Hansol Lee1, Yixin Ma1, Gabriel Ramos-Llordén1, Kwok-Shing Chan1, Eva A. Krijnen2,3, Mirsad Mahmutovic4, Boris Keil4,5, Eric C. Klawiter2, Hong-Hsi Lee1, and Susie Y. Huang1
1Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Charlestown, MA, United States, 2Department of Neurology, Massachusetts General Hospital, Boston, MA, United States, 3MS Center Amsterdam, Anatomy and Neurosciences, Amsterdam Neuroscience, Amsterdam UMC location VUmc, Amsterdam, Netherlands, 4Institute of Medical Physics and Radiation Protection, Mittelhessen University of Applied Sciences, Giessen, Germany, 5Department of Diagnostic and Interventional Radiology, University Hospital Marburg, Philipps University of Marburg, Marburg, Germany
Synopsis
Keywords: Gray Matter, Diffusion/other diffusion imaging techniques, Gray matter, High-performance gradient system
Motivation: The Connectome 2.0 MRI scanner equipped with 500 mT/m gradient strength and 600 T/m/s slew rate is expected to advance gray matter microstructural characterization within the living human brain.
Goal(s): To compare Soma And Neurite Density imaging (SANDI) metrics obtained from Connectome 2.0 and 1.0.
Approach: We applied SANDI model fitting to diffusion MRI data acquired from 10 healthy subjects scanned on the Connectome 2.0 and 1.0 scanners.
Results: We observed lower soma radius throughout the cortex on Connectome 2.0 compared to Connectome 1.0. SANDI metrics from Connectome 2.0 exhibited considerable contrast within the sensorimotor cortex that wasn’t apparent on Connectome 1.0.
Impact: The Connectome 2.0
MRI scanner with 500 mT/m gradients advances non-invasive characterization of
gray matter microstructure in the living human brain and enables mapping of real
differences in cyto- and myeloarchitecture with greater sensitivity compared to
the original Connectome scanner.
Introduction
Dedicated high-performance gradient systems offer many advantages for
diffusion MRI over conventional clinical MRI scanners equipped with lower
gradient strengths, including more efficient diffusion encoding and greater
sensitivity toward cellular and axonal microstructural features at fine
diffusion length scales. The original Connectome MRI scanner (Connectome 1.0) made
significant strides toward mapping connectional anatomy and microstructural
imaging in the living human brain, yet only accessed a portion of the full range
of scales necessary for investigating the brain’s microscopic and mesoscopic
structure. The recently installed Connectome 2.0 scanner is a cutting-edge MRI
scanner, featuring a maximum gradient strength of 500 mT/m and slew rate of 600
T/m/s,1 and offers a unique tool for evaluating gray matter
microstructure in the living human brain. Soma and Neurite Density Imaging
(SANDI) is a novel biophysical model estimating the contribution of soma
radius, soma fraction, and neurite fraction to diffusion MRI signal.2
In this study, we performed an initial comparative study of SANDI metrics in
the brain obtained from the Connectome 2.0 and Connectome 1.0 scanners in
healthy individuals.Methods
10 healthy adults (34.1±7.2 years, 9 female) were scanned on the 3T
Connectome 2.0 MRI scanner (MAGNETOM Connectom.X, Siemens Healthineers,
Erlangen, Germany) (Gmax=500 mT/m, SRmax=600
T/m/s) using a custom-built 72-channel in vivo head coil.3 10
age- and sex-matched healthy adults (34.5±6.6 years, 9 female) were scanned on the 3T
Connectome MRI scanner (MAGNETOM Connectom, Siemens Healthcare) (Gmax=300
mT/m, SRmax=200 T/m/s). Diffusion-weighted images were obtained
using a pulsed gradient spin-echo echo-planar-imaging sequence on each scanner using
the minimum accessible diffusion time (Δ=13 ms on C2.0 and Δ=19 ms on C1.0) and 8 b-values linearly spaced in
gradient strength up to Gmax (see parameters listed in Figure
1). 3D T1-magnetization-repared rapid acquisition with
gradient echo (MEMPRAGE) was acquired for cortical surface reconstruction and
segmentation using Freesurfer4 and co-registered to diffusion MRI
space.
Diffusion MRI data were preprocessed to correct for susceptibility and
eddy current-induced artifacts.5 The SANDI model was fitted to the
diffusion MRI data using the SANDI MATLAB toolbox.6 The resulting parametric
maps of soma radius and signal fractions of intra-soma and intra-neurite spaces
were projected onto the Freesurfer-averaged inflated cortical surface and
averaged across the 10 subjects scanned on each scanner. A comparison between SANDI
metrics from the Connectome 2.0 and Connectome 1.0 scanners was performed using
the Mann-Whitney U test.Results
SANDI maps calculated from Connectome 2.0
data showed higher values for intra-neurite signal fraction and lower estimated
soma radius across all cortical gray matter areas compared to Connectome 1.0 (P-values
< 0.001) (Figure 2). Averaged soma radius, intra-soma and intra-neurite
signal fraction maps from the SANDI model are presented on the inflated
cortical surface in Figure 3, labeled with sensorimotor cortex encompassing
primary motor cortex (Brodmann’s areas 4 anterior (4a) and 4 posterior (4p))
and somatosensory cortex (Brodmann’s areas 3a, 3b, and 1). Sensorimotor
cortex showed apparent differences in contrast between Connectome 2.0 and
Connectome 1.0. Specifically, a higher intra-soma signal fraction was observed in
primary motor cortex (4a and 4p) compared to area 3b of somatosensory
cortex in the Connectome 2.0 data (Figure 4). This pattern was not
observed in the Connectome 1.0 data. The intra-neurite signal fraction in primary
motor cortex (4a and 4p) was also higher than in somatosensory cortex (3b
and 1) in both datasets, which is consistent with observations from histology.7Discussions & Conclusion
In this study, we performed SANDI model-fitting on diffusion MRI data
acquired on the Connectome 2.0 and Connectome 1.0 scanners and examined
differences in cortical gray matter microstructure in the primary motor and somatosensory
cortex. The estimated soma radius in the Connectome 2.0 data was lower than
that in the Connectome 1.0 data, in line with the greater sensitivity of higher
Gmax to smaller compartment sizes.8 The higher
intra-neurite signal fractions observed in the Connectome 2.0 data may be
attributed to the shorter diffusion times accessible on the Connectome 2.0
protocol. Since the SANDI model does not account for the inter-compartmental
water exchange,2 using shorter diffusion times mitigates the effect
of water exchange on the estimated signal fractions. Moreover, the SANDI maps
on Connectome 2.0 show considerable contrast in intra-soma and intra-neurite
signal fractions within the primary motor and somatosensory cortex. The
Connectome 2.0 scanner features the world’s highest maximum gradient strength
and slew rate for in vivo human scans, enabling access to shorter
diffusion times, gradient pulse durations, and echo times. We envision these
enhanced capabilities will increase our sensitivity to inter-subject
differences in gray matter microstructure, as exemplified through these early
results on gray matter microstructural mapping.Acknowledgements
This work was supported by the National Institute of Biomedical
Imaging and Bioengineering of the National Institutes of Health under award
numbers U01EB026996 and P41EB030006 and by the Office of the Director and the National
Institute of Dental & Craniofacial Research of the National Institutes of
Health under award number DP5OD031854.References
1.
Huang
SY, Witzel T, Keil B, et al. Connectome 2.0: Developing the next-generation ultra-high gradient
strength human MRI scanner for bridging studies of the micro-, meso-and
macro-connectome. 2021;243:118530.
2. Palombo M, Ianus A, Guerreri M, et al. SANDI: a
compartment-based model for non-invasive apparent soma and neurite imaging by
diffusion MRI. NeuroImage. 2020;215:116835.
3. Mahmutovic M, Shrestha M, Ramos-Llordén G, et al. A 72-channel
Head Coil with an Integrated 16-Channel Field Camera for the Connectome 2.0
Scanner. Submitted to ISMRM 2024.
4. Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis: I. Segmentation and surface reconstruction. Neuroimage. 1999;9(2):179-194.
5. Tian Q, Fan Q, Witzel T, et
al. Comprehensive diffusion MRI dataset for in vivo human brain microstructure
mapping using 300 mT/m gradients. Scientific Data. 2022;9(1),7.
6.
https://github.com/palombom/SANDI-Matlab-Toolbox
7. Geyer S, Schleicher A, Zilles K. Areas 3a, 3b,
and 1 of human primary somatosensory cortex: 1. Microstructural organization
and interindividual variability. Neuroimage. 1999;10(1):63-83.
8. Afzali M, Nilsson M,
Palombo M, et al. SPHERIOUSLY? The challenges of estimating sphere radius
non-invasively in the human brain from diffusion MRI. Neuroimage. 2021;237:118183.