Compartment-resolved imaging of activity-dependent dynamics of cortical blood volume and oximetry

Journal of Neuroscience

Volumn 25, Issue 9, 2005, Pages 2233-2244

  Vanzetta, Ivo ^a,b   Hildesheim, Rina ^a   Grinvald, Amiram ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b CNRS   (France)

Author keywords

Arterioles; CBV; fMRI; Microvasculature; Neurovascular coupling; Optical imaging

Indexed keywords

HEMOGLOBIN;

ARTERIOLE; ARTERY; ARTICLE; BLOOD VESSEL REACTIVITY; BRAIN BLOOD VOLUME; BRAIN CORTEX; BRAIN CORTEX AREA 18; CAPILLARY; CAT; CELL DENSITY; ELECTRIC ACTIVITY; EVOKED SOMATOSENSORY RESPONSE; FLUORESCENCE; HEMATOCRIT; HEMODYNAMICS; HIGH RESOLUTION OPTICAL IMAGING; ILLUMINATION; IMAGING SYSTEM; LIGHT SCATTERING; MICROVASCULARIZATION; NONHUMAN; OXIMETRY; OXYGEN TENSION; PARENCHYMA; PRIORITY JOURNAL; VEIN;

ANIMALS; BRAIN MAPPING; CARBOCYANINES; CATS; CEREBROVASCULAR CIRCULATION; DIAGNOSTIC IMAGING; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; NONLINEAR DYNAMICS; OXIMETRY; OXYGEN; PHOTIC STIMULATION; REPRODUCIBILITY OF RESULTS; TIME FACTORS; VISUAL CORTEX;

EID: 14644398531     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3032-04.2005     Document Type: Article

References (76)

1. Ances BM, Buerk DG, Greenberg JH, Detre JA (2001) Temporal dynamics of the partial pressure of brain tissue oxygen during functional forepaw stimulation in rats. Neurosci Lett 306:106-110.
2. Bonhoeffer T, Grinvald A (1991) Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature 353:429-431.
3. Bonhoeffer T, Grinvald A (1993) The layout of iso-orientation domains in area 18 of cat visual cortex: optical imaging reveals a pinwheel-like organization. J Neurosci 13:4157-4180.
4. Bosking WH, Zhang Y, Schofield B, Fitzpatrick D (1997) Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. J Neurosci 17:2112-2127.
5. Buxton RB, Frank LR (1997) A model for the coupling between cerebral blood flow and oxygen metabolism during neural stimulation. J Cereb Blood Flow Metab 17:64-72.
6. Buxton RB, Wong EC, Frank LR (1998) Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magn Reson Med 39:855-864.
7. Buxton RB, Uludag K, Dubowitz DJ, Liu TT (2004) Modeling the hemodynamic response to brain activation. NeuroImage 23:S220-233.
8. Caesar K, Gold L, Lauritzen M (2003a) Context sensitivity of activity-dependent increases in cerebral blood flow. Proc Natl Acad Sci USA 100:4239-4244.
9. Caesar K, Thomsen K, Lauritzen M (2003b) Dissociation of spikes, synaptic activity, and activity-dependent increments in rat cerebellar blood flow by tonic synaptic inhibition. Proc Natl Acad Sci USA 100:16000-16005.
10. Chaigneau E, Oheim M, Audinat E, Charpak S (2003) Two-photon imaging of capillary blood flow in olfactory bulb glomeruli. Proc Natl Acad Sci USA 100:13081-13086.
11. Chatton JY, Pellerin L, Magistretti PJ (2003) GABA uptake into astrocytes is not associated with significant metabolic cost: implications for brain imaging of inhibitory transmission. Proc Natl Acad Sci USA 100:12456-12461.
12. Cheng K, Waggoner RA, Tanaka K (2001) Human ocular dominance columns as revealed by high-field functional magnetic resonance imaging. Neuron 32:359-374.
13. Collins DM, McCullough WT, Ellsworth ML (1998) Conducted vascular responses: communication across the capillary bed. Microvasc Res 56:43-53.
14. Cox SB, Woolsey TA, Rovainen CM (1993) 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 13:899-913.
15. Dietrich HH, Ellsworth ML, Sprague RS, Dacey RGJ (2000) Red blood cell regulation of microvascular tone through adenosine triphosphate. Am J Physiol Heart Circ Physiol 278:H1294-H1298.
16. Duong TQ, Kim D-S, Ugurbil K, Kim S-G (2000) Spatiotemporal dynamics of the BOLD fMRI signals: toward mapping submillimeter cortical columns using the early negative response. Magn Reson Med 44:231-242.
17. Duong TQ, Kim D-S, Ugurbil K, Kim S-G (2001) Localized cerebral blood flow response at submillimeter columnar resolution. Proc Natl Acad Sci USA 98:10904-10909.
18. Erinjeri JP, Woolsey TA (2002) Spatial integration of vascular changes with neural activity in mouse cortex. J Cereb Blood Flow Metab 22:353-360.
19. Frostig RD, Lieke EE, Ts'o DY, Grinvald A (1990) Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc Natl Acad Sci USA 87:6082-6086.
20. Goodyear BG, Menon RS (2001) Brief visual stimulation allows mapping of ocular dominance in visual cortex using fMRI. Hum Brain Mapp 14:210-217.
21. Grinvald A, Manker A, Segal M (1982) Visualization of the spread of electrical activity in rat hippocampal slices by voltage-sensitive optical probes. J Physiol (Lond) 333:269-291.
22. Grinvald A, Lieke E, Frostig RD, Gilbert CD, Wiesel TN (1986) Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324:361-364.
23. Grinvald A, Slovin H, Vanzetta I (2000) Non-invasive visualization of cortical columns by f-MRI. Nat Neurosci 3:105-107.
24. Harel N, Mori N, Sawada S, Mount RJ, Harrison RV (2000) Three distinct auditory areas of cortex (AI, AII, and AAF) defined by optical imaging of intrinsic signals. NeuroImage 11:302-312.
25. Harel N, Zhao F, Wang P, Kim SG (2002) Layer specificity of BOLD and CBV fMRI signals at ultra-high resolution [abstract]. Conference on Functional Mapping of the Human Brain. NeuroImage 16:1221-1223.
26. Harrison RV, Harel N, Panesar J, Mount RJ (2002) Blood capillary distribution correlates with hemodynamic-based functional imaging in cerebral cortex. Cereb Cortex 12:225-233.
27. Hill DK, Keynes RD (1949) Opacity changes in stimulated nerve. J Physiol (Lond) 108:278-281.
28. Hu X, Le TH, Ugurbil K (1997) Evaluation of the early response in fMRI in individual subjects using short stimulus duration. Magn Reson Med 37:877-884.
29. Kim DS, Doung TQ, Kim SG (2000) High-resolution mapping of isoorientation columns by fMRI. Nat Neurosci 3:164-199.
30. 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 95:15741-15746.
31. Kohl M, Lindauer U, Royl G, Kühl M, Gold L, Villringer A, Dirnagl U (2000) Physical model for the spectroscopic analysis of cortical intrinsic optical signals. Phys Med Biol 45:3749-3764.
32. Kuschinsky W (2000) Regulation of cerebral blood Flow. In: Functional MRI (medical radiology - diagnostic imaging and radiation oncology) (Moonen CTW, Bandettini PA, eds). pp 15-25. New York: Springer.
33. 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.
34. Lindauer U, Royl G, Leithner C, Kühl M, Gold L, Gethmann J, Kohl-Bareis M, Villringer A, Dirnagl U (2001) No evidence for early decrease in blood oxygenation in rat whisker cortex in response to functional activation. NeuroImage 13:988-1001.
35. Lipton P (1973) Effects of membrane depolarization on light scattering by cerebral cortical slices. J Physiol (Lond) 231:365-383.
36. Logothetis NK (2000) Can current fMRI techniques reveal the microarchitecture of cortex? Nat Neurosci 3:413.
37. Logothetis NK (2003) The underpinnings of the BOLD functional magnetic resonance imaging signal. J Neurosci 23:3963-3971.
38. MacVicar BA, Hochman D (1991) Imaging of synaptically evoked intrinsic optical signals in hippocampal slices. J Neurosci 11:1458-1469.
39. Magistretti PJ, Pellerin L (1999) Astrocytes couple synaptic activity to glucose utilization in the brain. News Physiol Sci 14:177-182.
40. Magistretti PJ, Sorg O, Naichen Y, Pellerin L, de Rham S, Martin JL (1994) Regulation of astrocyte energy metabolism by neurotransmitters. Ren Physiol Biochem 17:168-171.
41. Magistretti JP, Pellerin L, Rothman DL, Shulman RG (1999) Energy on demand. Science 283:496-497.
42. Malonek D, Grinvald A (1996) Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science 272:551-554.
43. Malonek D, Dirnagl U, Lindauer U, Yamada K, Kanno I, Grinvald A (1997) Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. Proc Natl Acad Sci USA 94:14826-14831.
44. Mayhew J, Zheng Y, Hou Y, Vuksanovic B, Berwick J, Askew S, Coffey P (1999) Spectroscopic analysis of changes in remitted illumination: the response to increased neural activity in brain. NeuroImage 10:304-326.
45. Mayhew J, Johnston D, Martindale J, Jones M, Berwick J, Zheng Y (2001) Increased oxygen consumption following activation of brain: theoretical footnotes using spectroscopic data from barrel cortex. NeuroImage 13:975-987.
46. Mc Loughlin NP, Blasdel GG (1998) Wavelength-dependent differences between optically determined functional maps from macaque striate cortex. NeuroImage 7:326-336.
47. Menon RS, Ogawa S, Strupp JP, Ugurbil K (1997) Ocular dominance in human V1 demonstrated by functional magnetic resonance imaging. J Neurophysiol 77:2780-2787.
48. Nemoto M, Sheth S, Guiou M, Pouratian N, Chen JW, Toga AW (2004) Functional signal- and paradigm-dependent linear relationships between synaptic activity and hemodynamic responses in rat somatosensory cortex. J Neurosci 24:3850-3861.
49. Obrig H, Israel H, Kohl-Bareis M, Uludag K, Wenzel R, Muller B, Arnold G, Villringer A (2002) Habituation of the visually evoked potential and its vascular response: implications for neurovascular coupling in the healthy adult. NeuroImage 17:1-18.
50. Orbach HS (1988) Monitoring electrical activity in rat cerebral cortex. In: Spectroscopic membrane probes, Vol 3 (Lowe LM, ed), pp 115-136. Boca Raton, FL: CRC.
51. Orbach HS, Cohen LB, Grinvald A (1985) Optical mapping of electrical activity in rat somatosensory and visual cortex. J Neurosci 5:1886-1895.
52. Parri R, Crunelli V (2003) An astrocyte bridge from synapse to blood flow. Nat Neurosci 6:5-6.
53. Patel U (1983) Non-random distribution of blood vessels in the posterior region of the rat somatosensory cortex. Brain Res 289:65-70.
54. 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.
55. Pellerin L, Magistretti PJ (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci USA 91:10625-10629.
56. Pellerin L, Magistretti JP (2004) Neuroenergetics: calling during astrocytes to satisfy hungry neurons. The Neuroscientist 10:53-62.
57. Ratzlaff EH, Grinvald A (1991) A tandem-lens epifluorescence macroscope: hundred-fold brightness advantage for wide-field imaging. J Neurosci Methods 36:127-137.
58. Rector DM, Rogers RF, Schwaber JS, Harper RM, George JS (2001) Scattered-light imaging in vivo tracks fast and slow processes of neurophysiological activation. NeuroImage 14:977-994.
59. Roy C, Sherrington C (1890) On the regulation of the blood supply of the brain. J Physiol (Lond) 11:85-108.
60. Sheth SA, Nemoto M, Guiou M, Walker M, Pouratian N, Toga AW (2003) Evaluation of coupling between optical intrinsic signals and neuronal activity in rat somatosensory cortex. NeuroImage 19:884-894.
61. Sheth SA, Nemoto M, Guiou M, Walker M, Pouratian N, Hageman N, Toga AW (2004) Columnar specificity of microvascular oxygenation and volume responses: implications for functional brain mapping. J Neurosci 24:634-641.
62. Shmuel A, Grinvald A (1996) Functional organization for direction of motion and its relationship to orientation maps in cat area 18. J Neurosci 16:6945-6964.
63. Shulman RG, Hyder FL, Rothman DL (2001) Cerebral energetics and the glycogen shunt: neurochemical basis of functional imaging. Proc Natl Acad Sci USA 98:6417-6422.
64. Stamler JS, Jia L, Eu JP, McMahon TJ, Demchenko IT, Bonaventura J, Gernert K, Piantadosi CA (1997) Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 276:2034-2037.
65. Thompson JK, Peterson MR, Freeman RD (2003) Single-neuron activity and tissue oxygenation in the cerebral cortex. Science 299:1070-1072.
66. Ugurbil K, Toth L, Kim DS (2003) How accurate is magnetic resonance imaging of brain function? Trends Neurosci 26:1108-1114.
67. Vanzetta I, Grinvald A (1999) Increased cortical oxidative metabolism due to sensory stimulation: implications for functional brain imaging. Science 286:1555-1558.
68. Vanzetta I, Grinvald A (2001) Evidence and no evidence for the initial dip in the anesthetized rat; implications for human functional brain imaging. NeuroImage 13:959-967.
69. Vanzetta I, Slovin H, Grinvald A (2002) Spatio-temporal characteristics of neurovascular coupling in the anesthetized cat and the awake monkey. In: Brain activation and CBF control (Tomita M, Kanno I, Hamel E, eds), pp 145-155. Tokyo: Elsevier.
70. Vanzetta I, Slovin H, Omer DB, Grinvald A (2004) Columnar resolution of blood volume and oximetry functional maps in the behaving monkey: implications for fMRI. Neuron 42:843-854.
71. Versnel H, Mossop JE, Mrsic-Flogel TD, Ahmed B, Moore DR (2002) Optical imaging of intrinsic signals in ferret auditory cortex: responses to narrowband sound stimuli. J Neurophysiol 88:1545-1558.
72. Villringer A, Dirnagl U (1995) Coupling of brain activity and cerebral blood flow: basis of functional neuroimaging. Cerebrovasc Brain Metab Rev 7:240-276.
73. Wang G, Tanaka K, Tanifuji M (1996) Optical imaging of functional organization in the monkey inferotemporal cortex. Science 272:1665-1668.
74. Weliky M, Bosking WH, Fitzpatrick D (1996) A systematic map of direction preference in primary visual cortex. Nature 379:725-728.
75. Yacoub E, Duong TQ, Van De Moortele PF, Lindquist M, Adriany G, Kim SG, Ugurbil K, Hu X (2003) Spin-echo fMRI in humans using high spatial resolutions and high magnetic fields. Magn Reson Med 49:655-664.
76. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, Carmignoto G (2003) Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6:43-50.