Hassanzadeh-Behbahani Shiva, Lan Zhou, Zekelman Leo, Rushmore R Jarrett, Chen Yuqian, Xue Tengfei, Cetin-Karayumak Suheyla, Pieper Steve, Tie Yanmei, Yeterian Edward, Golby Alexandra J, Makris Nikos, Zhang Fan, Rathi Yogesh, O'Donnell Lauren J
Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.
Center for Clinical Investigation, Channing Division of Network Medicine, Brigham and Women's Hospital, Boston, Massachusetts, USA.
bioRxiv. 2025 Aug 1:2025.07.31.666959. doi: 10.1101/2025.07.31.666959.
While deeper white matter connections, such as the arcuate fasciculus and frontal aslant tract, are well known for their role in language and show leftward asymmetries in adults, the contribution of the short-range cortico-cortical superficial white matter (SWM) connections remains less understood. In this preregistered study, we examined white matter connections of Broca's area and its right hemisphere homolog in early adolescents and young adults using two large, publicly available datasets: the Adolescent Brain Cognitive Development Study and the Human Connectome Project Young Adult Study, totaling over 10,000 participants. We anatomically curated the O'Donnell Research Group (ORG) tractography atlas to identify SWM fiber clusters intersecting Broca's area (pars opercularis and pars triangularis), confirmed through expert visual inspection. We investigated the microstructure, structural connectivity, and lateralization of Broca's area SWM and its relationship with language performance (Picture Vocabulary and Oral Reading Recognition assessments), in comparison to the deeper white matter connections of the frontal aslant tract and arcuate fasciculus. The arcuate fasciculus demonstrated the strongest and most consistent leftward lateralization of both microstructure (fractional anisotropy, FA) and structural connectivity (number of streamlines, NoS), with structure-function associations that were bilateral in adolescents and left-dominant in adults. Interestingly, despite weaker lateralization than the arcuate fasciculus, both the SWM and the frontal aslant tract demonstrated comparable associations with language performance. The frontal aslant tract showed greater leftward lateralization (FA and NoS) with age and was bilaterally associated with language performance, particularly in adolescents. Compared to these deeper tracts, Broca's area SWM demonstrated left-lateralized FA and right-lateralized NoS in both adolescents and adults, with stronger FA lateralization in adults. Bilateral SWM FA and NoS were significantly associated with language performance in both hemispheres and age groups. Overall, these results suggest that Broca's area SWM may support language in a more bilaterally distributed manner and highlight the importance of considering SWM connections in studies of language development and neurosurgical planning.
虽然诸如弓状束和额叶斜束等更深层的白质连接因其在语言中的作用而广为人知,并且在成年人中表现出左侧不对称,但短程皮质-皮质浅层白质(SWM)连接的贡献仍鲜为人知。在这项预先注册的研究中,我们使用两个大型公开可用数据集——青少年大脑认知发展研究和人类连接组计划青年成人研究,对青少年早期和青年成人中布洛卡区及其右半球对应区域的白质连接进行了研究,这两个数据集共有超过10000名参与者。我们对奥唐纳研究小组(ORG)的纤维束成像图谱进行了解剖学整理,以识别与布洛卡区(岛盖部和三角部)相交的SWM纤维簇,并通过专家视觉检查进行了确认。与额叶斜束和弓状束的深层白质连接相比,我们研究了布洛卡区SWM的微观结构、结构连接性和侧化及其与语言表现(图片词汇和口头阅读识别评估)的关系。弓状束在微观结构(分数各向异性,FA)和结构连接性(流线数量,NoS)方面均表现出最强且最一致的左侧化,其结构-功能关联在青少年中是双侧的,在成年人中以左侧为主导。有趣的是,尽管SWM和额叶斜束的侧化程度比弓状束弱,但它们与语言表现的关联相当。额叶斜束随着年龄增长表现出更大的左侧化(FA和NoS),并且与语言表现呈双侧关联,尤其是在青少年中。与这些更深层的纤维束相比,布洛卡区SWM在青少年和成年人中均表现出左侧化的FA和右侧化的NoS,成年人中的FA侧化更强。双侧SWM的FA和NoS在两个半球和年龄组中均与语言表现显著相关。总体而言,这些结果表明布洛卡区SWM可能以更双侧分布的方式支持语言,并强调在语言发展研究和神经外科手术规划中考虑SWM连接的重要性。