High-resolution 3D diffusion tensor MRI of anesthetized rhesus macaque brain at 3T

ABSTRACT Diffusion Magnetic Resonance Imaging (dMRI) has been widely used to investigate human brain microstructure and connectivity and its abnormalities in a variety of brain deficits, whether acute, neurodevelopmental or neurodegenerative. However, the biological interpretation and validation of dMRI data modelling is still a crucial challenge in the field. In this respect, achieving high spatial resolution in‐vivo dMRI in the non‐human primate to compare these observations both with human dMRI on the one hand and 'ground truth' microstructural and histological data on the other hand is of outmost importance. Here, we developed a dMRI pulse sequence based on 3D‐multishot Echo Planar Imaging (3D‐msEPI) on a 3T human clinical scanner. We demonstrate the feasibility of cerebral dMRI at an isotropic resolution of 0.5 mm in 4 anesthetized macaque monkeys. The added value of the high‐resolution dMRI is illustrated by focusing on two aspects. First, we show an enhanced descriptive power of the fine substructure of the hippocampus. Second, we show a more physiological description of the interface between cortex grey matter, superficial and deep white matter. Overall, the high spatial resolution dMRI acquisition method proposed in this study is a significant achievement with respect to the state of the art of dMRI on anesthetized monkeys. This study highlights also the potential of very high‐resolution dMRI to precisely capture the microstructure of thin cerebral structures such as the hippocampus and superficial white matter. HIGHLIGHTSThe proposed 3D‐msEPI dMRI pulse sequence presents several technical advantages over classical 2D‐single shot EPI and 2D‐msEPI sequences.0.5mm isotropic spatial resolution DTI of anesthetized macaque monkey brain using a 3T clinical MRI scanner.This high spatial resolution enhances the descriptive power of thin cerebral structures such as the hippocampus and superficial white matter

[1]  Robin M Heidemann,et al.  Generalized autocalibrating partially parallel acquisitions (GRAPPA) , 2002, Magnetic resonance in medicine.

[2]  Nan-Kuei Chen,et al.  Phase correction for three‐dimensional (3D) diffusion‐weighted interleaved EPI using 3D multiplexed sensitivity encoding and reconstruction (3D‐MUSER) , 2018, Magnetic resonance in medicine.

[3]  Alan Connelly,et al.  Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution , 2004, NeuroImage.

[4]  R. Deriche,et al.  Design of multishell sampling schemes with uniform coverage in diffusion MRI , 2013, Magnetic resonance in medicine.

[5]  Colin Studholme,et al.  Characterization of Laminar Zones in the Mid-Gestation Primate Brain with Magnetic Resonance Imaging and Histological Methods , 2015, Front. Neuroanat..

[6]  Qinmu Peng,et al.  Population-averaged macaque brain atlas with high-resolution ex vivo DTI integrated into in vivo space , 2017, Brain Structure and Function.

[7]  J. Pauly,et al.  Diffusion‐weighted interleaved echo‐planar imaging with a pair of orthogonal navigator echoes , 1996, Magnetic resonance in medicine.

[8]  Eugene Fiume,et al.  A practical approach to in vivo quantification of physiological cross-sectional area for human skeletal muscle , 2015 .

[9]  Alex J. de Crespigny,et al.  The effects of brain tissue decomposition on diffusion tensor imaging and tractography , 2007, NeuroImage.

[10]  P. Basser,et al.  In vivo measurement of axon diameter distribution in the corpus callosum of rat brain. , 2009, Brain : a journal of neurology.

[11]  S. Skare,et al.  On the effects of gating in diffusion imaging of the brain using single shot EPI. , 2001, Magnetic resonance imaging.

[12]  David K. Yu,et al.  Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography , 2015, Proceedings of the National Academy of Sciences.

[13]  Suliann Ben Hamed,et al.  The Prediction of Impact of a Looming Stimulus onto the Body Is Subserved by Multisensory Integration Mechanisms , 2017, The Journal of Neuroscience.

[14]  R. Deriche,et al.  Regularized, fast, and robust analytical Q‐ball imaging , 2007, Magnetic resonance in medicine.

[15]  J. Pauly,et al.  Isotropic diffusion‐weighted and spiral‐navigated interleaved EPI for routine imaging of acute stroke , 1997, Magnetic resonance in medicine.

[16]  Carl-Fredrik Westin,et al.  Processing and visualization for diffusion tensor MRI , 2002, Medical Image Anal..

[17]  F Fasano,et al.  High Resolution Diffusion-Weighted Imaging in Human at 7T , 2009, NeuroImage.

[18]  Fan Zhang,et al.  Effects of echo time on diffusion quantification of brain white matter at 1.5T and 3.0T , 2009, Magnetic resonance in medicine.

[19]  A. Connelly,et al.  Improved probabilistic streamlines tractography by 2 nd order integration over fibre orientation distributions , 2009 .

[20]  Don H. Johnson,et al.  Signal-to-noise ratio , 2006, Scholarpedia.

[21]  P. Basser,et al.  A simplified method to measure the diffusion tensor from seven MR images , 1998, Magnetic resonance in medicine.

[22]  B. Keil,et al.  An implanted 8-channel array coil for high-resolution macaque MRI at 3T , 2012, NeuroImage.

[23]  Angela R. Laird,et al.  Multi-region hemispheric specialization differentiates human from nonhuman primate brain function , 2013, Brain Structure and Function.

[24]  Hangyi Jiang,et al.  High‐resolution isotropic 3D diffusion tensor imaging of the human brain , 2002, Magnetic resonance in medicine.

[25]  Robin M Heidemann,et al.  High resolution diffusion‐weighted imaging using readout‐segmented echo‐planar imaging, parallel imaging and a two‐dimensional navigator‐based reacquisition , 2009, Magnetic resonance in medicine.

[26]  E. Dumont,et al.  Water excitation as an alternative to fat saturation in MR imaging: preliminary results in musculoskeletal imaging. , 2002, Radiology.

[27]  Jia-Hong Gao,et al.  DWI using navigated interleaved multishot EPI with realigned GRAPPA reconstruction , 2016, Magnetic resonance in medicine.

[28]  Carlo Pierpaoli,et al.  Artifacts in Diffusion MRI , 2010 .

[29]  Hongtu Zhu,et al.  Diffusion tensor imaging-based characterization of brain neurodevelopment in primates. , 2013, Cerebral cortex.

[30]  Yundi Shi,et al.  A diffusion tensor MRI atlas of the postmortem rhesus macaque brain , 2015, NeuroImage.

[31]  P. Boesiger,et al.  SENSE: Sensitivity encoding for fast MRI , 1999, Magnetic resonance in medicine.

[32]  Tong Zhu,et al.  A practical approach to in vivo high-resolution diffusion tensor imaging of rhesus monkeys on a 3-T human scanner. , 2009, Magnetic resonance imaging.

[33]  A. Connelly,et al.  Sampling and reconstruction effects due to motion in diffusion‐weighted interleaved echo planar imaging , 2000, Magnetic resonance in medicine.

[34]  Bruno Brochet,et al.  Selective dentate gyrus disruption causes memory impairment at the early stage of experimental multiple sclerosis , 2017, Brain, Behavior, and Immunity.

[35]  Peter Kellman,et al.  Image reconstruction in SNR units: A general method for SNR measurement † , 2005, Magnetic resonance in medicine.

[36]  Allen W. Song,et al.  Human brain diffusion tensor imaging at submillimeter isotropic resolution on a 3Tesla clinical MRI scanner , 2015, NeuroImage.

[37]  John C Gore,et al.  High‐resolution human diffusion tensor imaging using 2‐D navigated multishot SENSE EPI at 7 T , 2013, Magnetic resonance in medicine.

[38]  R. Ordidge,et al.  Correction of motional artifacts in diffusion-weighted MR images using navigator echoes. , 1994, Magnetic resonance imaging.

[39]  Lawrence L. Wald,et al.  Surface based analysis of diffusion orientation for identifying architectonic domains in the in vivo human cortex , 2013, NeuroImage.

[40]  Allen W. Song,et al.  3D-MB-MUSE: A robust 3D multi-slab, multi-band and multi-shot reconstruction approach for ultrahigh resolution diffusion MRI , 2017, NeuroImage.

[41]  Jean-Michel Verdier,et al.  Lessons from the analysis of nonhuman primates for understanding human aging and neurodegenerative diseases , 2015, Front. Neurosci..

[42]  Frederik Barkhof,et al.  Regional DTI differences in multiple sclerosis patients , 2009, NeuroImage.

[43]  Karla L. Miller,et al.  The extreme capsule fiber complex in humans and macaque monkeys: a comparative diffusion MRI tractography study , 2015, Brain Structure and Function.

[44]  Stefan Skare,et al.  On the signal‐to‐noise ratio efficiency and slab‐banding artifacts in three‐dimensional multislab diffusion‐weighted echo‐planar imaging , 2015, Magnetic resonance in medicine.

[45]  Laurent Petit,et al.  Bundle-Specific Tractography , 2018 .

[46]  Stefan Skare,et al.  How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging , 2003, NeuroImage.

[47]  Jennifer A McNab,et al.  3D steady‐state diffusion‐weighted imaging with trajectory using radially batched internal navigator echoes (TURBINE) , 2010, Magnetic resonance in medicine.

[48]  Bennett A Landman,et al.  Reproducibility and variation of diffusion measures in the squirrel monkey brain, in vivo and ex vivo. , 2017, Magnetic resonance imaging.

[49]  Alan Connelly,et al.  MRtrix: Diffusion tractography in crossing fiber regions , 2012, Int. J. Imaging Syst. Technol..

[50]  H Bruder,et al.  Image reconstruction for echo planar imaging with nonequidistant k‐space sampling , 1992, Magnetic resonance in medicine.

[51]  Jean-Philippe Thiran,et al.  DTI mapping of human brain connectivity: statistical fibre tracking and virtual dissection , 2003, NeuroImage.

[52]  Seong-Gi Kim,et al.  Dose‐dependent effect of isoflurane on neurovascular coupling in rat cerebral cortex , 2009, The European journal of neuroscience.

[53]  Jens Frahm,et al.  Rhesus monkey and human share a similar topography of the corpus callosum as revealed by diffusion tensor MRI in vivo. , 2008, Cerebral cortex.

[54]  A Villringer,et al.  Human Cerebellar Sub-millimeter Diffusion Imaging Reveals the Motor and Non-motor Topography of the Dentate Nucleus , 2016, Cerebral cortex.

[55]  Natasha Lepore,et al.  Fiber estimation and tractography in diffusion MRI: Development of simulated brain images and comparison of multi-fiber analysis methods at clinical b-values , 2015, NeuroImage.

[56]  Murat Aksoy,et al.  Slab profile encoding (PEN) for minimizing slab boundary artifact in three‐dimensional diffusion‐weighted multislab acquisition , 2015, Magnetic resonance in medicine.

[57]  Timothy Edward John Behrens,et al.  Quantitative Investigation of Connections of the Prefrontal Cortex in the Human and Macaque using Probabilistic Diffusion Tractography , 2005, The Journal of Neuroscience.

[58]  E. Heuer,et al.  Nonhuman primate models of Alzheimer-like cerebral proteopathy. , 2012, Current pharmaceutical design.

[59]  Myung-Ho In,et al.  High-resolution diffusion MRI at 7T using a three-dimensional multi-slab acquisition , 2016, NeuroImage.

[60]  Andrew L. Alexander,et al.  A Diffusion-Tensor-Based White Matter Atlas for Rhesus Macaques , 2014, PloS one.

[61]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[62]  Stefan Everling,et al.  Functional subdivisions of medial parieto-occipital cortex in humans and nonhuman primates using resting-state fMRI , 2015, NeuroImage.

[63]  Brian B. Avants,et al.  N4ITK: Improved N3 Bias Correction , 2010, IEEE Transactions on Medical Imaging.

[64]  Arthur W. Toga,et al.  Superficially Located White Matter Structures Commonly Seen in the Human and the Macaque Brain with Diffusion Tensor Imaging , 2011, Brain Connect..

[65]  Michael Schacht Hansen,et al.  Gadgetron: An open source framework for medical image reconstruction , 2013, Magnetic resonance in medicine.

[66]  Krystof S. Bankiewicz,et al.  Striatal volume differences between non-human and human primates , 2009, Journal of Neuroscience Methods.

[67]  Bertrand Audoin,et al.  Structure of WM bundles constituting the working memory system in early multiple sclerosis: A quantitative DTI tractography study , 2007, NeuroImage.

[68]  Stamatios N. Sotiropoulos,et al.  An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging , 2016, NeuroImage.

[69]  David A Porter,et al.  3D Multi‐slab diffusion‐weighted readout‐segmented EPI with real‐time cardiac‐reordered k‐space acquisition , 2014, Magnetic resonance in medicine.

[70]  J. E. Tanner,et al.  Spin diffusion measurements : spin echoes in the presence of a time-dependent field gradient , 1965 .

[71]  Stefan Skare,et al.  Diffusion‐weighted 3D multislab echo planar imaging for high signal‐to‐noise ratio efficiency and isotropic image resolution , 2013, Magnetic resonance in medicine.

[72]  Stephen M. Smith,et al.  DTI measures in crossing-fibre areas: Increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer's disease , 2011, NeuroImage.

[73]  Peter J. Koopmans,et al.  Reducing slab boundary artifacts in three‐dimensional multislab diffusion MRI using nonlinear inversion for slab profile encoding (NPEN) , 2015, Magnetic resonance in medicine.

[74]  C. Jack,et al.  MRI of hippocampal volume loss in early Alzheimer's disease in relation to ApoE genotype and biomarkers , 2008, Brain : a journal of neurology.

[75]  Karla L Miller,et al.  Nonlinear phase correction for navigated diffusion imaging , 2003, Magnetic resonance in medicine.

[76]  Bruno Madore,et al.  Reduced field‐of‐view MRI with two‐dimensional spatially‐selective RF excitation and UNFOLD , 2005, Magnetic resonance in medicine.

[77]  Edward J. Auerbach,et al.  Dose-dependent effect of isoflurane on regional cerebral blood flow in anesthetized macaque monkeys , 2013, Neuroscience Letters.

[78]  D. Pandya,et al.  Fiber Pathways of the Brain , 2006 .

[79]  Alan Connelly,et al.  Robust determination of the fibre orientation distribution in diffusion MRI: Non-negativity constrained super-resolved spherical deconvolution , 2007, NeuroImage.

[80]  K. Whittingstall,et al.  Tractography in the Study of the Human Brain: A Neurosurgical Perspective , 2012, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[81]  Peter Jezzard,et al.  Investigations on the efficiency of cardiac-gated methods for the acquisition of diffusion-weighted images. , 2005, Journal of magnetic resonance.