Direct imaging of macrovascular and microvascular contributions to BOLD fMRI in layers IV-V of the rat whisker-barrel cortex

NeuroImage

Volumn 59, Issue 2, 2012, Pages 1451-1460

  Yu, Xin ^a   Glen, Daniel ^b   Wang, Shumin ^a,c   Dodd, Stephen ^a   Hirano, Yoshiyuki ^a   Saad, Ziad ^b   Reynolds, Richard ^b   Silva, Afonso C ^a   Koretsky, Alan P ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c AUBURN UNIVERSITY   (United States)

Author keywords

BOLD; Rat; Somatosensory cortex; Spatial specificity; Whisker barrel

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BOLD SIGNAL; CONTROLLED STUDY; EVOKED RESPONSE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; MALE; MICROVASCULATURE; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; SIMULATION; SOMATOSENSORY CORTEX; VIBRISSA; VOXEL BASED MORPHOMETRY;

ANIMALS; BLOOD FLOW VELOCITY; EVOKED POTENTIALS, SOMATOSENSORY; MAGNETIC RESONANCE IMAGING; MALE; MICROCIRCULATION; OXYGEN CONSUMPTION; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SOMATOSENSORY CORTEX; VIBRISSAE;

EID: 83055194476     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.08.001     Document Type: Article

References (60)

1. Attwell D., Iadecola C. The neural basis of functional brain imaging signals. Trends Neurosci. 2002, 25:621-625.
2. 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.
3. Bandettini P.A., Wong E.C., Hinks R.S., Tikofsky R.S., Hyde J.S. Time course EPI of human brain function during task activation. Magn. Reson. Med. 1992, 25:390-397.
4. Bolan P.J., Yacoub E., Garwood M., Ugurbil K., Harel N. In vivo micro-MRI of intracortical neurovasculature. NeuroImage 2006, 32:62-69.
5. Buxton R.B. Introduction to Functional Magnetic Resonance Imaging: Principles and Techniques 2002, Cambridge University Press, Cambridge.
6. Chapin J.K., Lin C.S. Mapping the body representation in the SI cortex of anesthetized and awake rats. J. Comp. Neurol. 1984, 229:199-213.
7. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996, 29:162-173.
8. Cox S.B., Woolsey T.A., Rovainen C.M. Localized dynamic changes in cortical blood flow with whisker stimulation corresponds to matched vascular and neuronal architecture of rat barrels. J. Cereb. Blood Flow Metab. 1993, 13:899-913.
9. de Zwart J.A., Silva A.C., van Gelderen P., Kellman P., Fukunaga M., Chu R., Koretsky A.P., Frank J.A., Duyn J.H. Temporal dynamics of the BOLD fMRI impulse response. NeuroImage 2005, 24:667-677.
10. Duong T.Q., Kim D.S., Ugurbil K., Kim S.G. Localized cerebral blood flow response at submillimeter columnar resolution. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:10904-10909.
11. Duong T.Q., Yacoub E., Adriany G., Hu X., Ugurbil K., Kim S.G. Microvascular BOLD contribution at 4 and 7T in the human brain: gradient-echo and spin-echo fMRI with suppression of blood effects. Magn. Reson. Med. 2003, 49:1019-1027.
12. Duyn J.H., Moonen C.T., van Yperen G.H., de Boer R.W., Luyten P.R. Inflow versus deoxyhemoglobin effects in BOLD functional MRI using gradient echoes at 1.5 T. NMR Biomed. 1994, 7:83-88.
13. Engel S.A., Glover G.H., Wandell B.A. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb. Cortex 1997, 7:181-192.
14. Fox P.T., Raichle M.E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:1140-1144.
15. Goense J.B., Logothetis N.K. Laminar specificity in monkey V1 using high-resolution SE-fMRI. Magn. Reson. Imaging 2006, 24:381-392.
16. Goodyear B.G., Menon R.S. Brief visual stimulation allows mapping of ocular dominance in visual cortex using fMRI. Hum. Brain Mapp. 2001, 14:210-217.
17. Harel N., Ugurbil K., Uludag K., Yacoub E. Frontiers of brain mapping using MRI. J. Magn. Reson. Imaging 2006, 23:945-957.
18. Hillman E.M., Devor A., Bouchard M.B., Dunn A.K., Krauss G.W., Skoch J., Bacskai B.J., Dale A.M., Boas D.A. Depth-resolved optical imaging and microscopy of vascular compartment dynamics during somatosensory stimulation. NeuroImage 2007, 35:89-104.
19. Hirano Y., Stefanovic B., Silva A.C. Spatiotemporal evolution of the functional magnetic resonance imaging response to ultrashort stimuli. J. Neurosci. 2011, 31:1440-1447.
20. 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.
21. Jin T., Kim S.G. Cortical layer-dependent dynamic blood oxygenation, cerebral blood flow and cerebral blood volume responses during visual stimulation. NeuroImage 2008, 43:1-9.
22. Keilholz S.D., Silva A.C., Raman M., Merkle H., Koretsky A.P. BOLD and CBV-weighted functional magnetic resonance imaging of the rat somatosensory system. Magn. Reson. Med. 2006, 55:316-324.
23. Kim S.G., Ugurbil K. High-resolution functional magnetic resonance imaging of the animal brain. Methods 2003, 30:28-41.
24. Kim S.G., Hendrich K., Hu X., Merkle H., Ugurbil K. Potential pitfalls of functional MRI using conventional gradient-recalled echo techniques. NMR Biomed. 1994, 7:69-74.
25. Kim D.S., Ronen I., Olman C., Kim S.G., Ugurbil K., Toth L.J. Spatial relationship between neuronal activity and BOLD functional MRI. NeuroImage 2004, 21:876-885.
26. Krings T., Erberich S.G., Roessler F., Reul J., Thron A. MR blood oxygenation level-dependent signal differences in parenchymal and large draining vessels: implications for functional MR imaging. AJNR Am. J. Neuroradiol. 1999, 20:1907-1914.
27. Kwong K.K., Belliveau J.W., Chesler D.A., Goldberg I.E., Weisskoff R.M., Poncelet B.P., Kennedy D.N., Hoppel B.E., Cohen M.S., Turner R., et al. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:5675-5679.
28. Lai S., Hopkins A.L., Haacke E.M., Li D., Wasserman B.A., Buckley P., Friedman L., Meltzer H., Hedera P., Friedland R. Identification of vascular structures as a major source of signal contrast in high resolution 2D and 3D functional activation imaging of the motor cortex at 1.5T: preliminary results. Magn. Reson. Med. 1993, 30:387-392.
29. Lee A.T., Glover G.H., Meyer C.H. Discrimination of large venous vessels in time-course spiral blood-oxygen-level-dependent magnetic-resonance functional neuroimaging. Magn. Reson. Med. 1995, 33:745-754.
30. Lee S.P., Silva A.C., Ugurbil K., Kim S.G. Diffusion-weighted spin-echo fMRI at 9.4T: microvascular/tissue contribution to BOLD signal changes. Magn. Reson. Med. 1999, 42:919-928.
31. Lu H., Golay X., Pekar J.J., Van Zijl P.C. Functional magnetic resonance imaging based on changes in vascular space occupancy. Magn. Reson. Med. 2003, 50:263-274.
32. Lu H., Patel S., Luo F., Li S.J., Hillard C.J., Ward B.D., Hyde J.S. Spatial correlations of laminar BOLD and CBV responses to rat whisker stimulation with neuronal activity localized by Fos expression. Magn. Reson. Med. 2004, 52:1060-1068.
33. Malonek D., Dirnagl U., Lindauer U., Yamada K., Kanno I., Grinvald A. Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:14826-14831.
34. Masamoto K., Obata T., Kanno I. Intracortical microcirculatory change induced by anesthesia in rat somatosensory cortex. Adv. Exp. Med. Biol. 2010, 662:57-61.
35. Menon R.S. Postacquisition suppression of large-vessel BOLD signals in high-resolution fMRI. Magn. Reson. Med. 2002, 47:1-9.
36. Norup Nielsen A., Lauritzen M. Coupling and uncoupling of activity-dependent increases of neuronal activity and blood flow in rat somatosensory cortex. J. Physiol. 2001, 533:773-785.
37. Ogawa S., Lee T.M., Kay A.R., Tank D.W. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:9868-9872.
38. Ogawa S., Tank D.W., Menon R., Ellermann J.M., Kim S.G., Merkle H., Ugurbil K. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:5951-5955.
39. Parkes L.M., Schwarzbach J.V., Bouts A.A., Deckers R.H., Pullens P., Kerskens C.M., Norris D.G. Quantifying the spatial resolution of the gradient echo and spin echo BOLD response at 3 Tesla. Magn. Reson. Med. 2005, 54:1465-1472.
40. Reichenbach J.R., Venkatesan R., Schillinger D.J., Kido D.K., Haacke E.M. Small vessels in the human brain: MR venography with deoxyhemoglobin as an intrinsic contrast agent. Radiology 1997, 204:272-277.
41. Saad Z.S., Ropella K.M., Cox R.W., DeYoe E.A. Analysis and use of FMRI response delays. Hum. Brain Mapp. 2001, 13:74-93.
42. Seehafer J.U., Kalthoff D., Farr T.D., Wiedermann D., Hoehn M. No increase of the blood oxygenation level-dependent functional magnetic resonance imaging signal with higher field strength: implications for brain activation studies. J. Neurosci. 2010, 30:5234-5241.
43. Shmuel A., Yacoub E., Chaimow D., Logothetis N.K., Ugurbil K. Spatio-temporal point-spread function of fMRI signal in human gray matter at 7Tesla. NeuroImage 2007, 35:539-552.
44. Siero J.C., Petridou N., Hoogduin H., Luijten P.R., Ramsey N.F. Cortical depth-dependent temporal dynamics of the BOLD response in the human brain. J. Cereb. Blood Flow Metab. 2011, (Electronic publication ahead of print).
45. Silva A.C., Koretsky A.P. Laminar specificity of functional MRI onset times during somatosensory stimulation in rat. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15182-15187.
46. Silva A.C., Koretsky A.P., Duyn J.H. Functional MRI impulse response for BOLD and CBV contrast in rat somatosensory cortex. Magn. Reson. Med. 2007, 57:1110-1118.
47. Stefanovic B., Hutchinson E., Yakovleva V., Schram V., Russell J.T., Belluscio L., Koretsky A.P., Silva A.C. Functional reactivity of cerebral capillaries. J. Cereb. Blood Flow Metab. 2008, 28:961-972.
48. Thulborn K.R., Waterton J.C., Matthews P.M., Radda G.K. Oxygenation dependence of the transverse relaxation time of water protons in whole blood at high field. Biochim. Biophys. Acta 1982, 714:265-270.
49. Tian P., Teng I.C., May L.D., Kurz R., Lu K., Scadeng M., Hillman E.M., De Crespigny A.J., D'Arceuil H.E., Mandeville J.B., Marota J.J., Rosen B.R., Liu T.T., Boas D.A., Buxton R.B., Dale A.M., Devor A. Cortical depth-specific microvascular dilation underlies laminar differences in blood oxygenation level-dependent functional MRI signal. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:15246-15251.
50. Turner R. How much cortex can a vein drain? Downstream dilution of activation-related cerebral blood oxygenation changes. NeuroImage 2002, 16:1062-1067.
51. Ugurbil K., Toth L., Kim D.S. How accurate is magnetic resonance imaging of brain function?. Trends Neurosci. 2003, 26:108-114.
52. Uludag K., Muller-Bierl B., Ugurbil K. An integrative model for neuronal activity-induced signal changes for gradient and spin echo functional imaging. NeuroImage 2009, 48:150-165.
53. van Zijl P.C., Eleff S.M., Ulatowski J.A., Oja J.M., Ulug A.M., Traystman R.J., Kauppinen R.A. Quantitative assessment of blood flow, blood volume and blood oxygenation effects in functional magnetic resonance imaging. Nat. Med. 1998, 4:159-167.
54. Williams D.S., Detre J.A., Leigh J.S., Koretsky A.P. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:212-216.
55. Yacoub E., Duong T.Q., Van De Moortele P.F., Lindquist M., Adriany G., Kim S.G., Ugurbil K., Hu X. Spin-echo fMRI in humans using high spatial resolutions and high magnetic fields. Magn. Reson. Med. 2003, 49:655-664.
56. Yacoub E., Van De Moortele P.F., Shmuel A., Ugurbil K. Signal and noise characteristics of Hahn SE and GE BOLD fMRI at 7T in humans. NeuroImage 2005, 24:738-750.
57. Yacoub E., Shmuel A., Logothetis N., Ugurbil K. Robust detection of ocular dominance columns in humans using Hahn Spin Echo BOLD functional MRI at 7 Tesla. NeuroImage 2007, 37:1161-1177.
58. Yu X., Wang S., Chen D.Y., Dodd S., Goloshevsky A., Koretsky A.P. 3D mapping of somatotopic reorganization with small animal functional MRI. NeuroImage 2010, 49:1667-1676.
59. Zhao F., Wang P., Kim S.G. Cortical depth-dependent gradient-echo and spin-echo BOLD fMRI at 9.4T. Magn. Reson. Med. 2004, 51:518-524.
60. Zhao F., Wang P., Hendrich K., Kim S.G. Spatial specificity of cerebral blood volume-weighted fMRI responses at columnar resolution. NeuroImage 2005, 27:416-424.