Structural integrity of corticospinal motor fibers predicts motor impairment in chronic stroke

Abstract

Objective: Motor impairment after stroke has been related to infarct size, infarct location, and integrity of motor tracts. To determine the value of diffusion tensor imaging (DTI) as a predictor of motor outcome and its role as a structural surrogate marker of impairment in chronic stroke, we tested correlations between motor impairment and DTI-derived measures of motor tract integrity.

Methods: Thirty-five chronic stroke patients with varying degrees of recovery underwent DTI and motor impairment assessments. Fibers originating from the precentral gyrus were traced and separated into pyramidal tract (PT) and alternate motor fibers (aMF). Asymmetry indices of fiber number and regional fractional anisotropy (FA) values comparing lesional with nonlesional hemispheres were correlated with motor impairment scores and compared to an age-matched control group.

Results: Fiber number and regional FA value asymmetry significantly differed between the groups with lower values in the patients' lesional hemispheres. Both measures significantly predicted motor impairment with stronger predictions when all motor tracts were combined as compared to predictions using only the PT. The pattern of motor tract damage (PT only vs PT and aMF) led to a classification of mild, moderate, or severe impairment with significant between-group differences in motor impairment scores.

Conclusions: Diffusion tensor imaging-derived measures are valid structural markers of motor impairment. The integrity of all descending motor tracts, not merely the pyramidal tract, appears to account for stroke recovery. A 3-tier, hierarchical classification of impairment categories based on the pattern of motor tract damage is proposed that might be helpful in predicting recovery potential.

Figure 1 Visualization of motor fibers originating from the precentral gyrus and traveling through posterior limb of the internal capsule and pons (A) The descending tracts differentiate into 2 different components in the pons with an anterior component corresponding to the pyramidal tract (PT) and a posterior component consisting of alternate or supplementary motor fibers (aMF). (B) Examples of regions of interest (ROIs), overlaid onto a normalized fractional anisotropy image. The cortical ROI encompassed the precentral gyrus and its underlying white matter (z = 50), which could have also included some corticospinal fibers originating from premotor cortex since there are no clear gross-anatomic markers to discriminate between primary motor cortex and premotor cortex. The ROI encompassing the posterior limb of the internal capsule was drawn at z = 8 and the pontine ROIs were drawn just below the superior cerebellar peduncle at approximately z = −24. (Coordinates are given in Talairach space.)

Figure 2 Three impairment groups An asymmetry score of 1.0 indicates that no fibers could be traced in the ipsilesional hemisphere. Hence, in group 1 (A) fibers originating from the precentral gyrus were traceable both in the anterior pons (pyramidal tract [PT]) and in the posterior pons (alternate motor fibers [aMF]); in group 2 (B) only fibers passing through the posterior pons could be traced (aMF), but no fibers in the anterior pons (PT); in group 3 (C) no fibers passing through either the anterior or posterior part of the ipsilesional pons (PT or aMF) were traceable. Significant between-group differences were found in motor impairment scores for all groups (Bonferroni-corrected post hoc tests). All values are given as mean scores ± SD; Wolf Motor Function Test (WMFT) scores are given in sec[log]. UE-FM = Upper Extremity Fugl-Meyer assessment.

Figure 3 Regressing fiber number asymmetry with motor impairment scores (A) Top row: Fiber number asymmetry scores using the narrow pontine region of interest (ROI) (including only pyramidal tract [PT] fibers), and (B) bottom row: using the broad pontine ROI (including PT fibers and alternate motor fibers [aMF]).

Figure 4 Regressing regional fractional anisotropy (FA) value asymmetry of the posterior limb of the internal capsule with motor impairment scores Hemispheric asymmetry of mean FA values in the internal capsule region of interest (also used for tractography of pyramidal tract fibers and alternate motor fibers).