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

IF 2.6 3区 医学 Q2 BEHAVIORAL SCIENCES Frontiers in Integrative Neuroscience Pub Date : 2024-05-14 DOI:10.3389/fnint.2024.1359099
Olivia Surgent, Jose Guerrero-Gonzalez, Douglas C. Dean, Nagesh Adluru, Gregory R. Kirk, Steven R. Kecskemeti, Andrew L. Alexander, James J. Li, Brittany G. Travers
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Abstract

IntroductionMaximal 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.MethodsUsing 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).ResultsIn 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.DiscussionTogether, 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.
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自闭症儿童最大握力的微结构神经相关性:皮质-小脑网络和注意力缺陷/多动症特征的作用
导言最大握力是衡量一个人的手在挤压物体时能产生多大力量的指标,它可能是了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,自闭症患者的握力可能特别值得关注。虽然在成年人群中发现了自闭症特异性的握力-脑力关系差异,但当自闭症和非自闭症群体的握力在行为上相似时,这种握力-脑力关系的差异有可能在更早的年龄就已经存在。此外,这种神经差异可能会导致后来在青少年时期出现诊断性群体握力差异。本研究试图探讨这种可能性,同时还探讨握力是否能阐明自闭症患者表型异质性的神经运动来源。方法本研究采用高分辨率、多壳扩散和定量 R1 弛豫测量成像技术,对 68 名自闭症儿童和 70 名非自闭症(神经典型)儿童(6-11 岁)的本体感觉输入、侧向抓握、皮质-小脑和皮质脊髓网络中与感觉运动相关的关键白质通路的变化如何与握力的个体差异相关联进行了研究。结果在这两组儿童中,结果显示较强的握力与较高的本体感觉输入、侧向抓握和皮质脊髓(但不是皮质-小脑修饰)分数各向异性和 R1 相关,这些间接测量与较强的微结构一致性和髓鞘化增加一致。在这些握脑关系中未观察到诊断性群体差异,但自闭症群体表现出更大的变异性,尤其是在皮质-小脑修饰指数方面。对自闭症群体内部变异性的研究显示,注意力缺陷/多动症(ADHD)的特征调节了握力与外侧抓握网络的前运动-初级运动束和皮质-小脑网络束的分数各向异性和R1松弛度之间的关系。讨论这项研究表明,虽然学龄自闭症儿童和非自闭症儿童握力的基本要素相似,但自闭症儿童握力的神经机制可能还取决于是否存在多动症特征。具体来说,小脑修饰网络被认为在完善和优化运动指令方面发挥着作用,该网络更强、更连贯的连接可能会导致具有较多多多动症特征的儿童握力更强,而具有较少多动症特征的儿童握力较弱,而非自闭症儿童的握力则没有差异。虽然还需要未来的研究来了解这些发现是否会扩展到握力以外的其他运动任务,但这些结果对于了解自闭症儿童神经运动控制的生物学基础具有重要意义,并强调了在评估自闭症患者大脑与行为关系时评估并发症的重要性。
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来源期刊
Frontiers in Integrative Neuroscience
Frontiers in Integrative Neuroscience Neuroscience-Cellular and Molecular Neuroscience
CiteScore
4.60
自引率
2.90%
发文量
148
审稿时长
14 weeks
期刊介绍: Frontiers in Integrative Neuroscience publishes rigorously peer-reviewed research that synthesizes multiple facets of brain structure and function, to better understand how multiple diverse functions are integrated to produce complex behaviors. Led by an outstanding Editorial Board of international experts, this multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics, clinicians and the public worldwide. Our goal is to publish research related to furthering the understanding of the integrative mechanisms underlying brain functioning across one or more interacting levels of neural organization. In most real life experiences, sensory inputs from several modalities converge and interact in a manner that influences perception and actions generating purposeful and social behaviors. The journal is therefore focused on the primary questions of how multiple sensory, cognitive and emotional processes merge to produce coordinated complex behavior. It is questions such as this that cannot be answered at a single level – an ion channel, a neuron or a synapse – that we wish to focus on. In Frontiers in Integrative Neuroscience we welcome in vitro or in vivo investigations across the molecular, cellular, and systems and behavioral level. Research in any species and at any stage of development and aging that are focused at understanding integration mechanisms underlying emergent properties of the brain and behavior are welcome.
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