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Published Online: 24 June 2019

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

Shulamite A. Green, Ph.D. [email protected], Leanna Hernandez, Ph.D., Katherine E. Lawrence, B.A., Janelle Liu, B.A., Tawny Tsang, Ph.D., Jillian Yeargin, M.A., Kaitlin Cummings, B.A., Elizabeth Laugeson, Psy.D., Mirella Dapretto, Ph.D., and Susan Y. Bookheimer, Ph.D.Authors Info & Affiliations
Publication: American Journal of Psychiatry
Volume 176, Number 12
https://doi.org/10.1176/appi.ajp.2019.18121333
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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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Information & Authors

Information

Published In

Go to American Journal of Psychiatry
Go to American Journal of Psychiatry
American Journal of Psychiatry
Volume 176 • Number 12 • December 01, 2019
Pages: 1010 - 1020
PubMed: 31230465

History

Received: 3 December 2018
Revision received: 10 March 2019
Revision received: 8 April 2019
Accepted: 22 April 2019
Published online: 24 June 2019
Published in print: December 01, 2019

Keywords

  1. Autism
  2. Biological Markers

Authors

Details

Shulamite A. Green, Ph.D. [email protected]
The Jane and Terry Semel Institute of Neuroscience and Human Behavior, Psychiatry and Biobehavioral Sciences, University of California Los Angeles (Green, Hernandez, Lawrence, Liu, Yeargin, Cummings, Laugeson, Dapretto, Bookheimer); Yale Child Study Center, Yale University, New Haven, Conn. (Tsang); and the Help Group–UCLA Autism Research Alliance, Los Angeles (Laugeson).
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Leanna Hernandez, Ph.D.
The Jane and Terry Semel Institute of Neuroscience and Human Behavior, Psychiatry and Biobehavioral Sciences, University of California Los Angeles (Green, Hernandez, Lawrence, Liu, Yeargin, Cummings, Laugeson, Dapretto, Bookheimer); Yale Child Study Center, Yale University, New Haven, Conn. (Tsang); and the Help Group–UCLA Autism Research Alliance, Los Angeles (Laugeson).
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Katherine E. Lawrence, B.A.
The Jane and Terry Semel Institute of Neuroscience and Human Behavior, Psychiatry and Biobehavioral Sciences, University of California Los Angeles (Green, Hernandez, Lawrence, Liu, Yeargin, Cummings, Laugeson, Dapretto, Bookheimer); Yale Child Study Center, Yale University, New Haven, Conn. (Tsang); and the Help Group–UCLA Autism Research Alliance, Los Angeles (Laugeson).
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Janelle Liu, B.A.
The Jane and Terry Semel Institute of Neuroscience and Human Behavior, Psychiatry and Biobehavioral Sciences, University of California Los Angeles (Green, Hernandez, Lawrence, Liu, Yeargin, Cummings, Laugeson, Dapretto, Bookheimer); Yale Child Study Center, Yale University, New Haven, Conn. (Tsang); and the Help Group–UCLA Autism Research Alliance, Los Angeles (Laugeson).
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Tawny Tsang, Ph.D.
The Jane and Terry Semel Institute of Neuroscience and Human Behavior, Psychiatry and Biobehavioral Sciences, University of California Los Angeles (Green, Hernandez, Lawrence, Liu, Yeargin, Cummings, Laugeson, Dapretto, Bookheimer); Yale Child Study Center, Yale University, New Haven, Conn. (Tsang); and the Help Group–UCLA Autism Research Alliance, Los Angeles (Laugeson).
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Jillian Yeargin, M.A.
The Jane and Terry Semel Institute of Neuroscience and Human Behavior, Psychiatry and Biobehavioral Sciences, University of California Los Angeles (Green, Hernandez, Lawrence, Liu, Yeargin, Cummings, Laugeson, Dapretto, Bookheimer); Yale Child Study Center, Yale University, New Haven, Conn. (Tsang); and the Help Group–UCLA Autism Research Alliance, Los Angeles (Laugeson).
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Kaitlin Cummings, B.A.
The Jane and Terry Semel Institute of Neuroscience and Human Behavior, Psychiatry and Biobehavioral Sciences, University of California Los Angeles (Green, Hernandez, Lawrence, Liu, Yeargin, Cummings, Laugeson, Dapretto, Bookheimer); Yale Child Study Center, Yale University, New Haven, Conn. (Tsang); and the Help Group–UCLA Autism Research Alliance, Los Angeles (Laugeson).
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Elizabeth Laugeson, Psy.D.
The Jane and Terry Semel Institute of Neuroscience and Human Behavior, Psychiatry and Biobehavioral Sciences, University of California Los Angeles (Green, Hernandez, Lawrence, Liu, Yeargin, Cummings, Laugeson, Dapretto, Bookheimer); Yale Child Study Center, Yale University, New Haven, Conn. (Tsang); and the Help Group–UCLA Autism Research Alliance, Los Angeles (Laugeson).
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Mirella Dapretto, Ph.D.
The Jane and Terry Semel Institute of Neuroscience and Human Behavior, Psychiatry and Biobehavioral Sciences, University of California Los Angeles (Green, Hernandez, Lawrence, Liu, Yeargin, Cummings, Laugeson, Dapretto, Bookheimer); Yale Child Study Center, Yale University, New Haven, Conn. (Tsang); and the Help Group–UCLA Autism Research Alliance, Los Angeles (Laugeson).
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Susan Y. Bookheimer, Ph.D.
The Jane and Terry Semel Institute of Neuroscience and Human Behavior, Psychiatry and Biobehavioral Sciences, University of California Los Angeles (Green, Hernandez, Lawrence, Liu, Yeargin, Cummings, Laugeson, Dapretto, Bookheimer); Yale Child Study Center, Yale University, New Haven, Conn. (Tsang); and the Help Group–UCLA Autism Research Alliance, Los Angeles (Laugeson).
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Notes

Send correspondence to Dr. Green ([email protected]).

Funding Information

Supported by grants from the Simons Foundation Autism Research Initiative (grant 345389), the National Institute of Child Health and Human Development (grant P50 HD055784), and NIMH (grants R01MH100028 and K08 MH112871). The authors also thank the following for their generous support: the Brain Mapping Medical Research Organization, the Brain Mapping Support Foundation, the Pierson-Lovelace Foundation, the Ahmanson Foundation, the William M. and Linda R. Dietel Philanthropic Fund at the Northern Piedmont Community Foundation, the Tamkin Foundation, the Jennifer Jones-Simon Foundation, the Capital Group Companies Charitable Foundation, the Robson Family, and the Northstar Fund. The project was also supported by grants RR12169, RR13642, and RR00865 from the NIH National Center for Research Resources.Dr. Laugeson receives royalties from Wiley and Taylor & Francis. The other authors report no financial relationships with commercial interests.

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