Large arteriolar component of oxygen delivery implies a safe margin of oxygen supply to cerebral tissue

Nature Communications

Volumn 5, Issue , 2014, Pages

  Sakadžić, Sava ^a   Mandeville, Emiri T ^a   Gagnon, Louis ^a,b   Musacchia, Joseph J ^a   Yaseen, Mohammad A ^a   Yucel, Meryem A ^a   Lefebvre, Joel ^b   Lesage, Frédéric ^b   Dale, Anders M ^c   Eikermann Haerter, Katharina ^a   Ayata, Cenk ^a   Srinivasan, Vivek J ^a,d   Lo, Eng H ^a   Devor, Anna ^a,c   Boas, David A ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b ÉCOLE POLYTECHNIQUE DE MONTRÉAL   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d University of California   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN;

BLOOD; CAPILLARITY; DISEASE INCIDENCE; NUMERICAL MODEL; OXYGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; BLOOD FLOW; BOLD SIGNAL; BRAIN CORTEX; BRAIN TISSUE; CELL ACTIVITY; CONTROLLED STUDY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; MALE; MOUSE; NONHUMAN; OXYGEN SUPPLY; TISSUE OXYGENATION; ANIMAL; BRAIN; BRAIN CIRCULATION; C57BL MOUSE; CAPILLARY; CHEMISTRY; MICROSCOPY; MULTIMODAL IMAGING; NERVE CELL; NUCLEAR MAGNETIC RESONANCE IMAGING; OXYGEN CONSUMPTION; PHYSIOLOGY; THEORETICAL MODEL; VASCULARIZATION;

ANIMALS; ARTERIOLES; BRAIN; CAPILLARIES; CEREBROVASCULAR CIRCULATION; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY; MODELS, THEORETICAL; MULTIMODAL IMAGING; NEURONS; OXYGEN; OXYGEN CONSUMPTION;

EID: 84923265935     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6734     Document Type: Article

References (43)

1. Attwell, D. & Laughlin, S. B. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 21, 1133-1145 (2001).
2. 2 in the vicinity of the pial vessels. Pflugers Arch. 383, 29-34 (1979).
3. Vovenko, E. Distribution of oxygen tension on the surface of arterioles, capillaries and venules of brain cortex and in tissue in normoxia: an experimental study on rats. Pflugers Arch. 437, 617-623 (1999).
4. Vazquez, A. L., Masamoto, K., Fukuda, M. & Kim, S.-G. Cerebral oxygen delivery and consumption during evoked neural activity. Front. Neuroenergetics 2, 11 (2010).
5. Duling, B. R. & Berne, R. M. Longitudinal gradients in periarteriolar oxygen tension a possible mechanism for the participation of oxygen in local regulation of blood flow. Circ. Res. 27, 669-678 (1970).
6. Krogh, A. The supply of oxygen to the tissues and the regulation of the capillary circulation. J. Physiol. 52, 457-474 (1919).
7. Tsai, A. G., Johnson, P. C. & Intaglietta, M. Oxygen gradients in the microcirculation. Physiol. Rev. 83, 933-963 (2003).
8. Secomb, T. W., Alberding, J. P., Hsu, R., Dewhirst, M. W. & Pries, A. R. Angiogenesis: an adaptive dynamic biological patterning problem. PLoS Comput. Biol. 9, e1002983 (2013).
9. Pittman, R. Oxygen transport and exchange in the microcirculation. Microcirculation 12, 59-70 (2005).
10. Popel, A. Theory of oxygen-transport to tissue. Crit. Rev. Biomed. Eng. 17, 257-321 (1989).
11. Goldman, D. Theoretical models of microvascular oxygen transport to tissue. Microcirculation 15, 795-811 (2008).
12. Zlokovic, B. V. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat. Rev. Neurosci. 12, 723-738 (2011).
13. Buxton, R. B. Interpreting oxygenation-based neuroimaging signals: the importance and the challenge of understanding brain oxygen metabolism. Front. Neuroenergetics 2, 8 (2010).
14. Bolar, D. S., Rosen, B. R., Sorensen, A. G. & Adalsteinsson, E. QUantitative Imaging of eXtraction of Oxygen and TIssue consumption (QUIXOTIC) using venular-targeted velocity-selective spin labeling. Magn. Reson. Med. 66, 1550-1562 (2011).
15. Ma, D. et al. Magnetic resonance fingerprinting. Nature 495, 187-192 (2013).
16. Sakadzic, S. et al. Two-photon high-resolution measurement of partial pressure of oxygen in cerebral vasculature and tissue. Nat. Methods 7, 755-U125 (2010).
17. Finikova, O. S. et al. Oxygen microscopy by two-photon-excited phosphorescence. Chemphyschem 9, 1673-1679 (2008).
18. 2 is required to maintain baseline tissue oxygenation at locations distal to blood vessels. J. Neurosci. 31, 13676-13681 (2011).
19. Lecoq, J. et al. Simultaneous two-photon imaging of oxygen and blood flow in deep cerebral vessels. Nat. Med. 17, 893-U262 (2011).
20. Srinivasan, V. J. et al. Quantitative cerebral blood flow with optical coherence tomography. Opt. Express 18, 2477-2494 (2010).
21. Kasischke, K. A. et al. Two-photon NADH imaging exposes boundaries of oxygen diffusion in cortical vascular supply regions. J. Cereb. Blood Flow Metab. 31, 68-81 (2011).
22. Blinder, P. et al. The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow. Nat. Neurosci. 16, 889-897 (2013).
23. Masamoto, K., Kurachi, T., Takizawa, N., Kobayashi, H. & Tanishita, K. Successive depth variations in microvascular distribution of rat somatosensory cortex. Brain Res. 995, 66-75 (2004).
24. Hall, J. E. Guyton and Hall Textbook of Medical Physiology (Saunders, 2010).
25. 2 transport in skeletal muscle: diffusive exchange between arterioles and capillaries. Am. J. Physiol. 267, H1214-H1221 (1994).
26. Ellsworth, M. & Pittman, R. Arterioles supply oxygen to capillaries by diffusion as well as by convection. Am. J. Physiol. 258, H1240-H1243 (1990).
27. Munn, L. L., Kunert, C. & Tyrrell, J. A. in Mathematical Methods and Models in Biomedicine (eds Ledzewicz, U., Schättler, H., Friedman, A. & Kashdan, E.) 117-148 (Springer, 2012).
28. Pries, A. R. & Secomb, T. W. in Comprehensive Physiology 3-36 (John Wiley & Sons Inc., 2011).
29. Paulson, O. B., Hasselbalch, S. G., Rostrup, E., Knudsen, G. M. & Pelligrino, D. Cerebral blood flow response to functional activation. J. Cereb. Blood Flow Metab. 30, 2-14 (2010).
30. Fox, P. & Raichle, M. Focal physiological uncoupling of cerebral blood-flow and oxidative-metabolism during somatosensory stimulation in human-subjects. Proc. Natl Acad. Sci. USA 83, 1140-1144 (1986).
31. Hall, C. N. et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature 508, 55-60 (2014).
32. Jespersen, S. N. & Ostergaard, L. The roles of cerebral blood flow, capillary transit time heterogeneity, and oxygen tension in brain oxygenation and metabolism. J. Cereb. Blood Flow Metab. 32, 264-277 (2012).
33. Chance, B. Cellular oxygen requirements. Fed. Proc. 16, 671-680 (1957).
34. Wilson, D. F., Harrison, D. K. & Vinogradov, S. A. Oxygen, pH, and mitochondrial oxidative phosphorylation. J. Appl. Physiol. 113, 1838-1845 (2012).
35. Fang, Q. et al. Oxygen advection and diffusion in a three- dimensional vascular anatomical network. Opt. Express 16, 17530-17541 (2008).
36. Tsai, P. S. et al. Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of nuclei and vessels. J. Neurosci. 29, 14553-14570 (2009).
37. Floyd, R. Algorithm-97-shortest path. Commun. Acm 5, 345-345 (1962).
38. Gagnon, L. et al. Underpinning the microvascular origin of BOLD-fMRI with two-photon microscopy, in Biomedical Optics 2014, BT4A.1 (Optical Society of America, 2014).
39. Lorthois, S., Cassot, F. & Lauwers, F. 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. Neuroimage 54, 1031-1042 (2011).
40. Wehrl, H. F. et al. Simultaneous assessment of Perfusion with [15O] water PET and arterial spin labeling MR using a hybrid PET/MR device. Proc. Intl Soc. Mag. Reson. Med. 18, 715 (2010).
41. Zheng, B., Lee, P. T. H. & Golay, X. High-sensitivity cerebral perfusion mapping in mice by kbGRASE-FAIR at 9.4 T. NMR Biomed. 23, 1061-1070 (2010).
42. 2 transients in capillaries. Nat. Med. 19, 241-246 (2013).
43. Uchida, K., Reilly, M. P. & Asakura, T. Molecular stability and function of mouse hemoglobins. Zoolog. Sci. 15, 703-706 (1998).