Age-related changes in neural responses to sensory stimulation in autism: a cross-sectional study

Melis E Cakar; Kaitlin K Cummings; Susan Y Bookheimer; Mirella Dapretto; Shulamite A Green

doi:10.1186/s13229-023-00571-4

Age-related changes in neural responses to sensory stimulation in autism: a cross-sectional study

Mol Autism. 2023 Oct 11;14(1):38. doi: 10.1186/s13229-023-00571-4.

Authors

Melis E Cakar¹, Kaitlin K Cummings², Susan Y Bookheimer^{3

4}, Mirella Dapretto^{3

4}, Shulamite A Green^{3

4}

Affiliations

¹ Neuroscience Interdepartmental Program, Ahmanson Lovelace Brain Mapping Center, University of California Los Angeles, 660 Charles E. Young Drive South, Los Angeles, CA, 90095, USA. cakarm@g.ucla.edu.
² Department of Psychology and Neuroscience, The University of North Carolina at Chapel Hill, Chapel Hill, USA.
³ Department of Psychiatry and Biobehavioral Sciences, University of California Los Angeles, Los Angeles, USA.
⁴ Jane and Terry Semel Institute for Neuroscience and Human Behavior, University of California Los Angeles, Los Angeles, USA.

Abstract

Background: Sensory over-responsivity (SOR) is an impairing sensory processing challenge in autism spectrum disorder (ASD) which shows heterogenous developmental trajectories and appears to improve into adulthood in some but not all autistic individuals. However, the neural mechanisms underlying interindividual differences in these trajectories are currently unknown.

Methods: Here, we used functional magnetic resonance imaging (fMRI) to investigate the association between age and neural activity linearly and nonlinearly in response to mildly aversive sensory stimulation as well as how SOR severity moderates this association. Participants included 52 ASD (14F) and 41 (13F) typically developing (TD) youth, aged 8.6-18.0 years.

Results: We found that in pre-teens, ASD children showed widespread activation differences in sensorimotor, frontal and cerebellar regions compared to TD children, while there were fewer differences between ASD and TD teens. In TD youth, older age was associated with less activation in the prefrontal cortex. In contrast, in ASD youth, older age was associated with more engagement of sensory integration and emotion regulation regions. In particular, orbitofrontal and medial prefrontal cortices showed a nonlinear relationship with age in ASD, with an especially steep increase in sensory-evoked neural activity during the mid-to-late teen years. There was also an interaction between age and SOR severity in ASD youth such that these age-related trends were more apparent in youth with higher SOR.

Limitations: The cross-sectional design limits causal interpretations of the data. Future longitudinal studies will be instrumental in determining how prefrontal engagement and SOR co-develop across adolescence.

Conclusions: Our results suggest that enhanced recruitment of prefrontal regions may underlie age-related decreases in SOR for a subgroup of ASD youth.

Keywords: Autism spectrum disorder; Development; Neural activity; Sensory over-responsivity; Sensory processing; fMRI.

Publication types

Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural

MeSH terms

Adolescent
Autism Spectrum Disorder*
Autistic Disorder* / diagnostic imaging
Cerebellum
Child
Cross-Sectional Studies
Humans
Magnetic Resonance Imaging / methods
Prefrontal Cortex / diagnostic imaging

Abstract

Publication types

MeSH terms

Grants and funding