Sadiq Alishba, Funk Adrian T, Waugh Jeff L
Division of Pediatric Neurology, Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX, United States.
bioRxiv. 2024 Dec 17:2024.12.13.628392. doi: 10.1101/2024.12.13.628392.
The striatum is divided into two interdigitated tissue compartments, the striosome and matrix. These compartments exhibit distinct anatomical, neurochemical, and pharmacological characteristics and have separable roles in motor and mood functions. Little is known about the functions of these compartments in humans. While compartment-specific roles in neuropsychiatric diseases have been hypothesized, they have yet to be directly tested. Investigating compartment-specific functions is crucial for understanding the symptoms produced by striatal injury, and to elucidating the roles of each compartment in healthy human skills and behaviors. We mapped the functional networks of striosome and matrix in humans . We utilized a diverse cohort of 674 healthy adults, derived from the Human Connectome Project, including all subjects with complete diffusion and functional MRI data and excluding subjects with substance use disorders. We identified striatal voxels with striosome-like and matrix-like structural connectivity using probabilistic diffusion tractography. We then investigated resting state functional connectivity (rsFC) using these compartment-like voxels as seeds. We found widespread differences in rsFC between striosome-like and matrix-like seeds ( < 0.05, FWE corrected for multiple comparisons), suggesting that striosome and matrix occupy distinct functional networks. Slightly shifting seed voxel locations (<4 mm) eliminated these rsFC differences, underscoring the anatomic precision of these networks. Striosome-seeded networks exhibited ipsilateral dominance; matrix-seeded networks had contralateral dominance. Next, we assessed compartment-specific engagement with the triple-network model (default mode, salience, and frontoparietal networks). Striosome-like voxels dominated rsFC with the default mode network bilaterally. The anterior insula (a primary node in the salience network) had higher rsFC with striosome-like voxels. The inferior and middle frontal cortices (primary nodes, frontoparietal network) had stronger rsFC with matrix-like voxels on the left, and striosome-like voxels on the right. Since striosome-like and matrix-like voxels occupy highly segregated rsFC networks, striosome-selective injury may produce different motor, cognitive, and behavioral symptoms than matrix-selective injury. Moreover, compartment-specific rsFC abnormalities may be identifiable before disease-related structural injuries are evident. Localizing rsFC differences provides an anatomic substrate for understanding how the tissue-level organization of the striatum underpins complex brain networks, and how compartment-specific injury may contribute to the symptoms of specific neuropsychiatric disorders.
纹状体被分为两个相互交错的组织区室，即纹状体小体和基质。这些区室具有不同的解剖学、神经化学和药理学特征，并且在运动和情绪功能中发挥着不同的作用。关于这些区室在人类中的功能，我们了解得很少。虽然已经有人假设它们在神经精神疾病中具有特定区室的作用，但尚未得到直接验证。研究特定区室的功能对于理解纹状体损伤所产生的症状，以及阐明每个区室在健康人类技能和行为中的作用至关重要。我们绘制了人类纹状体小体和基质的功能网络。我们利用了来自人类连接体项目的674名健康成年人的多样化队列，包括所有具有完整扩散和功能磁共振成像数据的受试者，并排除了有物质使用障碍的受试者。我们使用概率性扩散束描记法识别具有类似纹状体小体和类似基质结构连接的纹状体体素。然后，我们以这些类似区室的体素为种子，研究静息态功能连接（rsFC）。我们发现类似纹状体小体和类似基质的种子之间的rsFC存在广泛差异（<0.05，经多重比较校正的FWE），这表明纹状体小体和基质占据不同的功能网络。稍微移动种子体素位置（<4毫米）就消除了这些rsFC差异，突出了这些网络的解剖学精确性。以纹状体小体为种子的网络表现出同侧优势；以基质为种子的网络具有对侧优势。接下来，我们评估了特定区室与三网络模型（默认模式、突显和额顶叶网络）的参与情况。类似纹状体小体的体素在双侧与默认模式网络的rsFC中占主导地位。前岛叶（突显网络中的一个主要节点）与类似纹状体小体的体素具有更高的rsFC。额下回和额中回（额顶叶网络的主要节点）在左侧与类似基质的体素具有更强的rsFC，在右侧与类似纹状体小体的体素具有更强的rsFC。由于类似纹状体小体和类似基质的体素占据高度隔离的rsFC网络，纹状体小体选择性损伤可能会产生与基质选择性损伤不同的运动、认知和行为症状。此外，在与疾病相关的结构损伤明显之前，可能就能识别出特定区室的rsFC异常。定位rsFC差异为理解纹状体的组织水平组织如何支撑复杂的脑网络，以及特定区室损伤如何导致特定神经精神疾病的症状提供了解剖学基础。
