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Featured ArticleResearch Articles, Behavioral/Cognitive

Pupil-Linked Arousal Response Reveals Aberrant Attention Regulation among Children with Autism Spectrum Disorder

Sijia Zhao, Yajie Liu and Kunlin Wei
Journal of Neuroscience 6 July 2022, 42 (27) 5427-5437; DOI: https://doi.org/10.1523/JNEUROSCI.0223-22.2022
Sijia Zhao
1Department of Experimental Psychology, University of Oxford, Oxford OX2 6AE, United Kingdom
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Yajie Liu
2Beijing Key Laboratory of Behavior and Mental Health, School of Psychological and Cognitive Sciences, Peking University, Beijing 100080, China
3Key Laboratory of Machine Perception (Ministry of Education), Peking University, Beijing 100080, China
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Kunlin Wei
2Beijing Key Laboratory of Behavior and Mental Health, School of Psychological and Cognitive Sciences, Peking University, Beijing 100080, China
3Key Laboratory of Machine Perception (Ministry of Education), Peking University, Beijing 100080, China
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Abstract

Autism spectrum disorder (ASD) is a developmental disorder that is characterized by difficulties with social interaction and interpersonal communication. It has been argued that abnormal attentional function to exogenous stimuli precedes and contributes to the core ASD symptoms. Notably, the locus ceruleus (LC) and its noradrenergic projections throughout the brain modulate attentional function, but the extent to which this locus ceruleus–norepinephrine (LC–NE) system influences attention in individuals with ASD, who frequently exhibit dysregulated alerting and attention orienting, is unknown. We examined dynamic attention control in girls and boys with ASD at rest using the pupil dilation response (PDR) as a noninvasive measure of LC–NE activity. When gender- and age-matched neurotypical participants were passively exposed to an auditory stream, their PDR decreased for recurrent stimuli but remained sensitive to surprising deviant stimuli. In contrast, children with ASD showed less habituation to recurrent stimuli as well as a diminished phasic response to deviants, particularly those containing social information. Their tonic habituation impairment predicts their phasic orienting impairment, and both impairments correlated with the severity of ASD symptom. Because of the fact that these pupil-linked responses are observed when individuals passively listen without any task engagement, our findings imply that the intricate and dynamic attention allocation mechanism, mediated by the subcortical LC–NE system, is impaired in ASD.

SIGNIFICANCE STATEMENT Autistic individuals show attentional abnormalities to even simple sensory inputs, which emerge even before formal diagnosis. One possible mechanism behind these abnormalities is a malfunctioning pacemaker of their attention system, the locus ceruleus–norepinephrine pathway. Here we found, according to the pupillary response (a noradrenergic activity proxy), autistic children are hypersensitive to repeated sounds but hyposensitive to surprising deviant sounds when compared with age-matched controls. Importantly, hypersensitivity to repetitions predicts hyposensitivity to deviant sounds, and both abnormalities positively correlate to the severity of autistic symptoms. This provides strong evidence that autistic children have faulty noradrenergic regulation, which might underly the attentional atypicalities previously evidenced in various cortical responses in autistic individuals.

  • attention
  • autism spectrum disorder
  • locus ceruleus
  • norepinephrine
  • pupil dilation response

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The Journal of Neuroscience: 42 (27)
Journal of Neuroscience
Vol. 42, Issue 27
6 Jul 2022
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Pupil-Linked Arousal Response Reveals Aberrant Attention Regulation among Children with Autism Spectrum Disorder
Sijia Zhao, Yajie Liu, Kunlin Wei
Journal of Neuroscience 6 July 2022, 42 (27) 5427-5437; DOI: 10.1523/JNEUROSCI.0223-22.2022

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Pupil-Linked Arousal Response Reveals Aberrant Attention Regulation among Children with Autism Spectrum Disorder
Sijia Zhao, Yajie Liu, Kunlin Wei
Journal of Neuroscience 6 July 2022, 42 (27) 5427-5437; DOI: 10.1523/JNEUROSCI.0223-22.2022
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Keywords

  • attention
  • autism spectrum disorder
  • locus ceruleus
  • norepinephrine
  • pupil dilation response

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