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Toward personalised diffusion MRI in psychiatry: improved delineation of fibre bundles with the highest-ever angular resolution in vivo tractography.

ABSTRACT: Diffusion MRI (dMRI) tractography is a uniquely powerful tool capable of demonstrating structural brain network abnormalities across a range of psychiatric disorders; however, it is not currently clinically useful. This is because limitations on sensitivity effectively restrict its application to scientific studies of cohorts, rather than individual patients. Recent improvements in dMRI hardware, acquisition, processing and analysis techniques may, however, overcome these measurement limitations. We therefore acquired the highest-ever angular resolution in vivo tractographic data set, and used these data to ask the question: 'is cutting-edge, optimised dMRI now sensitive enough to measure brain network abnormalities at a level that may enable personalised psychiatry?' The fibre tracking performance of this 'gold standard' data set of 1150 unique directions (11 shells) was compared to a conventional 64-direction protocol (single shell) and a clinically practical, highly optimised and accelerated 9-min protocol of 140 directions (3 shells). Three major tracts of relevance to psychiatry were evaluated: the cingulate bundle, the uncinate fasciculus and the corticospinal tract. We found up to a 34-fold improvement in tracking accuracy using the 1150-direction data set compared to the 64-direction data set, while 140-direction data offered a maximum 17-fold improvement. We also observed between 20 and 50% improvements in tracking efficiency for the 140-direction data set, a finding we then replicated in a normal cohort (n?=?53). We found evidence that lower angular resolution data may introduce systematic anatomical biases. These data highlight the imminent potential of dMRI as a clinically meaningful technique at a personalised level, and should inform current practice in clinical studies.

SUBMITTER: Callaghan F

PROVIDER: S-EPMC5915595 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Toward personalised diffusion MRI in psychiatry: improved delineation of fibre bundles with the highest-ever angular resolution in vivo tractography.

Callaghan Fraser F Maller Jerome J JJ Welton Thomas T Middione Matthew J MJ Shankaranarayanan Ajit A Grieve Stuart M SM

Translational psychiatry 20180425 1

Diffusion MRI (dMRI) tractography is a uniquely powerful tool capable of demonstrating structural brain network abnormalities across a range of psychiatric disorders; however, it is not currently clinically useful. This is because limitations on sensitivity effectively restrict its application to scientific studies of cohorts, rather than individual patients. Recent improvements in dMRI hardware, acquisition, processing and analysis techniques may, however, overcome these measurement limitations ...[more]

PMID: 29691374

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Project description: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.

Project description:Diffusion Tensor Magnetic Resonance Imaging (DTI) allows to decode the mobility of water molecules in cerebral tissue, which is highly directional along myelinated fibers. By integrating the direction of highest water diffusion through the tissue, DTI Tractography enables a non-invasive dissection of brain fiber bundles. As such, this technique is a unique probe for in vivo characterization of white matter architecture. Unraveling the principal brain texture features of preclinical models that are advantageously exploited in experimental neuroscience is crucial to correctly evaluate investigational findings and to correlate them with real clinical scenarios. Although structurally similar to the human brain, the gyrencephalic ovine model has not yet been characterized by a systematic DTI study. Here we present the first in vivo sheep (ovis aries) tractography atlas, where the course of the main white matter fiber bundles of the ovine brain has been reconstructed. In the context of the EU's Horizon EDEN2020 project, in vivo brain MRI protocol for ovine animal models was optimized on a 1.5T scanner. High resolution conventional MRI scans and DTI sequences (b-value = 1,000 s/mm2, 15 directions) were acquired on ten anesthetized sheep o. aries, in order to define the diffusion features of normal adult ovine brain tissue. Topography of the ovine cortex was studied and DTI maps were derived, to perform DTI tractography reconstruction of the corticospinal tract, corpus callosum, fornix, visual pathway, and occipitofrontal fascicle, bilaterally for all the animals. Binary masks of the tracts were then coregistered and reported in the space of a standard stereotaxic ovine reference system, to demonstrate the consistency of the fiber bundles and the minimal inter-subject variability in a unique tractography atlas. Our results determine the feasibility of a protocol to perform in vivo DTI tractography of the sheep, providing a reliable reconstruction and 3D rendering of major ovine fiber tracts underlying different neurological functions. Estimation of fiber directions and interactions would lead to a more comprehensive understanding of the sheep's brain anatomy, potentially exploitable in preclinical experiments, thus representing a precious tool for veterinaries and researchers.

Dataset Information

Toward personalised diffusion MRI in psychiatry: improved delineation of fibre bundles with the highest-ever angular resolution in vivo tractography.

Publications

Toward personalised diffusion MRI in psychiatry: improved delineation of fibre bundles with the highest-ever angular resolution in vivo tractography.

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