Structural White Matter Correlates of the Crowding Effect: Insights From a Tractography Study of the Arcuate Fasciculus Post-Hemispherotomy

IF 3.5 2区 医学 Q1 NEUROIMAGING
Justus Bisten, Johannes Grün, Christian Hoppe, Tobias Bauer, Nina R. Held, Renata Rose, Anita Althausen, Juri-Alexander Witt, Valeri Borger, Matthias Schneider, Hartmut Vatter, Christoph Helmstaedter, Alexander Radbruch, Rainer Surges, Thomas Schultz, Theodor Rüber
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This study investigates structural white matter correlates of crowding in the arcuate fasciculus (AF), a key language tract, using hemispherotomy as a unique setting to explore structural reorganization supporting language preservation. We explore two main hypotheses. First, the contralesional right AF undergoes white matter reorganization correlated with preserved language function at the expense of nonverbal abilities following left-hemispheric damage. Second, this reorganization varies with epilepsy etiology, influencing different stages of developmental language lateralization. This retrospective study included individuals post-hemispherotomy and healthy controls. Inclusion criteria were; (1) being a native German speaker, (2) having no MRI contraindication, (3) the ability to undergo approximately 2 h of MRI scans, and (4) the ability to participate in neuropsychological assessments over two consecutive days. Neuroimaging included T1-, T2-, and diffusion-weighted imaging, alongside postoperative neuropsychological assessments, where it was taken as evidence for crowding if verbal IQ exceeded performance IQ by at least 10 points. The AF was reconstructed using advanced tractography, and CoBundleMAP was used to compare morphologically corresponding AF subsections. Statistical significance was set at <span></span><math>\n <semantics>\n <mrow>\n <mi>p</mi>\n <mo>&lt;</mo>\n <mn>0.05</mn>\n </mrow>\n <annotation>$$ p&lt;0.05 $$</annotation>\n </semantics></math>, with correction for multiple comparisons applied across contiguous tract sections using Threshold-Free Cluster Enhancement. The final cohort comprised 22 individuals post-hemispherotomy (median age: <span></span><math>\n <semantics>\n <mrow>\n <mn>20.4</mn>\n </mrow>\n <annotation>$$ 20.4 $$</annotation>\n </semantics></math> years, range: <span></span><math>\n <semantics>\n <mrow>\n <mn>12.3</mn>\n <mo>−</mo>\n <mn>43.9</mn>\n </mrow>\n <annotation>$$ 12.3-43.9 $$</annotation>\n </semantics></math>; 55% female; 55% with left-sided surgeries) and 20 healthy controls (median age: <span></span><math>\n <semantics>\n <mrow>\n <mn>23.8</mn>\n </mrow>\n <annotation>$$ 23.8 $$</annotation>\n </semantics></math> years, range: <span></span><math>\n <semantics>\n <mrow>\n <mn>15.5</mn>\n <mo>−</mo>\n <mn>54.0</mn>\n </mrow>\n <annotation>$$ 15.5-54.0 $$</annotation>\n </semantics></math>; 55% female). Crowding was associated with significantly higher fractional anisotropy (FA) in the AF (<span></span><math>\n <semantics>\n <mrow>\n <mi>p</mi>\n <mo>=</mo>\n <mn>0.015</mn>\n </mrow>\n <annotation>$$ p=0.015 $$</annotation>\n </semantics></math>, Cohen's <span></span><math>\n <semantics>\n <mrow>\n <mi>d</mi>\n <mo>=</mo>\n <mn>1.69</mn>\n </mrow>\n <annotation>$$ d=1.69 $$</annotation>\n </semantics></math>), but only observed in individuals with left-sided hemispherotomy, localized to a subsection between Geschwind's territory and Wernicke's area (<span></span><math>\n <semantics>\n <mrow>\n <msub>\n <mi>p</mi>\n <mtext>corrected</mtext>\n </msub>\n <mo>=</mo>\n <mn>0.02</mn>\n </mrow>\n <annotation>$$ {p}_{\\mathrm{corrected}}=0.02 $$</annotation>\n </semantics></math>). This region also displayed significantly higher normalized FA in AF of individuals with congenital etiology and crowding compared to acquired etiology and no crowding (<span></span><math>\n <semantics>\n <mrow>\n <msub>\n <mi>p</mi>\n <mtext>corrected</mtext>\n </msub>\n <mo>=</mo>\n <mn>0.0189</mn>\n </mrow>\n <annotation>$$ {p}_{\\mathrm{corrected}}=0.0189 $$</annotation>\n </semantics></math>). This study identifies previously unreported neural correlates of crowding in right contralesional AF of individuals post-hemispherotomy and highlights specific AF subsections involved in preserving language functions at the cost of nonverbal abilities. 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Abstract

The neuropsychological crowding effect denotes the reallocation of cognitive functions within the contralesional hemisphere following unilateral brain damage, prioritizing language at the expense of nonverbal abilities. This study investigates structural white matter correlates of crowding in the arcuate fasciculus (AF), a key language tract, using hemispherotomy as a unique setting to explore structural reorganization supporting language preservation. We explore two main hypotheses. First, the contralesional right AF undergoes white matter reorganization correlated with preserved language function at the expense of nonverbal abilities following left-hemispheric damage. Second, this reorganization varies with epilepsy etiology, influencing different stages of developmental language lateralization. This retrospective study included individuals post-hemispherotomy and healthy controls. Inclusion criteria were; (1) being a native German speaker, (2) having no MRI contraindication, (3) the ability to undergo approximately 2 h of MRI scans, and (4) the ability to participate in neuropsychological assessments over two consecutive days. Neuroimaging included T1-, T2-, and diffusion-weighted imaging, alongside postoperative neuropsychological assessments, where it was taken as evidence for crowding if verbal IQ exceeded performance IQ by at least 10 points. The AF was reconstructed using advanced tractography, and CoBundleMAP was used to compare morphologically corresponding AF subsections. Statistical significance was set at p < 0.05 $$ p<0.05 $$ , with correction for multiple comparisons applied across contiguous tract sections using Threshold-Free Cluster Enhancement. The final cohort comprised 22 individuals post-hemispherotomy (median age: 20.4 $$ 20.4 $$ years, range: 12.3 43.9 $$ 12.3-43.9 $$ ; 55% female; 55% with left-sided surgeries) and 20 healthy controls (median age: 23.8 $$ 23.8 $$ years, range: 15.5 54.0 $$ 15.5-54.0 $$ ; 55% female). Crowding was associated with significantly higher fractional anisotropy (FA) in the AF ( p = 0.015 $$ p=0.015 $$ , Cohen's d = 1.69 $$ d=1.69 $$ ), but only observed in individuals with left-sided hemispherotomy, localized to a subsection between Geschwind's territory and Wernicke's area ( p corrected = 0.02 $$ {p}_{\mathrm{corrected}}=0.02 $$ ). This region also displayed significantly higher normalized FA in AF of individuals with congenital etiology and crowding compared to acquired etiology and no crowding ( p corrected = 0.0189 $$ {p}_{\mathrm{corrected}}=0.0189 $$ ). This study identifies previously unreported neural correlates of crowding in right contralesional AF of individuals post-hemispherotomy and highlights specific AF subsections involved in preserving language functions at the cost of nonverbal abilities. The findings suggest a link between crowding and epilepsy etiology, particularly in the region spanning Geschwind's territory and Wernicke's area.

Abstract Image

结构白质与拥挤效应的相关性:来自弓形神经束半球切开术后的束束造影研究
神经心理拥挤效应表明,在单侧脑损伤后,对侧半球的认知功能重新分配,以牺牲非语言能力为代价优先考虑语言能力。本研究研究了弓形神经束(AF)中与拥挤相关的白质结构,这是一个关键的语言通道,使用半球切开术作为一个独特的设置来探索支持语言保存的结构重组。我们探讨了两个主要假设。首先,在左半球损伤后,对位性右心房颤动经历了与保留语言功能相关的白质重组,其代价是非语言能力的丧失。其次,这种重组因癫痫病因而异,影响发育中语言侧化的不同阶段。本回顾性研究包括脑半球切除术后的个体和健康对照。纳入标准为;(1)以德语为母语,(2)没有核磁共振禁忌症,(3)能够接受大约2小时的核磁共振扫描,(4)能够连续两天参加神经心理学评估。神经影像学包括T1、T2和弥散加权成像,以及术后神经心理学评估,如果言语智商超过表现智商至少10分,则将其作为拥挤的证据。采用先进的肌束造影重建AF,并使用CoBundleMAP比较形态学上对应的AF亚段。p &lt;0.05 $$ p<0.05 $$,使用无阈值聚类增强技术对相邻区域的多次比较进行校正。最终队列包括22例半球切除术后患者(中位年龄:20.4 $$ 20.4 $$岁,范围:12.3−43.9 $$ 12.3-43.9 $$;55% female; 55% with left-sided surgeries) and 20 healthy controls (median age: 23.8 $$ 23.8 $$ years, range: 15.5 − 54.0 $$ 15.5-54.0 $$ ; 55% female). Crowding was associated with significantly higher fractional anisotropy (FA) in the AF ( p = 0.015 $$ p=0.015 $$ , Cohen's d = 1.69 $$ d=1.69 $$ ), but only observed in individuals with left-sided hemispherotomy, localized to a subsection between Geschwind's territory and Wernicke's area ( p corrected = 0.02 $$ {p}_{\mathrm{corrected}}=0.02 $$ ). This region also displayed significantly higher normalized FA in AF of individuals with congenital etiology and crowding compared to acquired etiology and no crowding ( p corrected = 0.0189 $$ {p}_{\mathrm{corrected}}=0.0189 $$ ). This study identifies previously unreported neural correlates of crowding in right contralesional AF of individuals post-hemispherotomy and highlights specific AF subsections involved in preserving language functions at the cost of nonverbal abilities. The findings suggest a link between crowding and epilepsy etiology, particularly in the region spanning Geschwind's territory and Wernicke's area.
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来源期刊
Human Brain Mapping
Human Brain Mapping 医学-核医学
CiteScore
8.30
自引率
6.20%
发文量
401
审稿时长
3-6 weeks
期刊介绍: Human Brain Mapping publishes peer-reviewed basic, clinical, technical, and theoretical research in the interdisciplinary and rapidly expanding field of human brain mapping. The journal features research derived from non-invasive brain imaging modalities used to explore the spatial and temporal organization of the neural systems supporting human behavior. Imaging modalities of interest include positron emission tomography, event-related potentials, electro-and magnetoencephalography, magnetic resonance imaging, and single-photon emission tomography. Brain mapping research in both normal and clinical populations is encouraged. Article formats include Research Articles, Review Articles, Clinical Case Studies, and Technique, as well as Technological Developments, Theoretical Articles, and Synthetic Reviews. Technical advances, such as novel brain imaging methods, analyses for detecting or localizing neural activity, synergistic uses of multiple imaging modalities, and strategies for the design of behavioral paradigms and neural-systems modeling are of particular interest. The journal endorses the propagation of methodological standards and encourages database development in the field of human brain mapping.
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