Superficial white matter imaging: Contrast mechanisms and whole-brain in vivo mapping

Kirilina, Evgeniya; Helbling, Saskia; Morawski, Markus; Pine, Kerrin; Reimann, Katja; Jánkuhn, Steffen; Dinse, Juliane; Deistung, Andreas; Reichenbach, Jürgen R.; Trampel, Robert; Geyer, Stefan; Müller, Larissa; Jakubowski, Norbert; Arendt, Thomas; Bazin, Pierre‐Louis; Weiskopf, Nikolaus

doi:10.1126/sciadv.aaz9281

Cited by 82 publications

(91 citation statements)

References 44 publications

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“…Specifically and consistently with prior studies [46, 63], we found that FA values increased in sWM. In contrast to deep WM that plays an important role in subcortical and remote cortical connectivity, sWM is strongly influenced by cortical GM, particularly short cortical association fibers (also called arcuate or “U”-fibers), which connect adjacent gyri and comprise the majority of corticocortical WM connections [15]. FA increases in sWM might thus indicate stronger influence from axonal packing organization and myelination on short corticocortical WM connections.…”

Section: Discussionmentioning

confidence: 99%

Cyto/myeloarchitectural changes of cortical gray matter and superficial white matter in early neurodevelopment: Multimodal MRI study of preterm neonates

Yuan

Liu

Kim

et al. 2021

Preprint

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The developing cerebral cortex undergoes rapid microstructural and morphological changes throughout the third trimester. Recently, increased attention has been focused on the identification of imaging features that represent the underlying cortical cyto/myeloarchitecture driving intracortical myelination and the maturation of cortical gray matter (GM) and its adjacent superficial white matter (sWM). However, the characterization and spatiotemporal pattern of complex cyto/myeloarchitectural changes in this critical time period remain incompletely understood. Using 92 MRI scans from 78 preterm neonates (baseline: n = 78, postmenstrual age=33.1+/-1.8 weeks; follow-up: n=14, 37.3+/-1.3), the current study leveraged combined T1/T2 intensity ratio and diffusion tensor imaging (DTI) measurements, including fractional anisotropy (FA) and mean diffusivity (MD), to characterize the cyto/myeloarchitectural architecture of cortical GM and its adjacent sWM in preterm neonates. DTI metrics during these weeks showed an overall linear developmental trajectory: FA decreased along with time in GM but increased in sWM; MD decreased in both GM and sWM. In contrast, T1/T2 measurements showed a distinctive parabolic developmental trajectory, revealing additional cyto/myeloarchitectural signature inferred. Furthermore, the spatiotemporal courses of T1/T2 ratio and DTI parameters were found to be regionally heterogeneous across the cerebral cortex, suggesting these imaging features specific relationship to regional cyto/myeloarchitectural maturation: faster T1/T2 ratio changes were found in the central, ventral, and temporal regions of GM and sWM, faster FA increases in anterior sWM areas, and faster MD decreases in GM and sWM central and cingulate areas. Taken together, our results may offer an explanation of the novel pattern of cyto/myeloarchitectural processes observed throughout the third trimester, including dendritic arborization, synaptogenesis, glial proliferation, as well as radial glial cell organization and apoptosis. Finally, T1/T2 ratio and DTI measurements were significantly associated with 1 year outcome scores of language and cognitive performance as well as perinatal clinical conditions, including intraventricular hemorrhage and chronic lung disease, demonstrating their potential as imaging biomarkers characterizing microstructural deviation in atypical neurodevelopment. Ultimately, with combined properties of cortical T1/T2 and DTI measurements, this study provides unique insights into the cellular processes and associated developmental mechanisms during the critical development of the third trimester.

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Section: Discussionmentioning

confidence: 99%

Cyto/myeloarchitectural changes of cortical gray matter and superficial white matter in early neurodevelopment: Multimodal MRI study of preterm neonates

Yuan

Liu

Kim

et al. 2021

Preprint

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“…These quantitative parameters contain specific and complementary information regarding the microstructural properties of brain tissue, such as the extent of myelination, iron and water concentration (e.g. Weiskopf et al, 2015; Kirilina et al, 2020). Combining diffusion MRI with MPM thus allows for the examination of microstructural information related to the neuronal conduction velocity in the form of the axonal g-ratio (Mohammadi et al, 2015a; Mohammadi and Callaghan, 2020).…”

Section: Introductionmentioning

confidence: 99%

Reducing susceptibility distortion related image blurring in diffusion MRI EPI data

Clark

Callaghan

Weiskopf

et al. 2021

Preprint

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Diffusion magnetic resonance imaging (MRI) is an increasingly popular technique in basic and clinical neuroscience. One promising application is to combine diffusion MRI with myelin maps from complementary MRI techniques such as multi-parameter mapping (MPM) to produce g-ratio maps that represent the relative myelination of axons and predict their conduction velocity. Statistical Parametric Mapping (SPM) can process both diffusion data and MPMs, making SPM the only widely accessible software that contains all the processing steps required to perform group analyses of g-ratio data in a common space. However, limitations have been identified in its method for reducing susceptibility-related distortion in diffusion data. More generally, susceptibility-related image distortion is often corrected by combining oppositely phase-encoded images (blip-up and blip-down) using the arithmetic mean (AM), however, this can lead to blurred images. In this study we sought to (1) improve the susceptibility-related distortion correction for diffusion MRI data in SPM; (2) deploy an alternative approach to the AM to reduce image blurring in diffusion MRI data when combining blip-up and blip-down EPI data after susceptibility-related distortion correction; and (3) assess the benefits of these changes for g-ratio mapping. We found that the new processing pipeline, called consecutive HySCO, improved distortion correction when compared to the standard approach in the ACID toolbox for SPM. Moreover, using a weighted average (WA) method to combine the distortion corrected data from each phase-encoding polarity achieved greater overlap of diffusion and more anatomically faithful structural white matter probability maps derived from minimally distorted multi-parameter maps as compared to the AM. Third, we showed that the consecutive HySCO WA performed better than the AM method when combined with multi-parameter maps to perform g-ratio mapping. These improvements mean that researchers can conveniently access a wide range of diffusion-related analysis methods within one framework because they are now available within the open-source ACID toolbox as part of SPM, which can be easily combined with other SPM toolboxes, such as the hMRI toolbox, to facilitate computation of myelin biomarkers that are necessary for g-ratio mapping.

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“…8,9 SWM mainly consists of short, thin, U-fibres linking nearby gyri that lie up to 2mm below the cortex but may represent 57-67% of all WM fibres. [10][11][12] SWM fibre organisation is also highly complex 13,14 and may form sub-networks of its own. 15 Unique anatomical, developmental and cellular SWM properties may lead to particular vulnerabilities to Alzheimer's disease-related pathology.…”

Section: Introductionmentioning

confidence: 99%

Loss and Reorganisation of Superficial White Matter in Alzheimer’s disease: A Diffusion MRI study

Veale

Poole

et al. 2021

Preprint

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Pathological involvement of cerebral white matter in Alzheimer's disease has been shown using diffusion tensor imaging. Superficial white matter (SWM) changes have been relatively understudied despite their importance in cortico-cortical connections. Measuring SWM degeneration using diffusion tensor imaging is challenging due to its complex structure and proximity to the cortex. To overcome this we investigated diffusion MRI changes in young-onset Alzheimer's disease using standard diffusion tensor imaging and Neurite Orientation Dispersion and Density Imaging to distinguish between disease-related changes that are due to degeneration (e.g. loss of myelinated fibres) and those due to reorganisation (e.g. increased fibre dispersion). Twenty-nine young-onset Alzheimer's disease patients and 22 healthy controls had both single-shell and multi-shell diffusion MRI. We calculated fractional anisotropy, mean diffusivity, neurite density index, orientation dispersion index and tissue fraction (1-free water fraction). Diffusion metrics were sampled in 15 a priori regions of interest at four points along the cortical profile: cortical grey matter, the grey/white boundary, SWM (1mm below grey/white boundary) and SWM/deeper white matter (2mm below grey/white boundary). To estimate cross-sectional group differences, we used average marginal effects from linear mixed effect models of participants' diffusion metrics along the cortical profile. The SWM of young-onset Alzheimer's disease individuals had lower neurite density index compared to controls in five regions (superior and inferior parietal, precuneus, entorhinal and parahippocampus) (all P<0.05), and higher orientation dispersion index in three regions (fusiform, entorhinal and parahippocampus) (all P<0.05). Young-onset Alzheimer's disease individuals had lower fractional anisotropy in the SWM of two regions (entorhinal and parahippocampus) (both P<0.05) and higher fractional anisotropy within the postcentral region (P<0.05). Mean diffusivity in SWM was higher in the young-onset Alzheimer's disease group in the parahippocampal region (P<0.05) and lower in three regions (postcentral, precentral and superior temporal) (all P<0.05). In the overlying grey matter, disease-related changes were largely consistent with SWM findings when using neurite density index and fractional anisotropy, but appeared at odds with orientation dispersion and mean diffusivity SWM changes. Tissue fraction was significantly lower across all grey matter regions in young-onset Alzheimer's disease individuals (all P<0.001) but group differences reduced in magnitude and coverage when moving towards the SWM. These results show that microstructural changes occur within SWM and along the cortical profile in individuals with young-onset Alzheimer's disease. Lower neurite density and higher orientation dispersion suggests underlying SWM fibres undergo neurodegeneration and reorganisation, two effects previously indiscernible using standard diffusion tensor metrics in SWM.

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Superficial white matter imaging: Contrast mechanisms and whole-brain in vivo mapping

Cited by 82 publications

References 44 publications

Cyto/myeloarchitectural changes of cortical gray matter and superficial white matter in early neurodevelopment: Multimodal MRI study of preterm neonates

Cyto/myeloarchitectural changes of cortical gray matter and superficial white matter in early neurodevelopment: Multimodal MRI study of preterm neonates

Reducing susceptibility distortion related image blurring in diffusion MRI EPI data

Loss and Reorganisation of Superficial White Matter in Alzheimer’s disease: A Diffusion MRI study

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