In vivo estimates of axonal stretch and 3D brain deformation during mild head impact

Abstract

The rapid deformation of brain tissue in response to head impact can lead to traumatic brain injury. In vivo measurements of brain deformation during non-injurious head impacts are necessary to understand the underlying mechanisms of traumatic brain injury and compare to computational models of brain biomechanics. Using tagged magnetic resonance imaging (MRI), we obtained measurements of three-dimensional strain tensors that resulted from a mild head impact after neck rotation or neck extension. Measurements of maximum principal strain (MPS) peaked shortly after impact, with maximal values of 0.019–0.053 that correlated strongly with peak angular velocity. Subject-specific patterns of MPS were spatially heterogeneous and consistent across subjects for the same motion, though regions of high deformation differed between motions. The largest MPS values were seen in the cortical gray matter and cerebral white matter for neck rotation and the brainstem and cerebellum for neck extension. Axonal fiber strain (Ef) was estimated by combining the strain tensor with diffusion tensor imaging data. As with MPS, patterns of Ef varied spatially within subjects, were similar across subjects within each motion, and showed group differences between motions. Values were highest and most strongly correlated with peak angular velocity in the corpus callosum for neck rotation and in the brainstem for neck extension. The different patterns of brain deformation between head motions highlight potential areas of greater risk of injury between motions at higher loading conditions. Additionally, these experimental measurements can be directly compared to predictions of generic or subject-specific computational models of traumatic brain injury.

Statement of Significance

Traumatic brain injury can result from the rapid acceleration of the skull, leading to deformation of brain tissue and elongation of axonal fibers. Because treatment options and prognostic models for patients are lacking, a better understanding of injury mechanisms is needed. Here, we use tagged magnetic resonance imaging to measure deformation throughout the live, human brain during non-injurious head accelerations. We present the first in vivo measurements of axonal stretch and compare MPS and axonal stretch experienced during neck rotation and neck extension. These results are important to elucidate brain regions at risk for injury. Additionally, they can be directly used to evaluate computational models of brain injury, which are used to predict risk of concussion during head impacts and design protective equipment.