Direct and specific assessment of axonal injury and spinal cord microenvironments using diffusion correlation imaging

Autor: Peter J. Basser, Guofeng Zhang, Courtney J. Comrie, Dan Benjamini, Carlo Pierpaoli, Susan C. Schwerin, Elizabeth B. Hutchinson, Michal E. Komlosh
Rok vydání: 2020
Předmět:
Male
Electron Microscope Tomography
Wallerian degeneration
Materials science
Anisotropic diffusion
Cognitive Neuroscience
Pyramidal Tracts
specificity
Neuroimaging
Sensitivity and Specificity
050105 experimental psychology
Article
lcsh:RC321-571
axonal injury
spectrum
030218 nuclear medicine & medical imaging
Correlation
03 medical and health sciences
0302 clinical medicine
Nuclear magnetic resonance
Head Injuries
Closed

distribution
medicine
Animals
0501 psychology and cognitive sciences
Diffusion (business)
Anisotropy
lcsh:Neurosciences. Biological psychiatry. Neuropsychiatry
DDCOSY
05 social sciences
diffusion
Ferrets
Cervical Cord
medicine.disease
Spinal cord
Immunohistochemistry
Axons
Diffusion Magnetic Resonance Imaging
medicine.anatomical_structure
Neurology
nervous system
correlation
Closed head injury
MADCO
030217 neurology & neurosurgery
MRI
Diffusion MRI
Zdroj: NeuroImage
NeuroImage, Vol 221, Iss, Pp 117195-(2020)
Popis: We describe a practical two-dimensional (2D) diffusion MRI framework to deliver specificity and improve sensitivity to axonal injury in the spinal cord. This approach provides intravoxel distributions of correlations of water mobilities in orthogonal directions, revealing sub-voxel diffusion components. Here we use it to investigate water diffusivities along axial and radial orientations within spinal cord specimens with confirmed, tract-specific axonal injury. First, we show using transmission electron microscopy (TEM) and immunohistochemistry that tract-specific axonal beading occurs following Wallerian degeneration in the cortico-spinal tract (CST) as direct sequelae to closed head injury (CHI). We demonstrate that although some voxel-averaged diffusion tensor imaging (DTI) metrics are sensitive to this axonal injury, they are non-specific, i.e., they do not reveal an underlying biophysical mechanism of injury. Then we employed 2D diffusion correlation imaging (DCI) to improve discrimination of different water microenvironments by measuring and mapping the joint water mobility distributions perpendicular and parallel to the spinal cord axis. We determined six distinct diffusion spectral components that differ according to their microscopic anisotropy and mobility. We further identified a distinct microenvironment that is specifically associated with the injury-induced axonal degeneration, with reduced and increased diffusivities parallel and perpendicular, respectively, hallmarks of axonal beading. An injury-specific MR image of the CHI spinal cord was then generated, and a radiological-pathological correlation with histological silver staining % area was performed. The resulting large and significant correlation ( r = 0.79, p < 0.0001) indicates the high specificity with which DCI detects injury-induced tissue alterations. We predict that the ability to selectively image microstructural changes following axonal injury in the spinal cord can be useful in clinical and research applications, by enabling specific detection and increased sensitivity to injury-induced microstructural alterations. These results also encourage us to translate DCI to higher spatial dimensions to enable assessment of traumatic axonal injury, and possibly other diseases and disorders in the brain.
Databáze: OpenAIRE