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In 228 chronic left-hemisphere stroke patients, normative tract disconnection predicted aphasia little better than a straight-fibre null; conduction aphasia followed posterior STG, not arcuate, damage

Question: does white-matter disconnection, estimated by projecting a lesion onto a normative tractogram, predict aphasia beyond lesion size and location, and does the fibre route matter? Approach: we registered the 228 manual lesion masks of the open Aphasia Recovery Cohort (OpenNeuro ds004884 v1.0.2) to MNI152NLin2009cAsym with dipy (brain-masked affine, enantiomorphic filling, SyN) and projected them onto the HCP-842 tractogram (144,678 streamlines, 78 bundles). As a control, we built a null tractogram with the same streamline end points but straight fibres. Outcomes were WAB-R aphasia quotient (n = 228), non-fluent versus fluent type (102 versus 94) and conduction versus anomic type (26 versus 61). We used two-stage ridge models with 10-fold cross-validation (100 repeats) and subject-bootstrap intervals, and a priori logistic tests. Findings: log lesion volume gave R2 = 0.366 for severity; parcel lesion load added 0.001, bundle disconnection 0.086 (0.033 to 0.139) and parcel-pair disconnection 0.067 (0.011 to 0.120), but the straight-fibre null also added 0.054 and 0.037; true minus null was 0.032 (-0.004 to 0.068) and 0.030 (-0.005 to 0.064). For fluency, bundles added 0.060 AUC to volume and the null 0.042; frontal aslant tract disconnection predicted non-fluency beyond frontal speech cortex damage (odds ratio 2.63 per SD, p = 0.0003) and beat its own straight-fibre null, but the frontopontine tract did equally well. For conduction aphasia, cortical location gave AUC 0.744 and pair disconnection 0.672, below its null (-0.059, -0.110 to -0.011); arcuate fasciculus disconnection did not predict conduction aphasia (odds ratio 1.24, p = 0.59) under three measures, while posterior STG damage did (3.23, p = 0.0001). Excluding 11 weaker registrations did not change these results. Limitations: normative not patient-specific tractography; template registration error; arcuate any-hit saturates in large lesions; ARC gives only AQ and WAB type, not sub-scores; 26 conduction cases, and arcuate and posterior cortex damage overlap. The registered masks, features, code and figures are included.

stroke · aphasia · lesion-symptom mapping · structural disconnection · normative connectome · tractography · null model · arcuate fasciculus · conduction aphasia · frontal aslant tract · verbal fluency · Aphasia Recovery Cohort · HCP-842 · cross-validation · MNI registration · lesion masks

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References

16
  1. usesdoi:10.18112/openneuro.ds004884.v1.0.2

    Aphasia Recovery Cohort lesion masks, T2 images and WAB scores (CC0).

  2. usesdoi:10.1038/s41597-024-03819-7

    Data descriptor of the Aphasia Recovery Cohort.

  3. usesdoi:10.6084/m9.figshare.7375883.v2

    RecoBundles 80-bundle atlas and whole-brain HCP-842 tractogram in MNI space (CC BY 4.0).

  4. usesdoi:10.1016/j.neuroimage.2018.05.027

    HCP-842 population-averaged tractography atlas.

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    dipy registration (affine and SyN).

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    MNI152 2009 nonlinear template.

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    Enantiomorphic lesion filling for normalization.

  9. challengesdoi:10.1093/brain/awaa156

    Reported that indirect structural disconnection predicts post-stroke deficits; we find that a straight-fibre null keeps most of the disconnection gain for aphasia.

  10. supportsdoi:10.1016/j.nicl.2018.03.037

    Found structural disconnection a weak addition to lesion location for language outcome; our fibre-route gains are small.

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    Lesion Quantification Toolkit, a normative-tractogram disconnection method of the type tested here.

  12. challengesdoi:10.1093/brain/88.2.237

    Disconnection account of conduction aphasia; arcuate disconnection did not predict conduction aphasia here.

  13. supportsdoi:10.1016/j.bandl.2010.12.001

    Cortical (Spt, posterior temporal) account of conduction aphasia, which our posterior STG result agrees with.

  14. supportsdoi:10.1523/JNEUROSCI.1120-10.2010

    Repetition deficits with posterior perisylvian damage; agrees with our PPC and STG results.

  15. supportsdoi:10.1093/brain/awt163

    Frontal aslant tract and fluency; AST disconnection predicted non-fluent aphasia beyond frontal cortex damage.

  16. doi:10.1016/j.cortex.2015.09.005

    Earlier aphasia-type prediction from lesion and connectome data in a cohort from the same laboratory.

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