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

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 , 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: $20.4$ years, range: $12.3-43.9$ ; 55% female; 55% with left-sided surgeries) and 20 healthy controls (median age: $23.8$ years, range: $15.5-54.0$ ; 55% female). Crowding was associated with significantly higher fractional anisotropy (FA) in the AF ( $p=0.015$ , Cohen's $d=1.69$ ), but only observed in individuals with left-sided hemispherotomy, localized to a subsection between Geschwind's territory and Wernicke's area ( $p_{\text{corrected}}=0.02$ ). This region also displayed significantly higher normalized FA in AF of individuals with congenital etiology and crowding compared to acquired etiology and no crowding ( $p_{\text{corrected}}=0.0189$ ). 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.

FIGURE 1

Normalized FA along the AF for individuals post‐hemispherotomy and controls. (a) Comparison of whole‐tract normalized FA between individuals post‐hemispherotomy and controls. (b) Comparison of normalized FA along the tract via CoBundleMAP. Bins with significant difference between individuals post‐hemispherotomy and controls are overlaid in red on the joint AF tractographies from the respective hemispheres ((c–e), right contralesional; (i–k), left‐contralesional). Corresponding slices (MNI152) are displayed for both contralesional hemispheres ((f–h), right; (l–n), left). Asterisks denote bins with statistically significant differences between groups ($p_{\text{corrected}}<0.05$) after TFCE correction for multiple comparisons.

FIGURE 2

Crowding‐related differences in FA of the AF. (a) Whole‐tract normalized fractional anisotropy (FA) for the crowding, no‐crowding, and control subgroups. (b) Sectional analysis of normalized FA using CoBundleMAP for the crowding and no‐crowding subgroups. Bins with significant difference between individuals with crowding and individuals without crowding are overlaid in red on the joint AF tractographies from the respective hemispheres ((c‐e), right contralesional; (i–k), left‐contralesional). Corresponding slices (MNI152) are displayed for right contralesional hemispheres (f–h). Asterisks denote statistically significant differences ($p_{\text{corrected}}<0.05$) after TFCE correction.

FIGURE 3

Specificity of crowding‐related differences with the ILF as a nonlanguage tract. (a) Whole‐tract normalized FA for the ILF post‐hemispherotomy, and control groups. (b) Section‐wise CoBundleMAP analysis of normalized FA of the ILF comparing healthy controls and individuals post‐hemispherotomy. Bins with significantly lower normalized FA are overlaid in blue along the ILF in both the right (c–h) and left (i–n) contralesional hemisphere. p values are corrected using TFCE. (o) Whole‐tract normalized FA and (p) section‐wise CoBundleMAP analysis of normalized FA of the ILF comparing individuals with crowding and no crowding.

FIGURE 4

Predicted probability of crowding as a function of normalized FA for three logistic regression models. The solid blue line represents the predicted probability of crowding from the respective logistic regression model estimated from normalized FA. The shaded blue area indicates the 95% confidence interval.

FIGURE 5

Verbal and nonverbal test performance in relation to etiology and normalized FA. (a) Sectional bin comparisons are shown for three groups: Congenital‐crowding, acquired‐no crowding, and congenital‐no crowding (all individuals post‐hemispherotomy, irrespective of surgery side). Bins showing significant differences between individuals with congenital etiology and crowding, and those with acquired etiology without crowding, are highlighted in red on the joint AF tractographies for the respective hemispheres ((b–d) right contralesional; (h–j) left contralesional). Corresponding MNI152 slices are provided for the right contralesional hemisphere (e–g) and the left contralesional hemisphere (k–m). (n) a 2 × 2 table showing the distribution of individuals by crowding and etiology. No cases of acquired‐crowding are present in this study group. Observed test scores for (o) VIQ, (p) PIQ, and (q) the delta (VIQ–PIQ), grouped by left and right contralesional hemisphere and further subgrouped by etiology (congenital and acquired) are shown. Statistically significant differences ($p_{\text{corrected}}<0.05$) after TFCE correction are marked with asterisks.

FIGURE 6

Methods Overview. Diffusion‐weighted MRI data of individuals with hemispherotomy and healthy controls (a) were used to compute fiber orientation distribution functions (fODFs) and low‐rank approximations (b) using an unscented Kalman filter. (c) Regions of interest (ROIs) for the AF were delineated in MNI152 space and transformed into subject space using ANTs‐based inverse affine matrices and warp fields. (d) Following whole‐brain tractography, the AF was extracted for each subject's intact hemispheres (n = 62). (e) Following alignment of right‐ and left‐sided AF via an iterative closest points algorithm and the computation of a joint manifold via isometric mapping (Tenenbaum et al. 2000), CoBundleMAP was used to segment the AFs of all subjects into 7 morphologically corresponding bins along their posterior–anterior trajectories.