought to present limitations in maintaining summary statistics representations for the recent history of sensory input. Here we examined ensemble perception of facial emotional expressions in 35 autistic children, 30 age- and ability-matched typical children and 25 typical adults. Participants received three tasks : a) an ‘ensemble’ emotion discrimination task ; b) a baseline (single-face) emotion discrimination task ; and c) a facial expression identification task. Children performed worse than adults on all three tasks. Unexpectedly, autistic and typical children were, on average, indistinguishable in their precision and accuracy on all three tasks. Computational modelling suggested that, on average, autistic and typical children used ensemble-encoding strategies to a similar extent ; but ensemble perception was related to non-verbal reasoning abilities in autistic but not in typical children. Eye-movement data also showed no group differences in the way children attended to the stimuli. Our combined findings suggest that the abilities of autistic and typical children for ensemble perception of emotions are comparable on average.
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13. Lawson RP, Aylward J, Roiser JP, Rees G. Adaptation of social and non-social cues to direction in adults with autism spectrum disorder and neurotypical adults with autistic traits. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:108-116.
Perceptual constancy strongly relies on adaptive gain control mechanisms, which shift perception as a function of recent sensory history. Here we examined the extent to which individual differences in magnitude of adaptation aftereffects for social and non-social directional cues are related to autistic traits and sensory sensitivity in healthy participants (Experiment 1) ; and also whether adaptation for social and non-social directional cues is differentially impacted in adults with Autism Spectrum Disorder (ASD) relative to neurotypical (NT) controls (Experiment 2). In Experiment 1, individuals with lower susceptibility to adaptation aftereffects, i.e. more ‘veridical’ perception, showed higher levels of autistic traits across social and non-social stimuli. Furthermore, adaptation aftereffects were predictive of sensory sensitivity. In Experiment 2, only adaptation to eye-gaze was diminished in adults with ASD, and this was related to difficulties categorizing eye-gaze direction at baseline. Autism Diagnostic Observation Schedule (ADOS) scores negatively predicted lower adaptation for social (head and eye-gaze direction) but not non-social (chair) stimuli. These results suggest that the relationship between adaptation and the broad socio-cognitive processing style captured by ‘autistic traits’ may be relatively domain-general, but in adults with ASD diminished adaptation is only apparent where processing is most severely impacted, such as the perception of social attention cues.
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14. Linke AC, Jao Keehn RJ, Pueschel EB, Fishman I, Müller R-A. Children with ASD show links between aberrant sound processing, social symptoms, and atypical auditory interhemispheric and thalamocortical functional connectivity. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:117-126.
Autism spectrum disorder (ASD) is a complex and prevalent neurodevelopmental disorder characterized by social and communicative deficits, as well as repetitive behaviors and atypical sensitivity to sensory stimulation. Alterations in network connectivity are widely recognized, but their interplay with social and sensory symptoms remains largely unclear. Here, functional magnetic resonance imaging and diagnostic and behavioral assessments were used in a cohort of children and adolescents with ASD (n=40) and matched typically developing (TD, n=38) controls to examine the relation between auditory processing, interhemispheric and thalamocortical network connectivity, and social-behavioral symptom severity. We found that atypical processing of sounds was related to social, cognitive, and communicative impairments. Additionally, severity of sensory processing deficits and lower verbal IQ were related to reduced interhemispheric connectivity of auditory cortices in ASD. Increased connectivity between the thalamus and auditory cortex in ASD, however, was associated with reduced cognitive and behavioral symptomatology, suggesting that thalamocortical overconnectivity might reflect a compensatory mechanism in ASD. These findings provide novel evidence for links between auditory sensory deficits and impairments in social interaction and communication.
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15. Green SA, Hernandez LM, Bowman HC, Bookheimer SY, Dapretto M. Sensory over-responsivity and social cognition in ASD : Effects of aversive sensory stimuli and attentional modulation on neural responses to social cues. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:127-139.
Sensory over-responsivity (SOR) is a common condition in autism spectrum disorders (ASD) that is associated with greater social impairment. However, the mechanisms through which sensory stimuli may affect social functioning are not well understood. This study used fMRI to examine brain activity while interpreting communicative intent in 15 high-functioning youth with ASD and 16 age- and IQ-matched typically-developing (TD) controls. Participants completed the task with and without a tactile sensory distracter, and with and without instructions directing their attention to relevant social cues. When completing the task in the presence of the sensory distracter, TD youth showed increased activity in auditory language and frontal regions whereas ASD youth showed decreased activation in these areas. Instructions mitigated this effect such that ASD youth did not decrease activation during tactile stimulation ; instead, the ASD group showed increased medial prefrontal activity. SOR severity modulated the effect of the tactile stimulus on social processing. Results demonstrate for the first time a neural mechanism through which sensory stimuli cause disruption of social cognition, and that attentional modulation can restore neural processing of social cues through prefrontal regulation. Findings have implications for novel, integrative interventions that incorporate attentional directives to target both sensory and social symptoms.
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16. Mikkelsen M, Wodka EL, Mostofsky SH, Puts NAJ. Autism spectrum disorder in the scope of tactile processing. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:140-150.
Sensory processing abnormalities are among the most common behavioral phenotypes seen in autism spectrum disorder (ASD), typically characterized by either over- or under-responsiveness to stimulation. In this review, we focus on tactile processing dysfunction in ASD. We firstly review clinical studies wherein sensitivity to tactile stimuli has traditionally been assessed by self-, parent- and experimenter-reports. We also discuss recent investigations using psychophysical paradigms that gauge individual tactile thresholds. These more experimentally rigorous studies allow for more objective assessments of tactile abnormalities in ASD. However, little is understood about the neurobiological mechanisms underlying these abnormalities, or the link between tactile abnormalities and ASD symptoms. Neurobiological research that has been conducted has pointed toward dysfunction in the excitation/inhibition balance of the central nervous system of those with ASD. This review covers recent efforts that have investigated tactile dysfunction in ASD from clinical and behavioral perspectives, and some of the efforts to link these to neurobiology. On the whole, findings are inconsistent, which can be ascribed to the subjectivity of clinical assessments, the heterogeneity of ASD cohorts, and the diversity of tactile sensitivity measures. Future endeavors into understanding tactile processing differences in ASD will greatly benefit from controlled experiments driven by neurobiological hypotheses.
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17. Thye MD, Bednarz HM, Herringshaw AJ, Sartin EB, Kana RK. The impact of atypical sensory processing on social impairments in autism spectrum disorder. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:151-167.
Altered sensory processing has been an important feature of the clinical descriptions of autism spectrum disorder (ASD). There is evidence that sensory dysregulation arises early in the progression of ASD and impacts social functioning. This paper reviews behavioral and neurobiological evidence that describes how sensory deficits across multiple modalities (vision, hearing, touch, olfaction, gustation, and multisensory integration) could impact social functions in ASD. Theoretical models of ASD and their implications for the relationship between sensory and social functioning are discussed. Furthermore, neural differences in anatomy, function, and connectivity of different regions underlying sensory and social processing are also discussed. We conclude that there are multiple mechanisms through which early sensory dysregulation in ASD could cascade into social deficits across development. Future research is needed to clarify these mechanisms, and specific focus should be given to distinguish between deficits in primary sensory processing and altered top-down attentional and cognitive processes.
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18. Bolis D, Schilbach L. Observing and participating in social interactions : Action perception and action control across the autistic spectrum. Developmental Cognitive Neuroscience ;2018 (2018/01/01/) ;29:168-175.
Autism is a developmental condition, characterized by difficulties of social interaction and communication, as well as restricted interests and repetitive behaviors. Although several important conceptions have shed light on specific facets, there is still no consensus about a universal yet specific theory in terms of its underlying mechanisms. While some theories have exclusively focused on sensory aspects, others have emphasized social difficulties. However, sensory and social processes in autism might be interconnected to a higher degree than what has been traditionally thought. We propose that a mismatch in sensory abilities across individuals can lead to difficulties on a social, i.e. interpersonal level and vice versa. In this article, we, therefore, selectively review evidence indicating an interrelationship between perceptual and social difficulties in autism. Additionally, we link this body of research with studies, which investigate the mechanisms of action control in social contexts. By doing so, we highlight that autistic traits are also crucially related to differences in integration, anticipation and automatic responding to social cues, rather than a mere inability to register and learn from social cues. Importantly, such differences may only manifest themselves in sufficiently complex situations, such as real-life social interactions, where such processes are inextricably linked.