Relating diffusion tensor imaging measurements to microstructural quantities in the cerebral cortex in multiple sclerosis.

Rebecca Mckavanagh,James Kolasinski,Steven A Chance,Karla L Miller,Charlotte J Stagg,Margaret M Esiri,Mario Torso,Mark Jenkinson,Heidi Johansen‐Berg,Jennifer A Mcnab

doi:10.1002/hbm.24711

Rebecca Mckavanagh, James Kolasinski + Show 8 more

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https://doi.org/10.1002/hbm.24711

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Abstract

To investigate whether the observed anisotropic diffusion in cerebral cortex may reflect its columnar cytoarchitecture and myeloarchitecture, as a potential biomarker for disease‐related changes, we compared postmortem diffusion magnetic resonance imaging scans of nine multiple sclerosis brains with histology measures from the same regions. Histology measurements assessed the cortical minicolumnar structure based on cell bodies and associated axon bundles in dorsolateral prefrontal cortex (Area 9), Heschl's gyrus (Area 41), and primary visual cortex (V1). Diffusivity measures included mean diffusivity, fractional anisotropy of the cortex, and three specific measures that may relate to the radial minicolumn structure: the angle of the principal diffusion direction in the cortex, the component that was perpendicular to the radial direction, and the component that was parallel to the radial direction. The cellular minicolumn microcircuit features were correlated with diffusion angle in Areas 9 and 41, and the axon bundle features were correlated with angle in Area 9 and to the parallel component in V1 cortex. This may reflect the effect of minicolumn microcircuit organisation on diffusion in the cortex, due to the number of coherently arranged membranes and myelinated structures. Several of the cortical diffusion measures showed group differences between MS brains and control brains. Differences between brain regions were also found in histology and diffusivity measurements consistent with established regional variation in cytoarchitecture and myeloarchitecture. Therefore, these novel measures may provide a surrogate of cortical organisation as a potential biomarker, which is particularly relevant for detecting regional changes in neurological disorders.

Highlights

Magnetic resonance imaging (MRI) is increasingly used to visualise the detailed structure of the cerebral cortex (e.g., cortical layers (Barazany & Assaf, 2011; Fatterpekar et al, 2002))
Diffusion in cortex exhibits some degree of fractional anisotropy (FA) (Anwander et al, 2010; Heidemann et al, 2009), most attention has been paid to the mean diffusivity (MD), which changes with age, pathology and across brain regions (Jeon et al, 2012)
Given the increasing interest in the cerebral cortex in multiple sclerosis (Wegner, Esiri, Chance, Palace, & Matthews, 2006), we have extended this investigation of the relationship between diffusion tensor imaging (DTI) and histology to the grey matter of the cortex in the same cohort

Summary

Introduction

Magnetic resonance imaging (MRI) is increasingly used to visualise the detailed structure of the cerebral cortex (e.g., cortical layers (Barazany & Assaf, 2011; Fatterpekar et al, 2002)). Several recent studies have shown that diffusion in the cortex is largely radial (i.e., perpendicular to the cortical surface) (McNab et al, 2009) while showing regional variation (Anwander et al, 2010; Kang et al, 2012; Kleinnijenhuis et al, 2013; McNab et al, 2013) and this has been interpreted as reflecting the cortex's anisotropic cytoarchitecture (Jespersen et al, 2012; Leuze et al, 2012). Such investigations have assessed the principal diffusion direction (PDD), revealing areas of consistently radial diffusion in motor (Anwander et al, 2010; McNab et al, 2013) and prefrontal (Anwander et al, 2010) cortex, and mixed reports of either more tangential (parallel to the cortical surface) (McNab et al, 2013) or radial (Kang et al, 2012) diffusion in other areas, for example, Heschl's gyrus

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