In vivo two-photon excited fluorescence microscopy reveals cardiac- and respiration-dependent pulsatile blood flow in cortical blood vessels in mice

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 7, 2012, Pages

  Santisakultarm, Thom P ^a   Cornelius, Nathan R ^a   Nishimura, Nozomi ^a   Schafer, Andrew I ^b   Silver, Richard T ^b   Doerschuk, Peter C ^a   Olbricht, William L ^a   Schaffer, Chris B ^a  

^a School of Operations Research and Industrial Engineering   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Brain; Hemodynamics; Intravital imaging; Microcirculation; Vessel bifurcation

Indexed keywords

ANIMAL EXPERIMENT; ARTERIOLE; ARTICLE; BLOOD FLOW; BLOOD FLOW VELOCITY; BRAIN BLOOD VESSEL; BRAIN CAPILLARY; BRAIN CORTEX; CAPILLARY FLOW; CAPILLARY TUBE; ELECTROCARDIOGRAM; ERYTHROCYTE; FEMALE; FLUORESCENCE MICROSCOPY; HEART BEAT; HEART HEMODYNAMICS; HEMATOCRIT; LUNG HEMODYNAMICS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PULSATILE FLOW; VENULE;

ALGORITHMS; ANESTHESIA; ANIMALS; ARTERIOLES; BLOOD FLOW VELOCITY; CAPILLARIES; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; ELECTROCARDIOGRAPHY; FEMALE; HEART; HEMATOCRIT; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; MYOCARDIAL CONTRACTION; PULSATILE FLOW; RESPIRATORY MECHANICS; VENULES;

EID: 84859464637     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00417.2011     Document Type: Article

References (54)

1. Audet D, Olbricht W. The motion of model cells at capillary bifurcations. Microvasc Res 33: 377-396, 1987.
2. Blinder P, Shih AY, Rafie C, Kleinfeld D. Topological basis for the robust distribution of blood to rodent neocortex. Proc Natl Acad Sci USA 107: 12670-12675, 2010.
3. Boas DA, Dunn AK. Laser speckle contrast imaging in biomedical optics. J Biomed Opt 15: 011109, 2010.
4. Bulte DP, Kelly M, Germuska M, Xie J, Chappell MA, Okell TW, Bright MG, Jezzard P. Quantitative measurement of cerebral physiology using respiratory-calibrated MRI. Neuroimage 60: 582-591, 2011.
5. Buxton RB, Frank LR. A model for the coupling between cerebral blood flow and oxygen metabolism during neural stimulation. J Cereb Blood Flow Metab 17: 64-72, 1997.
6. Constantinescu AA, Vink H, Spaan JA. Elevated capillary tube hematocrit reflects degradation of endothelial cell glycocalyx by oxidized LDL. Am J Physiol Heart Circ Physiol 280: H1051-H1057, 2001.
7. Cruickshank K, Riste L, Anderson SG, Wright JS, Dunn G, Gosling RG. Aortic pulse-wave velocity and its relationship to mortality in diabetes and glucose intolerance: an integrated index of vascular function? Circulation 106: 2085-2090, 2002.
8. Cuzick J. A Wilcoxon-type test for trend. Stat Med 4: 87-90, 1985.
9. Denk W, Strickler J, Webb W. Two-photon laser scanning fluorescence microscopy. Science 248: 73-76, 1990.
10. Drew P, Blinder P, Cauwenberghs G, Shih A, Kleinfeld D. Rapid determination of particle velocity from space-time images using the Radon transform. J Comput Neurosci 29: 5-11, 2010.
11. Gross JF, Intaglietta M, Zweifach BW. Network model of pulsatile hemodynamics in the microcirculation of the rabbit omentum. Am J Physiol 226: 1117-1123, 1974.
12. Guntheroth WG, Morgan BC, Mullins GL. Effect of respiration on venous return and stroke volume in cardiac tamponade. Mechanism of pulsus parodoxus. Circ Res 20: 381-390, 1967.
13. Guyton AC, Hall JE. Textbook of Medical Physiology. New York: Saunders, 2005.
14. Hahn C, Schwartz MA. The role of cellular adaptation to mechanical forces in atherosclerosis. Arterioscler Thromb Vasc Biol 28: 2101-2107, 2008.
15. Hawkey CM, Bennett PM, Gascoyne SC, Hart MG, Kirkwood JK. Erythrocyte size, number and haemoglobin content in vertebrates. Br J Haematol 77: 392-397, 1991.
16. Heinicke K, Baum O, Ogunshola OO, Vogel J, Stallmach T, Wolfer DP, Keller S, Weber K, Wagner PD, Gassmann M, Djonov V. Excessive erythrocytosis in adult mice overexpressing erythropoietin leads to hepatic, renal, neuronal, and muscular degeneration. Am J Physiol Regul Integr Comp Physiol 291: R947-R956, 2006.
17. Heiss W, Forsting M, Diener H. Imaging in cerebrovascular disease. Curr Opin Neurol 14: 67-75, 2001.
18. Intaglietta M, Richardson DR, Tompkins WR. Blood pressure, flow, and elastic properties in microvessels of cat omentum. Am J Physiol 221: 922-928, 1971.
19. Kleinfeld D, Delaney KR. Distributed representation of vibrissa movement in the upper layers of somatosensory cortex revealed with voltagesensitive dyes. J Comp Neurol 375: 89-108, 1996.
20. Kleinfeld D, Mitra P, Helmchen F, Denk W. Fluctuations and stimulusinduced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc Natl Acad Sci USA 95: 15741-15746, 1998.
21. Kobat D, Durst ME, Nishimura N, Wong AW, Schaffer CB, Xu C. Deep tissue multiphoton microscopy using longer wavelength excitation. Opt Express 17: 13354-13364, 2009.
22. 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.
23. Mills C, Gabe I, Gault J, Mason D, Ross J, Braunwald E, Shillingford J. Pressure-flow relationships and vascular impedance in man. Cardiovasc Res 4: 405-417, 1970.
24. Mitchell GF, Van Buchem MA, Sigurdsson S, Gotal JD, Jonsdottir MK, Kjartansson O, Garcia M, Aspelund T, Harris TB, Gudnason V, Launer LJ. Arterial stiffness, pressure and flow pulsatility and brain structure and function: the age, gene/environment susceptibility-Reykjavik study. Brain 134: 3398-3407, 2011.
25. Morgan B, Dillard D, Guntheroth W. Effect of cardiac and respiratory cycle on pulmonary vein flow, pressure, and diameter. J Appl Physiol 21: 1276-1280, 1966.
26. Motomiya M, Karino T. Flow patterns in the human carotid artery bifurcation. Stroke 15: 50-56, 1984.
27. Neu B, Wenby R, Meiselman HJ. Effects of dextran molecular weight on red blood cell aggregation. Biophys J 95: 3059-3065, 2008.
28. Nguyen J, Nishimura N, Fetcho RN, Iadecola C, Schaffer CB. Occlusion of cortical ascending venules causes blood flow decreases, reversals in flow direction, and vessel dilation in upstream capillaries. J Cereb Blood Flow Metab 31: 2243-2254, 2011.
29. Nguyen Q, Tsai P, Kleinfeld D. MPScope: a versatile software suite for multiphoton microscopy. J Neurosci Methods 156: 351-359, 2006.
30. Nishimura N, Rosidi NL, Iadecola C, Schaffer CB. Limitations of collateral flow after occlusion of a single cortical penetrating arteriole. J Cereb Blood Flow Metab 30: 1914-1927, 2010.
31. Nishimura N, Schaffer C, Friedman B, Tsai P, Lyden P, Kleinfeld D. Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke. Nat Methods 3: 99-108, 2006.
32. Nyman L, Wells K, Head W, McCaughey M, Ford E, Brissova M, Piston D, Powers A. Real-time, multidimensional in vivo imaging used to investigate blood flow in mouse pancreatic islets. J Clin Invest 118: 3790-3797, 2008.
33. O'Brien J. Vascular cognitive impairment. Am J Geriatr Psychiatry 14: 724-733, 2006.
34. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9: 689-701, 2010.
35. Popel AS, Johnson PC. Microcirculation and hemorheology. Annu Rev Fluid Mech 37: 43-69, 2005.
36. Pries A, Ley K, Claassen M, Gaehtgens P. Red cell distribution at microvascular bifurcations. Microvasc Res 38: 81-101, 1989.
37. Pries AR, Neuhaus D, Gaehtgens P. Blood viscosity in tube flow: dependence on diameter and hematocrit. Am J Physiol Heart Circ Physiol 263: H1770-H1778, 1992.
38. Rosenblum W. Erythrocyte velocity and a velocity pulse in minute blood vessels on the surface of the mouse brain. Circ Res 24: 887-892, 1969.
39. Salotto AG, Muscarella LF, Melbin J, Li JK, Noordergraaf A. Pressure pulse transmission into vascular beds. Microvasc Res 32: 152-163, 1986.
40. Schaffer C, Friedman B, Nishimura N, Schroeder L, Tsai P, Ebner F, Lyden P, Kleinfeld D. Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol 4: e22, 2006.
41. Schmid-Schonbein G. Biomechanics of microcirculatory blood perfusion. Annu Rev Biomed Eng 1: 73-102, 1999.
42. Schmid-Schönbein GW, Lee SY, Sutton D. Dynamic viscous flow in distensible vessels of skeletal muscle microcirculation: application to pressure and flow transients. Biorheology 26: 215-227, 1989.
43. Seed W, Wood N. Velocity patterns in the aorta. Cardiovasc Res 5: 319-330, 1971.
44. Skalak TC, Schmid-Schonbein GW. Viscoelastic properties of microvessels in rat spinotrapezius muscle. J Biomech Eng 108: 193-200, 1986.
45. Smaje LH, Fraser PA, Clough G. The distensibility of single capillaries and venules in the cat mesentery. Microvasc Res 20: 358-370, 1980.
46. Srinivasan VJ, Atochin DN, Radhakrishnan H, Jiang JY, Ruvinskaya S, Wu W, Barry S, Cable AE, Ayata C, Huang PL, Boas DA. Optical coherence tomography for the quantitative study of cerebrovascular physiology. J Cereb Blood Flow Metab 31: 1339-1345, 2011.
47. Tangelder G, Slaaf D, Muijtjens A, Arts T, Oude Egbrink M, Reneman R. Velocity profiles of blood platelets and red blood cells flowing in arterioles of the rabbit mesentery. Circ Res 59: 505-514, 1986.
48. Ts'o DY, Frostig RD, Lieke EE, Grinvald A. Functional organization of primate visual cortex revealed by high resolution optical imaging. Science 249: 417-420, 1990.
49. Tsai P, Kaufhold J, Blinder P, Friedman B, Drew P, Karten H, Lyden P, Kleinfeld D. 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.
50. Wexler L, Bergel D, Gabe I, Makin G, Mills C. Velocity of blood flow in normal human venae cavae. Circ Res 23: 349-359, 1968.
51. Wilkens H, Regelson W, Hoffmeister FS. The physiolgic importance of pulsatile blood flow. N Engl J Med 267: 443-446, 1962.
52. Windberger U, Bartholovitsch A, Plasenzotti R, Korak KJ, Heinze G. Whole blood viscosity, plasma viscosity and erythrocyte aggregation in nine mammalian species: reference values and comparison of data. Exp Physiol 88: 431-440, 2003.
53. Zipfel W, Williams R, Webb W. Nonlinear magic: multiphoton microscopy in the biosciences. Nat Biotechnol 21: 1369-1377, 2003.
54. Zweifach BW, Lipowsky HH. Quantitative studies of microcirculatory structure and function. III. Microvascular hemodynamics of cat mesentery and rabbit omentum. Circ Res 41: 380-390, 1977.