Quantification of blood flow and volume in arterioles and venules of the rat cerebral cortex using functional micro-ultrasound

NeuroImage

Volumn 63, Issue 3, 2012, Pages 1030-1037

  van Raaij, Martijn E ^a   Lindvere, Liis ^a   Dorr, Adrienne ^a   He, Jianfei ^a   Sahota, Bhupinder ^a   Foster, F Stuart ^a   Stefanovic, Bojana ^a  

^a Canada   (Canada)

Author keywords

Cerebral blood flow (CBF); Cerebral blood volume (CBV); Cerebral hemodynamics; Functional micro ultrasound imaging (fMUS); Functional neuroimaging; Rat

Indexed keywords

CONTRAST MEDIUM; UNCLASSIFIED DRUG; VEVO MICROMARKER;

ANIMAL EXPERIMENT; ARTERIOLE; ARTICLE; BLOOD FLOW VELOCITY; BRAIN BLOOD FLOW; BRAIN BLOOD VESSEL; BRAIN BLOOD VOLUME; BRAIN CORTEX; BRAIN MAPPING; COLOR ULTRASOUND FLOWMETRY; CONTRAST ENHANCEMENT; FUNCTIONAL MICROULTRASOUND; FUNCTIONAL NEUROIMAGING; GRAY MATTER; MALE; MICROBUBBLE; NONHUMAN; PRIORITY JOURNAL; RAT; ULTRASOUND; VENULE;

ANIMALS; ARTERIOLES; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; MALE; RATS; RATS, SPRAGUE-DAWLEY; ULTRASONOGRAPHY; VENULES;

EID: 84866047915     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.07.054     Document Type: Article

References (45)

1. Adam J.-F., Elleaume H., Le Duc G., Corde S., Charvet A.-M., Tropres I., Le Bas J.-F., Esteve F. Absolute cerebral blood volume and blood flow measurements based on synchrotron radiation quantitative computed tomography. J. Cereb. Blood Flow Metab. 2003, 23:499-512.
2. Anwar M., Kissen I., Weiss H.R. Effect of chemodenervation on the cerebral vascular and microvascular response to hypoxia. Circ. Res. 1990, 67:1365-1373.
3. Attwell D., Buchan A.M., Charpak S., Lauritzen M., Macvicar B.A., Newman E.A. Glial and neuronal control of brain blood flow. Nature 2010, 468:232-243.
4. Becher H., Burns P.N. Handbook of Contrast Echocardiography 2000, Springer, Berlin.
5. Brown W.R., Thore C.R. Review: cerebral microvascular pathology in ageing and neurodegeneration. Neuropathol. Appl. Neurobiol. 2011, 37:56-74.
6. Calamante F., Thomas D.L., Pell G.S., Wiersma J., Turner R. Measuring cerebral blood flow using magnetic resonance imaging techniques. J. Cereb. Blood Flow Metab. 1999, 19:701-735.
7. Chen H., Zhang J.H. Cerebral amyloid angiopathy-related microhemorrhages in Alzheimer's disease: a review of investigative animal models. Acta Neurochir. Suppl. 2011, 111:15-17.
8. Coles J.P. Imaging of cerebral blood flow and metabolism. Curr. Opin. Anaesthesiol. 2006, 19:473-480.
9. D'Esposito M., Deouell L.Y., Gazzaley A. Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat. Rev. Neurosci. 2003, 4:863-872.
10. Devor A., Sakadzic S., Srinivasan V.J., Yaseen M.A., Nizar K., Saisan P.A., Tian P., Dale A.M., Vinogradov S.A., Franceschini M.A., Boas D.A. Frontiers in optical imaging of cerebral blood flow and metabolism. J. Cereb. Blood Flow Metab. 2012, 32(7):1259-1276. (July).
11. Driscoll J.D., Shih A.Y., Drew P.J., Valmianski I., Kleinfeld D. Quantitative two-photon imaging of blood flow in cortex. Optical Imaging in Neuroscience 2009, Cold Spring Harbor Laboratory Press. F. Helmchen, A. Konnerth (Eds.).
12. Duong T.Q., Kim S.G. In vivo MR measurements of regional arterial and venous blood volume fractions in intact rat brain. Magn. Reson. Med. 2000, 43:393-402.
13. Ferrara K., Pollard R., Borden M. Ultrasound microbubble contrast agents: fundamentals and application to gene and drug delivery. Annu. Rev. Biomed. Eng. 2007, 9:415-447.
14. Foster F.S., Zhang M.Y., Zhou Y.Q., Liu G., Mehi J., Cherin E., Harasiewicz K.A., Starkoski B.G., Zan L., Knapik D.A., Adamson S.L. A new ultrasound instrument for in vivo microimaging of mice. Ultrasound Med. Biol. 2002, 28:1165-1172.
15. Goertz D.E., Needles A., Burns P.N., Foster F.S. High-frequency, nonlinear flow imaging of microbubble contrast agents. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2005, 52:495-502.
16. Grubb R.L., Raichle M.E., Eichling J.O., Ter-Pogossian M.M. The effects of changes in PaCO2 on cerebral blood volume, blood flow, and vascular mean transit time. Stroke 1974, 5:630-639.
17. Herman P., Sanganahalli B.G., Hyder F. Multimodal measurements of blood plasma and red blood cell volumes during functional brain activation. J. Cereb. Blood Flow Metab. 2009, 29:19-24.
18. Hudson J.M., Karshafian R., Burns P.N. Quantification of flow using ultrasound and microbubbles: a disruption replenishment model based on physical principles. Ultrasound Med. Biol. 2009, 35:2007-2020.
19. Hutchinson E.B., Stefanovic B., Koretsky A.P., Silva A.C. Spatial flow-volume dissociation of the cerebral microcirculatory response to mild hypercapnia. Neuroimage 2006, 32:520-530.
20. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 2004, 5:347-360.
21. Iadecola C., Nedergaard M. Glial regulation of the cerebral microvasculature. Nat. Neurosci. 2007, 10:1369-1376.
22. Jensen J.A. Estimation of Blood Velocities Using Ultrasound: A Signal Processing Approach 1996, Cambridge University Press, Cambridge; New York, USA.
23. Kennerley A.J., Berwick J., Martindale J., Johnston D., Papadakis N., Mayhew J.E. Concurrent fMRI and optical measures for the investigation of the hemodynamic response function. Magn. Reson. Med. 2005, 54:354-365.
24. Kim T., Kim S.G. Quantification of cerebral arterial blood volume and cerebral blood flow using MRI with modulation of tissue and vessel (MOTIVE) signals. Magn. Reson. Med. 2005, 54:333-342.
25. Lampaskis M., Averkiou M. Investigation of the relationship of nonlinear backscattered ultrasound intensity with microbubble concentration at low MI. Ultrasound Med. Biol. 2010, 36:306-312.
26. Lindvere L., Dorr A., Stefanovic B. Two-photon fluorescence microscopy of cerebral hemodynamics. Cold Spring Harb. Protoc. 2010, 10.1101/pdb.prot5494.
27. Lu J., Dai G., Egi Y., Huang S., Kwon S.J., Lo E.H., Kim Y.R. Characterization of cerebrovascular responses to hyperoxia and hypercapnia using MRI in rat. Neuroimage 2009, 45:1126-1134.
28. Mace E., Montaldo G., Cohen I., Baulac M., Fink M., Tanter M. Functional ultrasound imaging of the brain. Nat. Methods 2011, 8:662-664.
29. Maekawa T., Tommasino C., Shapiro H.M., Keifer-Goodman J., Kohlenberger R.W. Local cerebral blood flow and glucose utilization during isoflurane anesthesia in the rat. Anesthesiology 1986, 65:144-151.
30. Mellander S., Johansson B. Control of resistance, exchange, and capacitance functions in the peripheral circulation. Pharmacol. Rev. 1968, 20:117-196.
31. Mishra A.M., Ellens D.J., Schridde U., Motelow J.E., Purcaro M.J., DeSalvo M.N., Enev M., Sanganahalli B.G., Hyder F., Blumenfeld H. Where fMRI and electrophysiology agree to disagree: corticothalamic and striatal activity patterns in the WAG/Rij rat. J. Neurosci. 2011, 31:15053-15064.
32. Motulsky H.J., Christopoulos A. Fitting models to biological data using linear and nonlinear regression. A Practical Guide to Curvefitting 2003, GraphPad Software Inc., San Diego CA, www.graphpad.com.
33. Mulvagh S.L., Rakowski H., Vannan M.A., Abdelmoneim S.S., Becher H., Bierig S.M., Burns P.N., Castello R., Coon P.D., Hagen M.E., Jollis J.G., Kimball T.R., Kitzman D.W., Kronzon I., Labovitz A.J., Lang R.M., Mathew J., Moir W.S., Nagueh S.F., Pearlman A.S., Perez J.E., Porter T.R., Rosenbloom J., Strachan G.M., Thanigaraj S., Wei K., Woo A., Yu E.H.C., Zoghbi W.A. American society of echocardiography consensus statement on the clinical applications of ultrasonic contrast agents in echocardiography. J. Am. Soc. Echocardiogr. 2008, 21:1179-1201.
34. Needles A., Arditi M., Rognin N.G., Mehi J., Coulthard T., Bilan-Tracey C., Gaud E., Frinking P., Hirson D., Foster F.S. Nonlinear contrast imaging with an array-based micro-ultrasound system. Ultrasound Med. Biol. 2010, 36:2097-2106.
35. Piechnik S.K., Chiarelli P.A., Jezzard P. Modelling vascular reactivity to investigate the basis of the relationship between cerebral blood volume and flow under CO2 manipulation. Neuroimage 2008, 39:107-118.
36. Potdevin T.C., Fowlkes J.B., Moskalik A.P., Carson P.L. Refill model of rabbit kidney vasculature. Ultrasound Med. Biol. 2006, 32:1331-1338.
37. Powers J., Averkiou M., Bruce M. Principles of cerebral ultrasound contrast imaging. Cerebrovasc. Dis. 2009, 27:14-24.
38. Sanganahalli B.G., Herman P., Blumenfeld H., Hyder F. Oxidative neuroenergetics in event-related paradigms. J. Neurosci. 2009, 29:1707-1718.
39. Shih A.Y., Driscoll J.D., Drew P.J., Nishimura N., Schaffer C.B., Kleinfeld D. Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain. J. Cereb. Blood Flow Metab. 2012, 32(7):1277-1309. (July).
40. Sloan H.L., Austin V.C., Blamire A.M., Schnupp J.W., Lowe A.S., Allers K.A., Matthews P.M., Sibson N.R. Regional differences in neurovascular coupling in rat brain as determined by fMRI and electrophysiology. Neuroimage 2010, 53:399-411.
41. Sprague M.R., Cherin E., Goertz D.E., Foster F.S. Nonlinear emission from individual bound microbubbles at high frequencies. Ultrasound Med. Biol. 2010, 36:313-324.
42. Tang M.X., Mulvana H., Gauthier T., Lim A.K.P., Cosgrove D.O., Eckersley R.J., Stride E. Quantitative contrast-enhanced ultrasound imaging: a review of sources of variability. Interface Focus 2011, 1:520-539.
43. Unekawa M., Tomita M., Tomita Y., Toriumi H., Miyaki K., Suzuki N. RBC velocities in single capillaries of mouse and rat brains are the same, despite 10-fold difference in body size. Brain Res. 2010, 1320:69-73.
44. van Raaij M.E., Lindvere L., Dorr A., He J., Sahota B., Foster F.S., Stefanovic B. Functional micro-ultrasound imaging of rodent cerebral hemodynamics. Neuroimage 2011, 58:100-108.
45. Wei K., Jayaweera A.R., Firoozan S., Linka A., Skyba D.M., Kaul S. Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion. Circulation 1998, 97:473-483.