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

IF 4.1 2区 医学 Q1 CLINICAL NEUROLOGY Journal of Neurodevelopmental Disorders Pub Date : 2024-01-02 DOI:10.1186/s11689-023-09513-w
Jamie Wren-Jarvis, Rachel Powers, Maia C. Lazerwitz, Jaclyn Xiao, Lanya T. Cai, Hannah L. Choi, Annie Brandes-Aitken, Robyn Chu, Kaitlyn J. Trimarchi, Rafael D. Garcia, Mikaela A. Rowe, Mary C. Steele, Elysa J. Marco, Pratik Mukherjee
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Abstract

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. 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. 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. White matter microstructure is related to affective behavior in children with SOR.
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感觉过度反应儿童的白质微结构与情感行为有关
感觉处理功能障碍(SPD)与学龄儿童白质(WM)微结构的改变有关。感觉过度反应(SOR)是 SPD 的一种表现形式,至少有 2.5% 的儿童会受到影响,并对学习和心理健康造成严重不良影响。然而,目前还没有利用弥散核磁共振成像(dMRI)等微观结构成像技术对 SOR 进行深入研究。由于 SOR 涉及对外界刺激的超敏反应,我们测试了这样一种假设:SOR 儿童需要以优异的 WM 微结构完整性为形式的补偿性神经可塑性来防止内化行为,而那些 WM 微结构受损的儿童则容易出现躯体化和抑郁。研究人员对 8-12 岁有神经发育问题的儿童进行了 SOR 评估,评估采用了全面的结构化临床评估方法,即 "感觉处理三维评估",并进行了 3 特斯拉磁共振成像和多壳多波段 dMRI 检查。研究人员使用基于束的空间统计方法测量了全球 WM 和 19 个选定 WM 束的弥散张量成像(DTI)和神经元定向弥散与密度成像(NODDI)指标。在 SOR 组和有神经发育问题但没有 SOR 的匹配儿童中,计算了 DTI 和 NODDI 指标与第三版儿童行为评估系统(BASC-3)中躯体化和情绪障碍指标的相关性。在 SOR 组,全局 WM 分数各向异性(FA)与躯体化和情绪障碍呈负相关,而在非 SOR 组则不然。在 SOR 儿童中还观察到,径向扩散率(RD)和自由水分数(FISO)与躯体化呈正相关,在大多数情况下与情绪障碍呈正相关。这些影响在患有 SOR 的男孩中非常明显,而对女孩的研究则效果不佳。受影响最严重的白质是内侧半月板和内囊感觉束,但在许多大脑、小脑和脑干束中也观察到 SOR 的影响。白质微结构与 SOR 儿童的情感行为有关。
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来源期刊
CiteScore
7.60
自引率
4.10%
发文量
58
审稿时长
>12 weeks
期刊介绍: Journal of Neurodevelopmental Disorders is an open access journal that integrates current, cutting-edge research across a number of disciplines, including neurobiology, genetics, cognitive neuroscience, psychiatry and psychology. The journal’s primary focus is on the pathogenesis of neurodevelopmental disorders including autism, fragile X syndrome, tuberous sclerosis, Turner Syndrome, 22q Deletion Syndrome, Prader-Willi and Angelman Syndrome, Williams syndrome, lysosomal storage diseases, dyslexia, specific language impairment and fetal alcohol syndrome. With the discovery of specific genes underlying neurodevelopmental syndromes, the emergence of powerful tools for studying neural circuitry, and the development of new approaches for exploring molecular mechanisms, interdisciplinary research on the pathogenesis of neurodevelopmental disorders is now increasingly common. Journal of Neurodevelopmental Disorders provides a unique venue for researchers interested in comparing and contrasting mechanisms and characteristics related to the pathogenesis of the full range of neurodevelopmental disorders, sharpening our understanding of the etiology and relevant phenotypes of each condition.
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