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自闭症儿童最大握力的微观结构神经关联:皮质-小脑网络及注意力缺陷/多动障碍特征的作用

Microstructural neural correlates of maximal grip strength in autistic children: the role of the cortico-cerebellar network and attention-deficit/hyperactivity disorder features.

作者信息

Surgent Olivia, Guerrero-Gonzalez Jose, Dean Douglas C, Adluru Nagesh, Kirk Gregory R, Kecskemeti Steven R, Alexander Andrew L, Li James J, Travers Brittany G

机构信息

Waisman Center, University of Wisconsin-Madison, Madison, WI, United States.

Neuroscience Training Program, University of Wisconsin-Madison, Madison, WI, United States.

出版信息

Front Integr Neurosci. 2024 May 14;18:1359099. doi: 10.3389/fnint.2024.1359099. eCollection 2024.

Abstract

INTRODUCTION

Maximal grip strength, a measure of how much force a person's hand can generate when squeezing an object, may be an effective method for understanding potential neurobiological differences during motor tasks. Grip strength in autistic individuals may be of particular interest due to its unique developmental trajectory. While autism-specific differences in grip-brain relationships have been found in adult populations, it is possible that such differences in grip-brain relationships may be present at earlier ages when grip strength is behaviorally similar in autistic and non-autistic groups. Further, such neural differences may lead to the later emergence of diagnostic-group grip differences in adolescence. The present study sought to examine this possibility, while also examining if grip strength could elucidate the neuro-motor sources of phenotypic heterogeneity commonly observed within autism.

METHODS

Using high resolution, multi-shell diffusion, and quantitative R1 relaxometry imaging, this study examined how variations in key sensorimotor-related white matter pathways of the proprioception input, lateral grasping, cortico-cerebellar, and corticospinal networks were associated with individual variations in grip strength in 68 autistic children and 70 non-autistic (neurotypical) children (6-11 years-old).

RESULTS

In both groups, results indicated that stronger grip strength was associated with higher proprioceptive input, lateral grasping, and corticospinal (but not cortico-cerebellar modification) fractional anisotropy and R1, indirect measures concordant with stronger microstructural coherence and increased myelination. Diagnostic group differences in these grip-brain relationships were not observed, but the autistic group exhibited more variability particularly in the cortico-cerebellar modification indices. An examination into the variability within the autistic group revealed that attention-deficit/hyperactivity disorder (ADHD) features moderated the relationships between grip strength and both fractional anisotropy and R1 relaxometry in the premotor-primary motor tract of the lateral grasping network and the cortico-cerebellar network tracts. Specifically, in autistic children with elevated ADHD features (60% of the autistic group) stronger grip strength was related to higher fractional anisotropy and R1 of the cerebellar modification network (stronger microstructural coherence and more myelin), whereas the opposite relationship was observed in autistic children with reduced ADHD features.

DISCUSSION

Together, this work suggests that while the foundational elements of grip strength are similar across school-aged autistic and non-autistic children, neural mechanisms of grip strength within autistic children may additionally depend on the presence of ADHD features. Specifically, stronger, more coherent connections of the cerebellar modification network, which is thought to play a role in refining and optimizing motor commands, may lead to stronger grip in children with more ADHD features, weaker grip in children with fewer ADHD features, and no difference in grip in non-autistic children. While future research is needed to understand if these findings extend to other motor tasks beyond grip strength, these results have implications for understanding the biological basis of neuromotor control in autistic children and emphasize the importance of assessing co-occurring conditions when evaluating brain-behavior relationships in autism.

摘要

引言

最大握力是衡量一个人在挤压物体时手部能够产生多大力量的指标,它可能是理解运动任务中潜在神经生物学差异的有效方法。由于其独特的发育轨迹,自闭症个体的握力可能特别受关注。虽然在成年人群中已经发现了握力与大脑关系中特定于自闭症的差异,但当自闭症和非自闭症组的握力在行为上相似时,这种握力与大脑关系的差异可能在更早的年龄就已存在。此外,这种神经差异可能导致在青春期后期出现诊断组之间的握力差异。本研究旨在探讨这种可能性,同时研究握力是否能够阐明自闭症中常见的表型异质性的神经运动来源。

方法

本研究使用高分辨率、多壳扩散和定量R1弛豫测量成像技术,研究了68名自闭症儿童和70名非自闭症(神经典型)儿童(6 - 11岁)中本体感觉输入、侧向抓握、皮质 - 小脑和皮质脊髓网络等关键感觉运动相关白质通路的变化与握力个体差异之间的关联。

结果

在两组中,结果表明更强的握力与更高的本体感觉输入、侧向抓握和皮质脊髓(而非皮质 - 小脑调节)分数各向异性和R1相关,这些间接测量结果与更强的微观结构连贯性和增加的髓鞘形成一致。未观察到这些握力与大脑关系中的诊断组差异,但自闭症组表现出更大的变异性,特别是在皮质 - 小脑调节指数方面。对自闭症组内变异性的检查发现,注意力缺陷多动障碍(ADHD)特征调节了握力与侧向抓握网络和皮质 - 小脑网络束的运动前 - 初级运动束中的分数各向异性和R1弛豫测量之间的关系。具体而言,在具有较高ADHD特征的自闭症儿童(占自闭症组的60%)中,更强的握力与小脑调节网络更高的分数各向异性和R1相关(更强的微观结构连贯性和更多的髓鞘),而在具有较低ADHD特征的自闭症儿童中观察到相反的关系。

讨论

总体而言,这项工作表明,虽然学龄期自闭症和非自闭症儿童握力的基础要素相似,但自闭症儿童握力的神经机制可能还取决于ADHD特征的存在。具体来说,被认为在细化和优化运动指令中起作用的小脑调节网络更强、更连贯的连接,可能导致具有更多ADHD特征的儿童握力更强,具有较少ADHD特征的儿童握力较弱,而非自闭症儿童的握力无差异。虽然需要未来的研究来了解这些发现是否扩展到握力之外的其他运动任务,但这些结果对于理解自闭症儿童神经运动控制的生物学基础具有重要意义,并强调在评估自闭症患者的脑 - 行为关系时评估共病情况的重要性。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fe18/11130426/d9e9ead3141a/fnint-18-1359099-g001.jpg

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