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Laminar perfusion imaging with zoomed arterial spin labeling at 7 Tesla

Xingfeng Shao, Fanhua Guo, Qinyang Shou, Kai Wang, Kay Jann, Lirong Yan, View ORCID ProfileArthur W. Toga, Peng Zhang, Danny JJ Wang
doi: https://doi.org/10.1101/2021.04.13.439689
Xingfeng Shao
aLaboratory of FMRI Technology (LOFT), USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA
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Fanhua Guo
bState Key Laboratory of Brain and Cognitive Science, Beijing MRI Center for Brain Research, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
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Qinyang Shou
aLaboratory of FMRI Technology (LOFT), USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA
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Kai Wang
aLaboratory of FMRI Technology (LOFT), USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA
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Kay Jann
aLaboratory of FMRI Technology (LOFT), USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA
cDepartment of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA
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Lirong Yan
aLaboratory of FMRI Technology (LOFT), USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA
cDepartment of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA
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Arthur W. Toga
dLaboratory of Neuroimaging, USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA
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  • ORCID record for Arthur W. Toga
Peng Zhang
bState Key Laboratory of Brain and Cognitive Science, Beijing MRI Center for Brain Research, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
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Danny JJ Wang
aLaboratory of FMRI Technology (LOFT), USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA
cDepartment of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA
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  • For correspondence: JJ.Wang@loni.usc.edu
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Abstract

Laminar fMRI based on BOLD and CBV contrast at ultrahigh magnetic fields has been applied for studying the dynamics of mesoscopic brain networks. However, the quantitative interpretations of BOLD/CBV fMRI results are confounded by different baseline physiology across cortical layers. Here we introduce a novel 3D zoomed pseudo-continuous arterial spin labeling technique at 7T that offers the unique capability for quantitative measurements of laminar cerebral blood flow (CBF) both at rest and during task activation with high spatial specificity and sensitivity. We found arterial transit time in superficial layers is ∼100 msec shorter than in middle/deep layers revealing the dynamics of labeled blood flowing from pial arteries to downstream microvasculature. Resting state CBF peaked in the middle layers which is highly consistent with microvascular density measured from human cortex specimens. Finger tapping induced a robust two-peak laminar profile of CBF increases in the superficial (somatosensory and premotor input) and deep (spinal output) layers of M1, while finger brushing task induced a weaker CBF increase in superficial layers (somatosensory input). We further demonstrated that top-down attention induced a predominant CBF increase in deep layers and a smaller CBF increase on top of the lower baseline CBF in superficial layers of V1 (feedback cortical input), while bottom-up stimulus driven activity peaked in the middle layers (feedforward thalamic input). These quantitative laminar profiles of perfusion activity suggest an important role of M1 superficial layers for the computation of finger movements, and that visual attention may amplify deep layer output to the subcortex.

Significance Statement CBF or microvascular perfusion measured by arterial spin labeling (ASL) is a key parameter for in vivo assessment of neurovascular function. Compared to BOLD or VASO fMRI, ASL perfusion contrast offers the unique capability for quantitative CBF measurements both at baseline and during task activation, which is critical for quantitative estimation of metabolic activities tightly related to neuronal activation. We proposed a zoomed 3D ASL technique at 7T for laminar perfusion imaging with high spatial specificity and sensitivity. This technique is able to differentiate and quantify the input/output and feedforward/feedback activities of human motor and visual cortex, thereby providing an important tool for quantitative assessment of neurovascular function and metabolic activities of neural circuits across cortical layers.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Author Contributions: X.S. implemented the MRI pulse sequence, conducted the experiments and data analysis. D.W., P.Z and A.T. provided advice on experimental design and research direction. X.S., D.W. and P.Z. designed the experiments. F.G., Q.S., K.W., L.Y. and K.J. provided input on the design of the analysis. All authors wrote the manuscript.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 14, 2021.
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Laminar perfusion imaging with zoomed arterial spin labeling at 7 Tesla
Xingfeng Shao, Fanhua Guo, Qinyang Shou, Kai Wang, Kay Jann, Lirong Yan, Arthur W. Toga, Peng Zhang, Danny JJ Wang
bioRxiv 2021.04.13.439689; doi: https://doi.org/10.1101/2021.04.13.439689
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Laminar perfusion imaging with zoomed arterial spin labeling at 7 Tesla
Xingfeng Shao, Fanhua Guo, Qinyang Shou, Kai Wang, Kay Jann, Lirong Yan, Arthur W. Toga, Peng Zhang, Danny JJ Wang
bioRxiv 2021.04.13.439689; doi: https://doi.org/10.1101/2021.04.13.439689

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