Maria Marcella Lagana1, Laura Pelizzari1,2, Alice Pirastru1, Niels Bergsland1,3, Mario Clerici1,4, Pietro Cecconi5, and Francesca Baglio1
1Fondazione Don Carlo Gnocchi ONLUS, Milan, Italy, 2Department of Electronics, Information and Bioengineering, Politecnico di Milano, Milan, Italy, 3Buffalo Neuroimaging Analysis Center, Department of Neurology, School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, NY, United States, 4Università degli Studi di Milano, Milan, Italy, 5Radiology, Fondazione Don Carlo Gnocchi ONLUS, Milan, Italy
Synopsis
In this study, we aimed to assess the
consistency of the perfusion patterns that can be extracted using independent
component analysis (ICA) on cerebral blood flow (CBF) maps derived from
arterial spin labeling (ASL) data. Furthermore, we aimed to evaluate the
similarity between the CBF-derived components and the well-known spatial
patterns of functional MRI resting state networks (RSN) and cerebral vascular
territories (VT). Our results showed that good spatial constancy of perfusion
patterns can be extracted from CBF maps. Almost all the derived components
overlapped with RSN or specific VT.
INTRODUCTION
Arterial spin labeling (ASL) provides the opportunity to detect resting
state functional networks (RSN), which are commonly extracted from blood
oxygenated-dependent (BOLD) data1. Furthermore, previous studies
showed that cerebral vascular
territories (VT) could be mapped by specifically tagging
major
arteries supplying the brain2. In this study, we aimed to assess the
consistency of the perfusion patterns that can be extracted using independent
component analysis (ICA) on cerebral blood flow (CBF) maps of healthy controls
(HC), and to evaluate the similarity between the CBF-derived components and the
well-known spatial patterns of RSN and VT.METHODS
Sixty-five HC (mean age= 42.5±18.4, 30
females) (whole group - G) were imaged on a 1.5 Siemens scanner. The
acquisition protocol included a high resolution T1-weighted image(TR=1900 ms, TE=3.37 ms, resolution=1×1×1 mm3, 176
axial slices) and a multi-delay pseudo-continuous ASLwith background suppressed
GRASE sequence (TR/TE=3500/22.58 ms, labeling duration=1500 ms, 5
post-labelling delays=[700, 1200, 1700, 2200, 2700] ms, 12 pairs of tag/control
images for each delay, resolution=3.5x3.5x5 mm3, 32 slices). ASL data were preprocessed (i.e. re-alignment,
motion correction and partial volume correction), and gray matter CBF maps were
computed3. Then, CBF maps were
aligned to the corresponding T1-weighted images and registered to MNI standard
space4.
In order to test perfusion pattern consistency, the 65 HC were randomly
split in two age and sex-matched groups (G1 and G2, consisting of 33 and 32 HC respectively).
ICA (dimensionality=10) was performed5 on G1 and G2 data
separately. Reliability of obtained ICs was
assessed with Icasso6 (stability index ≥ 0.8). The reliable components (ICs) were visually compared between
G1 and G2, in order to verify if corresponding CBF pattern could be identified
in both the groups independently. Furthermore, Dice Similarity index (DSI) was
computed between ICsG1 and ICsG2 to quantify the overlap
between matching ICs7,8. Once assessed the consistency
of the CBF patterns, ICA (dimensionality=15) was run on the whole G-dataset. ICA
with higher dimensionality with respect to G1/G2 analysis was allowed by the
bigger sample size. The obtained reliable ICs were visually and quantitatively (i.e.
with DSI) compared to Smith’s RSN template9 and to a VT atlas. The used
VT atlas identified areas supplied by left and right anterior, middle and
posterior cerebral arteries (ACA, MCA and PCA respectively).10RESULTS
Nine out of ten ICsG1 and ICsG2 were
classified as stable. For all reliable components, ICG1-ICG2
pairs showing similar perfusion patterns were visually recognized (Figure 1). According
to DSI, the matching was classified as fair/moderate8 for five out
of nine ICs (IC00G1-IC00G2, DSI=0.64; IC01G1-IC05G2,
DSI=0.45; IC04G1-IC03G2, DSI=0.43; IC06G1-
IC03G2, DSI=0.48; IC07G1-IC08G2, DSI=0.31).
ICA performed on G-dataset resulted in eleven out of fifteen
reliable ICs (Figure 2). At the visual inspection, IC00G was not
classified neither as a VT nor as a RSN. IC01G was classified as
visual RSN (DSI=0.43) and right PCA VT (DSI=0.34) (Figure 3). IC02G partially
overlapped with executive RSN (DSI<0.30), with the frontal portion of the two
fronto-parietal RSNs (DSI<0.30), and with right MCA VT (DSI=0.34). IC03G
was classified as right fronto-parietal RSN (DSI=0.42) and right MCA VT (DSI=0.93).
IC04G overlapped with default mode network (DSI=0.31) and left MCA VT
(DSI=0.56). IC05G was identified as sensory-motor RSN (DSI<0.3),
while IC06G and IC07G overlapped to visual RSN (DSI<0.30
and DSI=0.41 respectively). IC09G overlapped to auditory RSN (DSI=0.42),
and left and right MCA VT (DSI=0.32 and 0.58 respectively). IC08G
and IC10G were identified as cerebellum ICs but did not overlap with
any of Smith’s RSN or VT.DISCUSSION
ICsG1 vs
ICsG2 comparison showed good consistency of the perfusion patterns that
can be identified by performing ICA on HC CBF maps. The majority of ICsG
could be visually matched with either a RSN or a VT, and showed fair/moderate
overlap with them8. Although presenting DSI<0.30 with any RSN/VT,
IC05G could be identified as sensory motor RSN pattern at the visual
inspection. IC00G clearly represented the white matter still
included in the used gray matter mask, thus it could be considered as a
component of no interest. Finally, IC08G and IC10G
represented perfusion pattern of the cerebellum that is known to be supplied by
vertebral arteries11, but which is not included in the used VT atlas.CONCLUSIONS
ICA performed on ASL data allows to
consistently identify robust common perfusion patterns, similar to either RSN or
specific VT. Therefore, this approach could be used to investigate the coupling
strength between perfusion, function and the inflow from major cerebral
arteries.Acknowledgements
This study was in part funded by
a grant awarded by the Annette Funicello Research Fund for Neurological
Diseases.
Prof. Danny JJ Wang (UCLA, CA, USA) provided us with the pCASL sequence.
References
1. Dai W, Varma G, Scheidegger R, Alsop DC. Quantifying fluctuations of resting state networks
using arterial spin labeling perfusion MRI. Journal of Cerebral Blood Flow
& Metabolism 2016. 36(3):463-73.
2. Paiva FF, Tannús A, Talagala SL, Silva AC. Arterial spin labeling of cerebral perfusion
territories using a separate labeling coil. Journal of Magnetic Resonance
Imaging 2008. 1;27(5):970-7.
3. Chappell MA, Groves AR, Whitcher
B, Woolrich MW. Variational Bayesian inference for a nonlinear forward model.
IEEE Transactions on Signal Processing. 2009;57(1):223-36.
4. Avants BB, Tustison N, Song G.
Advanced normalization tools (ANTS). Insight j. 2009;2:1-35.
5. Beckmann, C.F. and S.M. Smith,
Probabilistic independent component analysis for functional magnetic resonance
imaging. IEEE Trans Med Imaging. 2004. 23(2): p. 137-52.
6. Himberg J, Hyvarinen A. Icasso:
software for investigating the reliability of ICA estimates by clustering and
visualization. InNeural Networks for Signal Processing, 2003. NNSP'03. 2003
IEEE 13th Workshop on 2003 Sep 17 (pp. 259-268). IEEE.
7. Zhu S, Fang Z, Hu S, Wang Z, Rao H. Resting
state brain function analysis using concurrent BOLD in ASL perfusion fMRI. PloS
one 2013. 4;8(6):e65884.
8. Zijdenbos AP, Dawant BM, Margolin
RA, Palmer AC. Morphometric analysis of white matter lesions in MR images:
method and validation. IEEE transactions on medical imaging 1994.13(4):716-24.
9. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM,
Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF.
Correspondence of the brain's functional architecture during activation and rest.
Proceedings of the National Academy of Sciences 2009. Aug 4;106(31):13040-5.
10. Tatu L, Moulin T, Bogousslavsky
J, Duvernoy H. Arterial territories of the human brain cerebral hemispheres.
Neurology 1998. 1;50(6):1699-708.
11. Kansagra AP, Wong EC. Mapping of vertebral artery
perfusion territories using arterial spin labeling MRI. Journal of Magnetic
Resonance Imaging 2008.1;28(3):762-6.