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Research Articles, Neurobiology of Disease

Altered Development of Amygdala-Connected Brain Regions in Males and Females with Autism

Joshua K. Lee, Derek S. Andrews, Arzu Ozturk, Marjorie Solomon, Sally Rogers, David G. Amaral and Christine Wu Nordahl
Journal of Neuroscience 3 August 2022, 42 (31) 6145-6155; DOI: https://doi.org/10.1523/JNEUROSCI.0053-22.2022
Joshua K. Lee
1MIND Institute, University of California Davis School of Medicine, Sacramento, California 95817
2Department of Psychiatry and Behavioral Sciences
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Derek S. Andrews
1MIND Institute, University of California Davis School of Medicine, Sacramento, California 95817
2Department of Psychiatry and Behavioral Sciences
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Arzu Ozturk
3Department of Radiology, University of California Davis School of Medicine, Sacramento, California 95817
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Marjorie Solomon
1MIND Institute, University of California Davis School of Medicine, Sacramento, California 95817
2Department of Psychiatry and Behavioral Sciences
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Sally Rogers
1MIND Institute, University of California Davis School of Medicine, Sacramento, California 95817
2Department of Psychiatry and Behavioral Sciences
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David G. Amaral
1MIND Institute, University of California Davis School of Medicine, Sacramento, California 95817
2Department of Psychiatry and Behavioral Sciences
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Christine Wu Nordahl
1MIND Institute, University of California Davis School of Medicine, Sacramento, California 95817
2Department of Psychiatry and Behavioral Sciences
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Abstract

Altered amygdala development is implicated in the neurobiology of autism, but little is known about the coordinated development of the brain regions directly connected with the amygdala. Here we investigated the volumetric development of an amygdala-connected network, defined as the set of brain regions with monosynaptic connections with the amygdala, in autism from early to middle childhood. A total of 950 longitudinal structural MRI scans were acquired from 282 children (93 female) with autism and 128 children with typical development (61 female) at up to four time points (mean ages: 39, 52, 64, and 137 months, respectively). Volumes from 32 amygdala-connected brain regions were examined using mixed effects multivariate distance matrix regression. The Social Responsiveness Scale-2 was administered to assess degree of autistic traits and social impairments. The amygdala-connected network exhibited persistent diagnostic differences (p values ≤ 0.03) that increased over time (p values ≤ 0.02). These differences were most prominent in autistics with more impacted social functioning at baseline. This pattern was not observed across regions without monosynaptic amygdala connection. We observed qualitative sex differences. In males, the bilateral subgenual anterior cingulate cortices were most affected, while in females the left fusiform and superior temporal gyri were most affected. In conclusion, (1) autism is associated with widespread alterations to the development of brain regions connected with the amygdala, which were associated with autistic social behaviors; and (2) autistic males and females exhibited different patterns of alterations, adding to a growing body of evidence of sex differences in the neurobiology of autism.

SIGNIFICANCE STATEMENT Global patterns of development across brain regions with monosynaptic connection to the amygdala differentiate autism from typical development, and are modulated by social functioning in early childhood. Alterations to brain regions within the amygdala-connected network differed in males and females with autism. Results also indicate larger volumetric differences in regions having monosynaptic connection with the amygdala than in regions without monosynaptic connection.

  • amygdala
  • autism spectrum disorder
  • brain
  • development
  • longitudinal
  • sex difference

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The Journal of Neuroscience: 42 (31)
Journal of Neuroscience
Vol. 42, Issue 31
3 Aug 2022
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Altered Development of Amygdala-Connected Brain Regions in Males and Females with Autism
Joshua K. Lee, Derek S. Andrews, Arzu Ozturk, Marjorie Solomon, Sally Rogers, David G. Amaral, Christine Wu Nordahl
Journal of Neuroscience 3 August 2022, 42 (31) 6145-6155; DOI: 10.1523/JNEUROSCI.0053-22.2022

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Altered Development of Amygdala-Connected Brain Regions in Males and Females with Autism
Joshua K. Lee, Derek S. Andrews, Arzu Ozturk, Marjorie Solomon, Sally Rogers, David G. Amaral, Christine Wu Nordahl
Journal of Neuroscience 3 August 2022, 42 (31) 6145-6155; DOI: 10.1523/JNEUROSCI.0053-22.2022
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Keywords

  • amygdala
  • autism spectrum disorder
  • brain
  • development
  • longitudinal
  • sex difference

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