Functional connectivity of the sensorimotor cerebellum in autism: associations with sensory over-responsivity

Melis E Cakar; Nana J Okada; Kaitlin K Cummings; Jiwon Jung; Susan Y Bookheimer; Mirella Dapretto; Shulamite A Green

doi:10.3389/fpsyt.2024.1337921

Functional connectivity of the sensorimotor cerebellum in autism: associations with sensory over-responsivity

Front Psychiatry. 2024 Mar 25:15:1337921. doi: 10.3389/fpsyt.2024.1337921. eCollection 2024.

Authors

Melis E Cakar¹, Nana J Okada^{2

3

4}, Kaitlin K Cummings^{3

4

5}, Jiwon Jung^{3

4}, Susan Y Bookheimer^{3

4}, Mirella Dapretto^{3

4}, Shulamite A Green^{3

4}

Affiliations

¹ Neuroscience Interdepartmental Program, University of California Los Angeles, Los Angeles, CA, United States.
² Department of Psychology, Harvard Medical School, Boston, MA, United States.
³ Department of Psychiatry and Biobehavioral Sciences, University of California Los Angeles, Los Angeles, CA, United States.
⁴ Jane and Terry Semel Institute for Neuroscience and Human Behavior, University of California Los Angeles, Los Angeles, CA, United States.
⁵ Department of Psychology and Neuroscience, The University of North Carolina at Chapel Hill, Chapel Hill, NC, United States.

Abstract

The cerebellum has been consistently shown to be atypical in autism spectrum disorder (ASD). However, despite its known role in sensorimotor function, there is limited research on its association with sensory over-responsivity (SOR), a common and impairing feature of ASD. Thus, this study sought to examine functional connectivity of the sensorimotor cerebellum in ASD compared to typically developing (TD) youth and investigate whether cerebellar connectivity is associated with SOR. Resting-state functional connectivity of the sensorimotor cerebellum was examined in 54 ASD and 43 TD youth aged 8-18 years. Using a seed-based approach, connectivity of each sensorimotor cerebellar region (defined as lobules I-IV, V-VI and VIIIA&B) with the whole brain was examined in ASD compared to TD youth, and correlated with parent-reported SOR severity. Across all participants, the sensorimotor cerebellum was functionally connected with sensorimotor and visual regions, though the three seed regions showed distinct connectivity with limbic and higher-order sensory regions. ASD youth showed differences in connectivity including atypical connectivity within the cerebellum and increased connectivity with hippocampus and thalamus compared to TD youth. More severe SOR was associated with stronger connectivity with cortical regions involved in sensory and motor processes and weaker connectivity with cognitive and socio-emotional regions, particularly prefrontal cortex. These results suggest that atypical cerebellum function in ASD may play a role in sensory challenges in autism.

Keywords: autism spectrum disorder; cerebellum; fMRI; functional connectivity; sensorimotor; sensory over-responsivity.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by grants from the Simons Foundation Autism Research Initiative (Grant Number 345389), National Institute of Child Health and Human Development (P50 HD055784), and the National Institute of Mental Health (R01 MH100028; R01 MH117982; K08 MH112871; R01 MH124977). For generous support, the authors also wish to thank the Brain Mapping Medical Research Organization, Brain Mapping Support Foundation, Pierson-Lovelace Foundation, The Ahmanson Foundation, William M. and Linda R. Dietel Philanthropic Fund at the Northern Piedmont Community Foundation, Tamkin Foundation, Jennifer Jones-Simon Foundation, Capital Group Companies Charitable Foundation, Robson Family and Northstar Fund. The project described was supported by Grant Numbers RR12169, RR13642, and RR00865 from the National Center for Research Resources (NCRR), a component of the National Institutes of Health (NIH); its contents are solely the responsibility of the authors and do not necessarily represent the official views of NCR or NIH. The funding sources and organizations listed above had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. These research efforts were conducted in part under the auspices of The Help Group-UCLA Autism Research Alliance, which contributed to participant recruitment.