Introduction

Characterization of skull-brain interactions during applied motion is essential to understanding the mechanics of traumatic brain injury, but in vivo characterization is limited. A previous study utilized MR elastography (MRE) combined with accelerometers to investigate the relative brain-skull motion; however, the skull motion was indirectly assessed and the motion was limited to vertical vibrations[1]. Direct measurement of skull and brain motion responding to different vibrational directions could expand our understanding of how the skull-brain interface attenuates and delays motion transmission into the brain. Towards this goal, we developed a dual-saturation imaging and dual-sensitivity motion encoding scheme to directly measure and reliably unwrap the skull as well as brain phase images using MRE. In addition we used this technique to study the relative skull-brain motion in volunteers with a newly developed multi-excitation head driver.

Methods

MRE exams were performed on 3 healthy volunteers with a multi-excitation head driver that is integrated into a 12-channel head coil (Fig.1). Three distinct excitation patterns (anterior-posterior(AP), left-right(LR), and clockwise(CW)) at 60-Hz were introduced into the head by independently setting the amplitude and phase of the individual actuators (Fig.1D). Dual-saturation imaging- i.e., one MRE scan with water-selective SPSP excitation (fat-suppression) and the other with fat-selective SPSP excitation (water-suppression) – was performed to characterize mechanically-induced motion of the brain and skull respectively. The signal from the skull was detected from the fatty marrow contained within the medullary cavity. The 3D skull-plus-brain MRE data were generated by combing the dominantly water and fat MRE data in the complex image domain. MRE data was acquired with a modified SS-SE-EPI-MRE sequence incorporating the dual-sensitivity motion encoding scheme, in which the amplitude of negative MEGs were set to be smaller (77.7%) than that of positive MEGs, resulting in both low and high motion encoding sensitivity phase in a single scan when these phases are added or subtracted respectively. The low-sensitivity phase images that are practically free of skull-based phase wrap were then used to guide unwrapping of the high-sensitivity phase image. Other imaging parameters include: TR/TE=4000/58.7ms; FOV=24cm; 80×80 acquisition matrix reconstructed to 128×128; 48 contiguous 3-mm-thick axial slices; 2xASSET; 4 phase offsets. MRE displacements from the brain and skull ROIs (Fig.2D) were fitted to a model of rigid-body motion to obtain rigid-body translation and rotation. The amplitude and temporal phase delay between the skull and brain were compared for each rigid-body component. The relative motion of the skull and brain was also visualized by slip interface imaging (SII) as previous described[2].

Results

An example of the combined skull-plus-brain image is shown in Fig.2. Fig.3 shows the wrap-free images following the proposed unwrapping process that is guided by the low-sensitivity phase data. Fig.4 shows the amplitude and temporal phase delay of the rigid-body translation and rotation of the skull and brain under different vibration patterns. The amplitude of the translation from skull to brain was slightly reduced, whereas the rotation transmission was highly attenuated. The phase delay between the skull and brain rotation was longer (0.80±0.16rad) than that of the translation (0.07±0.01rad). The temporal phase delay was found to be independent of vibrational directions. Fig.5 shows one example of SII to qualitatively visualize the relative skull-brain motion. Note that the skull-brain slip interface is spatially heterogeneous.

Discussion

Direct skull displacement measurement is difficult for two reasons: the signal void of the skull on the standard SE-EPI-MRE sequence and heavily wrapped phase in the skull that is topologically separated from the brain. In this study, by switching to water-suppressed acquisition, the medullary cavity filled of fatty marrow has high enough signal to be used to track the skull motion. By using the dual-sensitivity motion encoded acquisition, wrap-free estimates of phase were successfully generated even with only 4 phase offsets, a scenario where conventional phase unwrapping algorithms often fail. We demonstrated that the multi-excitation driver can induce the desired motion patterns. With it, our results suggest that the skull-brain interface may significantly attenuate and delay the rotational motion that is potentially more harmful in regard to brain injury[3]. Interestingly, the slip interface between the skull and brain does not appear to be completely evident. This suggests that some areas of the interface may be mechanically different. Of note, there appears to exist a complete slip interface between the scalp and skull, suggesting that the scalp motion may not be an accurate surrogate measure of skull motion.

Conclusion

Our results suggest that the proposed dual-saturation imaging and dual-sensitivity motion encoding MRE technique is an effective tool for measuring 3D in vivo skull and brain motion under different vibrational conditions.

Acknowledgements

This work was supported by grant from the National Institute of Health RO1 EB001981.

References

[1] Badachhape, A. A. et al. The Relationship of Three-Dimensional Human Skull Motion to Brain Tissue Deformation in Magnetic Resonance Elastography Studies. J Biomech Eng 139, doi:10.1115/1.4036146 (2017). [2] Yin, Z. et al. Slip Interface Imaging Predicts Tumor-Brain Adhesion in Vestibular Schwannomas. Radiology 277, 507-517, doi:10.1148/radiol.2015151075 (2015). [3] Rowson, S. et al. Biomechanical Perspectives on Concussion in Sport. Sports medicine and arthroscopy review 24, 100-107, doi:10.1097/jsa.0000000000000121 (2016).