Frontiers in Neuroscience (Mar 2020)

fMRI-Targeted High-Angular Resolution Diffusion MR Tractography to Identify Functional Language Tracts in Healthy Controls and Glioma Patients

  • Francesco Sanvito,
  • Francesco Sanvito,
  • Eduardo Caverzasi,
  • Marco Riva,
  • Marco Riva,
  • Kesshi M. Jordan,
  • Valeria Blasi,
  • Paola Scifo,
  • Antonella Iadanza,
  • Antonella Iadanza,
  • Sofia Allegra Crespi,
  • Sofia Allegra Crespi,
  • Sara Cirillo,
  • Sara Cirillo,
  • Alessandra Casarotti,
  • Antonella Leonetti,
  • Guglielmo Puglisi,
  • Marco Grimaldi,
  • Lorenzo Bello,
  • Lorenzo Bello,
  • Maria Luisa Gorno-Tempini,
  • Roland G. Henry,
  • Andrea Falini,
  • Andrea Falini,
  • Antonella Castellano,
  • Antonella Castellano

DOI
https://doi.org/10.3389/fnins.2020.00225
Journal volume & issue
Vol. 14

Abstract

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BackgroundMR Tractography enables non-invasive preoperative depiction of language subcortical tracts, which is crucial for the presurgical work-up of brain tumors; however, it cannot evaluate the exact function of the fibers.PurposeA systematic pipeline was developed to combine tractography reconstruction of language fiber bundles, based on anatomical landmarks (Anatomical-T), with language fMRI cortical activations. A fMRI-targeted Tractography (fMRI-T) was thus obtained, depicting the subsets of the anatomical tracts whose endpoints are located inside a fMRI activation. We hypothesized that fMRI-T could provide additional functional information regarding the subcortical structures, better reflecting the eloquent white matter structures identified intraoperatively.MethodsBoth Anatomical-T and fMRI-T of language fiber tracts were performed on 16 controls and preoperatively on 16 patients with left-hemisphere brain tumors, using a q-ball residual bootstrap algorithm based on High Angular Resolution Diffusion Imaging (HARDI) datasets (b = 3000 s/mm2; 60 directions); fMRI ROIs were obtained using picture naming, verbal fluency, and auditory verb generation tasks. In healthy controls, normalized MNI atlases of fMRI-T and Anatomical-T were obtained. In patients, the surgical resection of the tumor was pursued by identifying eloquent structures with intraoperative direct electrical stimulation mapping and extending surgery to the functional boundaries. Post-surgical MRI allowed to identify Anatomical-T and fMRI-T non-eloquent portions removed during the procedure.ResultsMNI Atlases showed that fMRI-T is a subset of Anatomical-T, and that different task-specific fMRI-T involve both shared subsets and task-specific subsets – e.g., verbal fluency fMRI-T strongly involves dorsal frontal tracts, consistently with the phonogical-articulatory features of this task. A quantitative analysis in patients revealed that Anatomical-T removed portions of AF-SLF and IFOF were significantly greater than verbal fluency fMRI-T ones, suggesting that fMRI-T is a more specific approach. In addition, qualitative analyses showed that fMRI-T AF-SLF and IFOF predict the exact functional limits of resection with increased specificity when compared to Anatomical-T counterparts, especially the superior frontal portion of IFOF, in a subcohort of patients.ConclusionThese results suggest that performing fMRI-T in addition to the ‘classic’ Anatomical-T may be useful in a preoperative setting to identify the ‘high-risk subsets’ that should be spared during the surgical procedure.

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