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Distinct Patterns of Neural Habituation and Generalization in Children and Adolescents With Autism With Low and High Sensory Overresponsivity

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Green, Shulamite A., Hernandez, Leanna, Lawrence, Katherine E., Liu, Janelle, Tsang, Tawny, Yeargin, Jillian, Cummings, Kaitlin, Laugeson, Elizabeth +2 more·2019·American Journal of Psychiatry
DOI 10.1176/appi.ajp.2019.18121333PMC PMC6889004
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Abstract

OBJECTIVE: Sensory overresponsivity (SOR), an atypical negative reaction to sensory stimuli, is highly prevalent in autism spectrum disorder (ASD). Previous work has related SOR to increased brain response in sensory-limbic regions. This study investigated where these atypical responses fall in three fundamental stages of sensory processing: arousal (i.e., initial response), habituation (i.e., change in response over time), and generalization of response to novel stimuli. Different areas of atypical response would require distinct intervention approaches. METHODS: Functional MRI was used to examine these patterns of neural habituation to two sets of similar mildly aversive auditory and tactile stimuli in 42 high-functioning children and adolescents with ASD (21 with high levels of SOR and 21 with low levels of SOR) and 27 age-matched typically developing youths (ages 8-17). The relationship between SOR and change in amygdala-prefrontal functional connectivity across the sensory stimulation was also examined. RESULTS: Across repeated sensory stimulation, high-SOR participants with ASD showed reduced ability to maintain habituation in the amygdala and relevant sensory cortices and to maintain inhibition of irrelevant sensory cortices. These results indicate that sensory habituation is a dynamic, time-varying process dependent on sustained regulation across time, which is a particular deficit in high-SOR participants with ASD. However, low-SOR participants with ASD also showed distinct, nontypical neural response patterns, including reduced responsiveness to novel but similar stimuli and increases in prefrontal-amygdala regulation across the sensory exposure. CONCLUSIONS: The results suggest that all children with autism have atypical brain responses to sensory stimuli, but whether they express atypical behavioral responses depends on top-down regulatory mechanisms. Results are discussed in terms of targeted intervention approaches.

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  • Children with high sensory over-responsivity show reduced ability to maintain habituation in the amygdala.

    “Children with high sensory over-responsivity showed reduced ability to maintain habituation in the amygdala (Green et al. 2019), together with increased resting-state functional connectivity between salience network nodes and brain regions implicated in primary sensory processing and attention (Green et al. 2018).”

    From Autism Spectrum Disorder and auditory sensory alterations: a systematic review on the integrity of cognitive and neuronal functions related to auditory processing (2023) · cites this paper as Green et al. 2019

    The Results (fMRI Results, Amygdala) show that the high-SOR group initially decreased but then increased its amygdala response, while the comparison groups sustained their decreases. The Methods specify that the high-SOR participants were youth with autism; the citing sentence omits that population qualifier and could be read as applying to children with high sensory over-responsivity generally. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • Autistic people with high sensory reactivity have atypical brain responses to sensory input, including difficulty with neural habituation and emotional down-regulation.

    “For example, Green et al. (2019) found that autistic people with high sensory reactivity have atypical brain responses to sensory input, including difficulty with neural habituation and emotional down-regulation.”

    From A mixed methods study of autistic adults' mental health therapy experiences (2023) · cites this paper as Green et al. (2019)

    The Discussion reports that autistic youth with high sensory overresponsivity lacked habituation in sensory cortices and the amygdala and could not maintain regulation of sensory responses. The Conclusions and Clinical Implications likewise say that high-SOR youth could not maintain down-regulation. The findings support the neural-response claim, but the study examined children and adolescents, not autistic people of all ages. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • Children with low sensory over-responsivity show atypical neural response patterns, with increased prefrontal-amygdala regulation across sensory exposure.

    “Children with low sensory over-responsivity showed atypical neural response patterns, with increased prefrontal–amygdala regulation across sensory exposure (Green et al. 2019).”

    From Autism Spectrum Disorder and auditory sensory alterations: a systematic review on the integrity of cognitive and neuronal functions related to auditory processing (2023) · cites this paper as Green et al. 2019

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Research works printed but not linked: 21

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Cited by

Sorted by citations

Authors
Green, S. A., Hernandez, L., Lawrence, K. E., Liu, J., Tsang, T., Yeargin, J., Cummings, K., Laugeson, E., Dapretto, M., & Bookheimer, S. Y.
Affiliations
University of California, Los Angeles (US)
ORCID
Venue
American Journal of Psychiatry
Publisher
American Psychiatric Association Publishing
Published
2019-12-01
Volume
176
Issue
12
Pages
1010-1020
ISSN
  • 0002-953X (ISSN-L)
  • 1535-7228
DOI
10.1176/appi.ajp.2019.18121333
PMC
PMC6889004
OpenAlex
W2954801592
Cited by
75
References
10
Citations by year
2026: 11 · 2025: 5 · 2024: 12 · 2023: 15 · 2022: 10 · 2021: 11 · 2020: 8 · 2019: 3
FWCI
4.65
Type
journal article
Language
en
Open access
Locations
  • American Journal of Psychiatry (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • National Institute of Mental Health (K08MH112871, F32MH105167, F31MH093999, R01MH100028, F31MH110140)
  • National Institute of Neurological Disorders and Stroke (F99NS105206, R01NS035193, T32NS048004)
  • National Center for Research Resources (P41RR013642, M01RR000865, C06RR012169)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (F31HD088102, U54HD087101, F31HD090937, P50HD055784)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
  • Health Sciences › Medicine › Psychiatry and Mental health › Child Nutrition and Feeding Issues
Keywords
sensory hypersensitivity, autism spectrum disorder, sensory habituation, amygdala, prefrontal cortex, sensory processing, auditory stimuli, tactile stimuli, children and adolescents, top-down control
MeSH terms
Autism Spectrum Disorder, Acoustic Stimulation, Adolescent, Amygdala, Arousal, Child, Female, Generalization, Psychological, Habituation, Psychophysiologic, Humans, Magnetic Resonance Imaging, Male, Touch, Case-Control Studies, Prefrontal Cortex, Central Nervous System Sensitization

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