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 J J Wang
Author Information
  1. Xingfeng Shao: Laboratory of FMRI Technology (LOFT), USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, 2025 Zonal Ave, Los Angeles, CA 90033, USA.
  2. Fanhua Guo: State Key Laboratory of Brain and Cognitive Science, Beijing MRI Center for Brain Research, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China.
  3. Qinyang Shou: Laboratory of FMRI Technology (LOFT), USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, 2025 Zonal Ave, Los Angeles, CA 90033, USA.
  4. Kai Wang: Laboratory of FMRI Technology (LOFT), USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, 2025 Zonal Ave, Los Angeles, CA 90033, USA.
  5. Kay Jann: Laboratory of FMRI Technology (LOFT), USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, 2025 Zonal Ave, Los Angeles, CA 90033, USA; Department of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA.
  6. Lirong Yan: Laboratory of FMRI Technology (LOFT), USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, 2025 Zonal Ave, Los Angeles, CA 90033, USA; Department of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA.
  7. Arthur W Toga: Laboratory of Neuroimaging, USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA.
  8. Peng Zhang: State Key Laboratory of Brain and Cognitive Science, Beijing MRI Center for Brain Research, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China.
  9. Danny J J Wang: Laboratory of FMRI Technology (LOFT), USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, 2025 Zonal Ave, Los Angeles, CA 90033, USA; Department of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA. Electronic address: JJ.Wang@loni.usc.edu.

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 (pCASL) technique at 7T that offers the 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 ms shorter than in middle/deep layers revealing the time course 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). This observation is highly consistent with reported laminar profiles of CBV activation on M1. We further demonstrated that visuospatial 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 stimulus driven activity peaked in the middle layers (feedforward thalamic input). With the capability for quantitative CBF measurements both at baseline and during task activation, high-resolution ASL perfusion fMRI at 7T provides an important tool for in vivo assessment of neurovascular function and metabolic activities of neural circuits across cortical layers.

Keywords

References

  1. AJNR Am J Neuroradiol. 2007 Sep;28(8):1480-5 [PMID: 17846195]
  2. Magn Reson Imaging. 2017 Jan;35:20-28 [PMID: 27580519]
  3. Neuroimage. 2020 Feb 15;207:116358 [PMID: 31740341]
  4. Magn Reson Med. 2010 Feb;63(2):374-84 [PMID: 19953506]
  5. J Cereb Blood Flow Metab. 2020 Sep;40(9):1823-1837 [PMID: 31429358]
  6. Neuroimage. 2009 Oct 15;48(1):63-72 [PMID: 19573611]
  7. Proc Natl Acad Sci U S A. 2007 Jan 2;104(1):365-70 [PMID: 17190804]
  8. Neuroimage. 2010 Jan 15;49(2):1340-9 [PMID: 19800013]
  9. PLoS One. 2012;7(3):e32536 [PMID: 22448223]
  10. Magn Reson Med. 2022 Jan;87(1):207-219 [PMID: 34411335]
  11. Magn Reson Med. 2003 Aug;50(2):263-74 [PMID: 12876702]
  12. Magn Reson Med. 2002 May;47(5):903-11 [PMID: 11979569]
  13. Magn Reson Med. 2016 Jul;76(1):270-81 [PMID: 26285144]
  14. NMR Biomed. 1997 Jun-Aug;10(4-5):216-21 [PMID: 9430351]
  15. Clin Neurophysiol. 2002 May;113(5):621-34 [PMID: 11976042]
  16. PLoS One. 2021 Apr 26;16(4):e0250504 [PMID: 33901230]
  17. Neuroimage. 2017 Aug 1;156:363-376 [PMID: 28528845]
  18. Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10904-9 [PMID: 11526212]
  19. Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):13081-6 [PMID: 14569029]
  20. Cereb Cortex. 1991 Jan-Feb;1(1):1-47 [PMID: 1822724]
  21. NMR Biomed. 1997 Jun-Aug;10(4-5):237-49 [PMID: 9430354]
  22. NMR Biomed. 2011 Dec;24(10):1313-25 [PMID: 21608057]
  23. J Cereb Blood Flow Metab. 2014 Oct;34(10):1585-98 [PMID: 25052556]
  24. J Cereb Blood Flow Metab. 1996 Nov;16(6):1236-49 [PMID: 8898697]
  25. Nature. 2006 Oct 12;443(7112):700-4 [PMID: 17036005]
  26. Nat Neurosci. 2008 Mar;11(3):360-6 [PMID: 18246064]
  27. Curr Biol. 2020 May 4;30(9):1721-1725.e3 [PMID: 32220318]
  28. Neuroimage. 2014 Jun;93 Pt 2:210-20 [PMID: 23603284]
  29. Magn Reson Med. 2017 Jan;77(1):434-443 [PMID: 27770469]
  30. Neuroimage. 2015 Feb 15;107:23-33 [PMID: 25479018]
  31. PLoS One. 2013 Jun 20;8(6):e66612 [PMID: 23818950]
  32. J Cereb Blood Flow Metab. 2013 May;33(5):635-48 [PMID: 23443173]
  33. Neuroimage. 2010 Oct 1;52(4):1334-46 [PMID: 20460157]
  34. Behav Res Methods. 2013 Mar;45(1):83-97 [PMID: 22806703]
  35. Curr Biol. 2007 Jun 19;17(12):R443-9 [PMID: 17580069]
  36. Magn Reson Med. 2021 May;85(5):2490-2506 [PMID: 33231890]
  37. Magn Reson Med. 2004 Dec;52(6):1407-17 [PMID: 15562477]
  38. Front Neuroenergetics. 2010 May 21;2: [PMID: 20725515]
  39. Magn Reson Med. 2002 Aug;48(2):242-54 [PMID: 12210932]
  40. NMR Biomed. 2013 Jan;26(1):65-73 [PMID: 22674638]
  41. Nature. 2014 Apr 3;508(7494):55-60 [PMID: 24670647]
  42. Brain. 1997 Jan;120 ( Pt 1):141-57 [PMID: 9055804]
  43. Magn Reson Med. 2020 Dec;84(6):3128-3145 [PMID: 32557752]
  44. Neurobiol Aging. 2013 Apr;34(4):1018-31 [PMID: 23084084]
  45. Neuron. 2015 Dec 16;88(6):1086-1107 [PMID: 26687219]
  46. Front Neurosci. 2015 May 05;9:163 [PMID: 25999810]
  47. Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):11050-5 [PMID: 10984517]
  48. Neuroimage. 2019 Aug 15;197:742-760 [PMID: 28736310]
  49. Neuroimage. 2008 Feb 1;39(3):936-48 [PMID: 17997329]
  50. Magn Reson Med. 2016 Feb;75(2):801-9 [PMID: 25820458]
  51. Comput Biomed Res. 1996 Jun;29(3):162-73 [PMID: 8812068]
  52. Magn Reson Med. 2015 Jan;73(1):102-16 [PMID: 24715426]
  53. Magn Reson Imaging. 2013 Apr;31(3):477-9 [PMID: 23102945]
  54. Radiology. 1985 Sep;156(3):743-7 [PMID: 4023236]
  55. Neuroimage. 2021 Aug 15;237:118091 [PMID: 33991698]
  56. Brain Res Bull. 1981 Nov;7(5):519-79 [PMID: 7317796]
  57. J Magn Reson Imaging. 2015 Feb;41(2):266-95 [PMID: 24737382]
  58. Nat Commun. 2020 Aug 6;11(1):3925 [PMID: 32764538]
  59. Neuroimage. 2007 Jan 1;34(1):74-84 [PMID: 17011213]
  60. Magn Reson Med. 2009 Apr;61(4):874-82 [PMID: 19189295]
  61. J Cereb Blood Flow Metab. 2008 Mar;28(3):640-52 [PMID: 17960143]
  62. Neuron. 2011 Oct 6;72(1):111-23 [PMID: 21982373]
  63. J Cereb Blood Flow Metab. 2021 Aug;41(8):1899-1911 [PMID: 33444098]
  64. Neuroimage. 2020 Jan 1;204:116209 [PMID: 31546051]
  65. PLoS Biol. 2006 Feb;4(2):e22 [PMID: 16379497]
  66. Diabetologia. 2015 Apr;58(4):666-77 [PMID: 25512003]
  67. Neuroimage. 2020 Feb 1;206:116337 [PMID: 31707191]
  68. Eye Brain. 2014 Sep;2014(6 Suppl 1):5-18 [PMID: 25788835]
  69. Neuron. 2017 Dec 20;96(6):1253-1263.e7 [PMID: 29224727]
  70. J Magn Reson Imaging. 2019 May;49(5):1253-1262 [PMID: 30328209]
  71. Magn Reson Med. 2017 Oct;78(4):1405-1419 [PMID: 27813164]
  72. Neuroimage. 2015 Feb 1;106:111-22 [PMID: 25463468]
  73. Neuroimage. 2002 Mar;15(3):488-500 [PMID: 11848692]
  74. J Cereb Blood Flow Metab. 2013 Dec;33(12):1825-37 [PMID: 24064495]
  75. J Physiol. 1961 Dec;159:203-21 [PMID: 13883391]
  76. Magn Reson Med. 2003 May;49(5):796-802 [PMID: 12704760]
  77. Neuroimage. 2011 Jun 1;56(3):1276-85 [PMID: 21338697]
  78. Prog Neurobiol. 2021 Dec;207:101897 [PMID: 32818495]
  79. Magn Reson Med. 2007 Nov;58(5):1020-7 [PMID: 17969096]
  80. Magn Reson Med. 1998 Sep;40(3):383-96 [PMID: 9727941]
  81. Magn Reson Med. 2014 Jun;71(6):2035-42 [PMID: 23843129]
  82. Neuroimage. 2009 Feb 1;44(3):839-48 [PMID: 18976717]
  83. Neuroimage Clin. 2013 Jul 06;3:1-7 [PMID: 24159561]
  84. Magn Reson Med. 2022 Jan;87(1):249-262 [PMID: 34427341]
  85. Neurophotonics. 2015 Apr;2(2):025006 [PMID: 26158010]

Grants

  1. U01 AG051218/NIA NIH HHS
  2. R01 EB028297/NIBIB NIH HHS
  3. S10 OD025312/NIH HHS
  4. UF1 NS100614/NINDS NIH HHS
  5. R01 EB032169/NIBIB NIH HHS
  6. UH3 NS100614/NINDS NIH HHS
  7. P41 EB015922/NIBIB NIH HHS
  8. R01 NS114382/NINDS NIH HHS

MeSH Term

Adult
Brain Mapping
Cerebrovascular Circulation
Female
Humans
Imaging, Three-Dimensional
Magnetic Resonance Imaging
Male
Motor Cortex
Perfusion Imaging
Signal Processing, Computer-Assisted
Spin Labels
Visual Cortex

Chemicals

Spin Labels

Word Cloud

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