Cerebral blood volume changes during brain activation

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 8, 2012, Pages 1618-1631

  Krieger, Steffen Norbert ^a   Streicher, Markus Nikolar ^a   Trampel, Robert ^a   Turner, Robert ^a  

^a MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

Author keywords

blood brain barrier; capillaries; cerebral blood flow; cerebral hemodynamics; mathematical modeling; physiology

Indexed keywords

ARTICLE; BRAIN; BRAIN BLOOD VESSEL; BRAIN BLOOD VOLUME; BRAIN NERVE CELL; CAPILLARY WALL; ERYTHROCYTE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; INTRACRANIAL PRESSURE; MATHEMATICAL MODEL; MICROSCOPY; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; YOUNG MODULUS;

BLOOD VOLUME; BRAIN; CAPILLARIES; CEREBROVASCULAR CIRCULATION; ELASTICITY; HUMANS; MODELS, BIOLOGICAL; PERMEABILITY;

EID: 84864544620     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2012.63     Document Type: Article

References (84)

1. An H, Lin W (2002a) Cerebral venous and arterial blood volumes can be estimated separately in humans using magnetic resonance imaging. Magn Reson Med 48:583-8
2. An H, Lin W (2002b) Cerebral oxygen extraction fraction and cerebral venous blood volume measurements using MRI: effects of magnetic field variation. Magn Reson Med 47:958-66
3. Ances BM, Leontiev O, Perthen JE, Liang C, Lansing AE, Buxton RB (2008) Regional differences in the coupling of cerebral blood flow and oxygen metabolism changes in response to activation: implications for BOLD-fMRI. NeuroImage 39:1510-21
4. Asgari S, Bergsneider M, Hamilton R, Vespa P, Hu X (2010) Consistent changes in intracranial pressure waveform morphology induced by acute hypercapnic cerebral vasodilatation. Neurocrit Care 15:55-62
5. Berwick J, Johnston D, Jones M, Martindale J, Redgrave P, McLoughlin N, Schiessl I, Mayhew JE (2005) Neurovascular coupling investigated with two-dimensional optical imaging spectroscopy in rat whisker barrel cortex. Eur J Neurosci 22:1655-66
6. Blockley NP, Driver ID, Fisher JA, Francis ST, Gowland PA (2012a) Measuring venous blood volume changes during activation using hyperoxia. NeuroImage 59: 3266-74
7. Blockley NP, Griffeth VE, Buxton RB (2012b) A general analysis of calibrated BOLD methodology for measuring CMRO(2) responses: comparison of a new approach with existing methods. NeuroImage 60:279-89
8. Buxton RB (2010) Interpreting oxygenation-based neuroimaging signals: the importance and the challenge of understanding brain oxygen metabolism. Front Neuroenerget 2:8
9. Buxton RB, Wong EC, Frank LR (1998) Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magn Reson Med 39:855-64
10. Buxton RB (2009) Introduction to Functional Magnetic Resonance Imaging: Principles and Techniques, 2nd edn Cambridge: Cambridge University Press
11. Chen JJ, Pike GB (2009) BOLD-specific cerebral blood volume and blood flow changes during neuronal activation in humans. NMR Biomed 22:1054-62
12. Chiarelli PA, Bulte DP, Wise R, Gallichan D, Jezzard P (2007) A calibration method for quantitative BOLD fMRI based on hyperoxia. NeuroImage 37:808-20
13. Davis TL, Kwong KK, Weisskoff RM, Rosen BR (1998) Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc Natl Acad Sci USA 95: 1834-9
14. Devor A, Hillman EM, Tian P, Waeber C, Teng IC, Ruvinskaya L, Shalinsky MH, Zhu H, Haslinger RH, Narayanan SN, Ulbert I, Dunn AK, Lo EH, Rosen BR, Dale AM, Kleinfeld D, Boas DA (2008) Stimulusinduced changes in blood flow and 2-deoxyglucose uptake dissociate in ipsilateral somatosensory cortex. J Neurosci 28:14347-57
15. Devor A, Tian P, Nishimura N, Teng IC, Hillman EM, Narayanan SN, Ulbert I, Boas DA, Kleinfeld D, Dale AM (2007) Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal. J Neurosci 27:4452-9
16. Donahue MJ, Blicher JU, Ostergaard L, Feinberg DA, MacIntosh BJ, Miller KL, Gunther M, Jezzard P (2009) Cerebral blood flow, blood volume, and oxygen metabolism dynamics in human visual and motor cortex as measured by whole-brain multi-modal magnetic resonance imaging. J Cereb Blood Flow Metab 29:1856-66
17. Donahue MJ, Sideso E, MacIntosh BJ, Kennedy J, Handa A, Jezzard P (2010) Absolute arterial cerebral blood volume quantification using inflow vascular-space-occupancy with dynamic subtraction magnetic resonance imaging. J Cereb Blood Flow Metab 30:1329-42
18. Drew PJ, Shih AY, Kleinfeld D (2011) Fluctuating and sensory-induced vasodynamics in rodent cortex extend arteriole capacity. Proc Natl Acad Sci USA 108:8473-8
19. Duelli R, Kuschinsky W (1993) Changes in brain capillary diameter during hypocapnia and hypercapnia. J Cereb Blood Flow Metab 13:1025-8
20. Farkas E, De Jong GI, Apro E, Keuker JI, Luiten PG (2001) Calcium antagonists decrease capillary wall damage in aging hypertensive rat brain. Neurobiol Aging 22: 299-309
21. Feihl F, Perret C (1994) Permissive hypercapnia. How permissive should we be? Am J Respir Crit Care Med 150:1722-37
22. Fernandez-Klett F, Offenhauser N, Dirnagl U, Priller J, Lindauer U (2010) Pericytes in capillaries are contractile in vivo, but arterioles mediate functional hyperemia in the mouse brain. Proc Natl Acad Sci USA 107: 22290-22295
23. Frahm J, Baudewig J, Kallenberg K, Kastrup A, Merboldt KD, Dechent P (2008) The post-stimulation undershoot in BOLD fMRI of human brain is not caused by elevated cerebral blood volume. NeuroImage 40:473-81
24. Frank JA, Mattay VS, Duyn J, Sobering G, Barrios FA, Zigun J, Sexton R, Kwok P, Woo J, Moonen C et al. (1994) Measurement of relative cerebral blood volume changes with visual stimulation by 'double-dose' gadopentetatedimeglumine-enhanced dynamic magnetic resonance imaging. Invest Radiol 29(Suppl 2):S157-60
25. Gauthier CJ, Madjar C, Tancredi FB, Stefanovic B, Hoge RD (2011) Elimination of visually evoked BOLD responses during carbogen inhalation: implications for calibrated MRI. NeuroImage 54:1001-11
26. Ginsberg MD, Busto R, Harik SI (1985) Regional blood-brain barrier permeability to water and cerebral blood flow during status epilepticus: insensitivity to norepinephrine depletion. Brain Res 337:59-71
27. Girouard H, Iadecola C (2006) Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 100:328-35
28. Griffeth VE, Buxton RB (2011) A theoretical framework for estimating cerebral oxygen metabolism changes using the calibrated-BOLD method: modeling the effects of blood volume distribution, hematocrit, oxygen extraction fraction, and tissue signal properties on the BOLD signal. NeuroImage 58:198-212
29. Gu H, Lu H, Ye FQ, Stein EA, Yang Y (2006) Noninvasive quantification of cerebral blood volume in humans during functional activation. NeuroImage 30: 377-87
30. Hauck EF, Apostel S, Hoffmann JF, Heimann A, Kempski O (2004) Capillary flow and diameter changes during reperfusion after global cerebral ischemia studied by intravital video microscopy. J Cereb Blood Flow Metab 24:383-91
31. Herman P, Sanganahalli BG, Hyder F (2009) Multimodal measurements of blood plasma and red blood cell volumes during functional brain activation. J Cereb Blood Flow Metab 29:19-24
32. Hernandez-Garcia L (2004) Arterial spin labeling for quantitative functional MRI. Conf Proc IEEE Eng Med Biol Soc 7:5230-3
33. Hillman EM, Devor A, Bouchard MB, Dunn AK, Krauss GW, Skoch J, Bacskai BJ, Dale AM, Boas DA (2007) Depth-resolved optical imaging and microscopy of vascular compartment dynamics during somatosensory stimulation. NeuroImage 35:89-104
34. Hoge RD, Atkinson J, Gill B, Crelier GR, Marrett S, Pike GB (1999) Investigation of BOLD signal dependence on cerebral blood flow and oxygen consumption: the deoxyhemoglobin dilution model. Magn Reson Med 42: 849-63
35. Hoge RD, Franceschini MA, Covolan RJ, Huppert T, Mandeville JB, Boas DA (2005) Simultaneous recording of task-induced changes in blood oxygenation, volume, and flow using diffuse optical imaging and arterial spinlabeling MRI. NeuroImage 25:701-7
36. Hua J, Donahue MJ, Zhao JM, Grgac K, Huang AJ, Zhou J, van Zijl PC (2009) Magnetization transfer enhanced vascular-space-occupancy (MT-VASO) functional MRI. Magn Reson Med 61:944-51
37. Hudetz AG (1997) Blood flow in the cerebral capillary network: a review emphasizing observations with intravital microscopy. Microcirculation 4:233-52
38. Hudetz AG, Feher G, Knuese DE, Kampine JP (1994) Erythrocyte flow heterogeneity in the cerebrocortical capillary network. Adv Exp Med Biol 345:633-42
39. Iadecola C (1993) Regulation of the cerebral microcirculation during neural activity: is nitric oxide the missing link? Trends Neurosci 16:206-14
40. Iadecola C, Zhang F (1994) Nitric oxide-dependent and-independent components of cerebrovasodilation elicited by hypercapnia. Am J Physiol 266:R546-52
41. Ito H, Kanno I, Kato C, Sasaki T, Ishii K, Ouchi Y, Iida A, Okazawa H, Hayashida K, Tsuyuguchi N, Kuwabara Y, Senda M (2004) Database of normal human cerebral blood flow, cerebral blood volume, cerebral oxygen extraction fraction and cerebral metabolic rate of oxygen measured by positron emission tomography with 15Olabelled carbon dioxide or water, carbon monoxide and oxygen: a multicentre study in Japan. Eur J Nucl Med Mol Imaging 31:635-43
42. Ito H, Takahashi K, Hatazawa J, Kim SG, Kanno I (2001) Changes in human regional cerebral blood flow and cerebral blood volume during visual stimulation measured by positron emission tomography. J Cereb Blood Flow Metab 21:608-12
43. Karbowski J (2011) Scaling of brain metabolism and blood flow in relation to capillary and neural scaling. PLoS ONE 6:e26709
44. Kennerley AJ, Berwick J, Martindale J, Johnston D, Papadakis N, Mayhew JE (2005) Concurrent fMRI and optical measures for the investigation of the hemodynamic response function. Magn Reson Med 54:354-65
45. Kennerley AJ, Mayhew JE, Redgrave P, Berwick J (2010) Vascular origins of BOLD and CBV fMRI signals: statistical mapping and histological sections compared. Open Neuroimag J 4:1-8
46. Kim T, Hendrich KS, Masamoto K, Kim SG (2007) Arterial versus total blood volume changes during neural activity-induced cerebral blood flow change: implication for BOLD fMRI. J Cereb Blood Flow Metab 27: 1235-1247
47. Kim T, Kim SG (2005) Quantification of cerebral arterial blood volume and cerebral blood flow using MRI with modulation of tissue and vessel (MOTIVE) signals. Magnet Reson Med 54:333-42
48. Kim T, Kim SG (2011) Temporal dynamics and spatial specificity of arterial and venous blood volume changes during visual stimulation: implication for BOLD quantification. J Cereb Blood Flow Metab 31:1211-22
49. Kleinfeld D, Mitra PP, Helmchen F, Denk W (1998) Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc Natl Acad Sci USA 95:15741-6
50. Knapp JM (2005) Hyperosmolar therapy in the treatment of severe head injury in children: mannitol and hypertonic saline. AACN Clin Issues 16:199-211
51. Kong Y, Zheng Y, Johnston D, Martindale J, Jones M, Billings S, Mayhew J (2004) A model of the dynamic relationship between blood flow and volume changes during brain activation. J Cereb Blood Flow Metab 24:1382-92
52. Lee SP, Duong TQ, Yang G, Iadecola C, Kim SG (2001) Relative changes of cerebral arterial and venous blood volumes during increased cerebral blood flow: implications for BOLD fMRI. Magn Reson Med 45:791-800
53. Leite FP, Tsao D, Vanduffel W, Fize D, Sasaki Y, Wald LL, Dale AM, Kwong KK, Orban GA, Rosen BR, Tootell RB, Mandeville JB (2002) Repeated fMRI using iron oxide contrast agent in awake, behaving macaques at 3 Tesla. NeuroImage 16:283-94
54. Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR (2005) IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med 202:473-7
55. Lorthois S, Cassot F, Lauwers F (2011a) Simulation study of brain blood flow regulation by intra-cortical arterioles in an anatomically accurate large human vascular network. Part I: methodology and baseline flow. Neuro-Image 54:1031-42
56. Lorthois S, Cassot F, Lauwers F (2011b) Simulation study of brain blood flow regulation by intra-cortical arterioles in an anatomically accurate large human vascular network. Part II: flow variations induced by global or localized modifications of arteriolar diameters. Neuro-Image 54:2840-53
57. Lu H, Golay X, Pekar JJ, Van Zijl PC (2003) Functional magnetic resonance imaging based on changes in vascular space occupancy. Magn Reson Med 50:263-274
58. Lu H, Law M, Johnson G, Ge Y, van Zijl PC, Helpern JA (2005) Novel approach to the measurement of absolute cerebral blood volume using vascular-space-occupancy magnetic resonance imaging. Magn Reson Med 54: 1403-1411
59. Mandeville JB, Marota JJ, Ayata C, Zaharchuk G, Moskowitz MA, Rosen BR, Weisskoff RM (1999) Evidence of a cerebrovascular postarteriole windkessel with delayed compliance. J Cereb Blood Flow Metab 19:679-89
60. Mark CI, Fisher JA, Pike GB (2011) Improved fMRI calibration: precisely controlled hyperoxic versus hypercapnic stimuli. NeuroImage 54:1102-11
61. Mark CI, Pike GB (2011) Indication of BOLD-specific venous flow-volume changes from precisely controlled hyperoxic vs. hypercapnic calibration. J Cereb Blood Flow Metab 32:709-19
62. Mathur AB, Collinsworth AM, Reichert WM, Kraus WE, Truskey GA (2001) Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy. J Biomech 34:1545-53
63. Mokri B (2001) The Monro-Kellie hypothesis: applications in CSF volume depletion. Neurology 56:1746-8
64. Pawlik G, Rackl A, Bing RJ (1981) Quantitative capillary topography and blood flow in the cerebral cortex of cats: an in vivo microscopic study. Brain Res 208:35-58
65. Pears JA, Francis ST, Butterworth SE, Bowtell RW, Gowland PA (2003) Investigating the BOLD effect during infusion of Gd-DTPA using rapid T2 mapping. Magn Reson Med 49:61-70
66. Peppiatt CM, Howarth C, Mobbs P, Attwell D (2006) Bidirectional control of CNS capillary diameter by pericytes. Nature 443:700-4
67. Piechnik SK, Chiarelli PA, Jezzard P (2008) Modelling vascular reactivity to investigate the basis of the relationship between cerebral blood volume and flow under CO2 manipulation. NeuroImage 39:107-18
68. Piechnik SK, Evans J, Bary LH, Wise RG, Jezzard P (2009) Functional changes in CSF volume estimated using measurement of water T2 relaxation. Magn ResonMed 61:579-86
69. Pike GB (2011) Quantitative functional MRI: concepts, issues and future challenges. NeuroImage; doi:10.1016/j.neuroimage.2011.10.046 (in press)
70. Poser BA, Norris DG (2011) Application of whole-brain CBV-weighted fMRI to a cognitive stimulation paradigm: robust activation detection in a stroop task experiment using 3D GRASE VASO. Hum Brain Mapp 32:974-81
71. Schmidt RF, Thews G. (1997) Physiologie des Menschen. Heidelberg: Springer Starling EH (1896) On the absorption of fluids from the connective tissue spaces. J Physiol 19:312-26
72. Stefanovic B, Hutchinson E, Yakovleva V, Schram V, Russell JT, Belluscio L, Koretsky AP, Silva AC (2008) Functional reactivity of cerebral capillaries. J Cereb Blood Flow Metab 28:961-72
73. Stefanovic B, Pike GB (2005) Venous refocusing for volume estimation: VERVE functional magnetic resonance imaging. Magn Reson Med 53:339-47
74. Tian P, Teng IC, May LD, Kurz R, Lu K, Scadeng M, Hillman EM, De Crespigny AJ, D'Arceuil HE, Mandeville JB, Marota JJ, Rosen BR, Liu TT, Boas DA, Buxton RB, Dale AM, Devor A (2010) Cortical depth-specific microvascular dilation underlies laminar differences in blood oxygenation level-dependent functional MRI signal. Proc Natl Acad Sci USA 107:15246-51
75. Turner R, Thomas D (2006) Cerebral blood volume: measurement change. Proceedings of the ISMRM 14th Scientific Meeting & Exhibition, Washington, Seattle, WA
76. Ursino M, Lodi CA (1997) A simple mathematical model of the interaction between intracranial pressure and cerebral hemodynamics. J Appl Physiol 82:1256-69
77. van Zijl PC, Eleff SM, Ulatowski JA, Oja JM, Ulug AM, Traystman RJ, Kauppinen RA (1998) Quantitative assessment of blood flow, blood volume and blood oxygenation effects in functional magnetic resonance imaging. Nat Med 4:159-67
78. Vazquez AL, Fukuda M, Tasker ML, Masamoto K, Kim SG (2010) Changes in cerebral arterial, tissue and venous oxygenation with evoked neural stimulation: implications for hemoglobin-based functional neuroimaging. J Cereb Blood Flow Metab 30:428-39
79. Vetterlein F, Demmerle B, Bardosi A, Gobel U, Schmidt G (1990) Determination of capillary perfusion pattern in rat brain by timed plasma labeling. Am J Physiol 258:H80-4
80. Villringer A, Them A, Lindauer U, Einhaupl K, Dirnagl U (1994) Capillary perfusion of the rat brain cortex. An in vivo confocal microscopy study. Circ Res 75:55-62
81. Wu WC, Buxton RB, Wong EC (2007) Vascular space occupancy weighted imaging with control of residual blood signal and higher contrast-to-noise ratio. IEEE Trans Med Imaging 26:1319-27
82. Zhao F, Jin T, Wang P, Kim SG (2007) Improved spatial localization of post-stimulus BOLD undershoot relative to positive BOLD. NeuroImage 34: 1084-92
83. Zhao M, Beauregard DA, Loizou L, Davletov B, Brindle KM (2001) Non-invasive detection of apoptosis using magnetic resonance imaging and a targeted contrast agent. Nat Med 7:1241-4
84. Zheng Y, Johnston D, Berwick J, Chen D, Billings S, Mayhew J (2005) A three-compartment model of the hemodynamic response and oxygen delivery to brain. NeuroImage 28:925-39