White matter microstructure of children with sensory over-responsivity is associated with affective behavior

Author:

Wren-Jarvis Jamie,Powers Rachel,Lazerwitz Maia C.,Xiao Jaclyn,Cai Lanya T.,Choi Hannah L.,Brandes-Aitken Annie,Chu Robyn,Trimarchi Kaitlyn J.,Garcia Rafael D.,Rowe Mikaela A.,Steele Mary C.,Marco Elysa J.,Mukherjee PratikORCID

Abstract

Abstract Background Sensory processing dysfunction (SPD) is linked to altered white matter (WM) microstructure in school-age children. Sensory over-responsivity (SOR), a form of SPD, affects at least 2.5% of all children and has substantial deleterious impact on learning and mental health. However, SOR has not been well studied using microstructural imaging such as diffusion MRI (dMRI). Since SOR involves hypersensitivity to external stimuli, we test the hypothesis that children with SOR require compensatory neuroplasticity in the form of superior WM microstructural integrity to protect against internalizing behavior, leaving those with impaired WM microstructure vulnerable to somatization and depression. Methods Children ages 8–12 years old with neurodevelopmental concerns were assessed for SOR using a comprehensive structured clinical evaluation, the Sensory Processing 3 Dimensions Assessment, and underwent 3 Tesla MRI with multishell multiband dMRI. Tract-based spatial statistics was used to measure diffusion tensor imaging (DTI) and neurite orientation dispersion and density imaging (NODDI) metrics from global WM and nineteen selected WM tracts. Correlations of DTI and NODDI measures with measures of somatization and emotional disturbance from the Behavioral Assessment System for Children, 3rd edition (BASC-3), were computed in the SOR group and in matched children with neurodevelopmental concerns but not SOR. Results Global WM fractional anisotropy (FA) is negatively correlated with somatization and with emotional disturbance in the SOR group but not the non-SOR group. Also observed in children with SOR are positive correlations of radial diffusivity (RD) and free water fraction (FISO) with somatization and, in most cases, emotional disturbance. These effects are significant in boys with SOR, whereas the study is underpowered for girls. The most affected white matter are medial lemniscus and internal capsule sensory tracts, although effects of SOR are observed in many cerebral, cerebellar, and brainstem tracts. Conclusion White matter microstructure is related to affective behavior in children with SOR.

Funder

National Institutes of Health

Publisher

Springer Science and Business Media LLC

Subject

Cognitive Neuroscience,Neurology (clinical),Pathology and Forensic Medicine,Pediatrics, Perinatology and Child Health

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