New insights into the hemodynamic blood oxygenation level-dependent response through combination of functional magnetic resonance imaging and optical recording in gerbil barrel cortex

Journal of Neuroscience

Volumn 20, Issue 9, 2000, Pages 3328-3338

  Hess, Andreas ^a   Stiller, Detlef ^a   Kaulisch, Thomas ^a   Heil, Peter ^a   Scheich, Henning ^a  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

2 DG; Barrel field; BOLD; FMRI; Gerbil; Imaging; Optical recording; Rodent; Somatosensory cortex

Indexed keywords

DEOXYHEMOGLOBIN;

ANIMAL EXPERIMENT; ARTICLE; BLOOD OXYGENATION; BLOOD VOLUME; CELL ACTIVATION; GERBIL; HEMODYNAMICS; NERVE CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RECORDING; SIGNAL DETECTION; SOMATOSENSORY CORTEX;

EID: 0034193469     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-09-03328.2000     Document Type: Article

References (80)

1. Armstrong-James M, Fox K (1987) Spatiotemporal convergence and divergence in the rat S1 "barrel" cortex. J Comp Neurol 263:265-281.
2. Bandettini PA, Wong EC (1997) Magnetic resonance imaging of human brain function. Principles, practicalities, and possibilities. Clin Neurosurg 8:345-371.
3. Bandettini PA, Jesmanowicz A, Wong EC, Hyde JS (1993) Processing strategies for time-course data sets in functional MRI of the human brain. Magn Reson Med 30:161-173.
4. Baumgart F, Gaschler-Markefski B, Woldorff MG, Heinze HJ, Scheich H (1999) A movement-sensitive area in auditory cortex [letter]. Nature 400:724-726.
5. Blasdel GG, Salama G (1986) Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321:579-585.
6. Bonhoeffer T. Grinvald A (1996) Optical imaging based on intrinsic signals: the methodology. In: Brain mapping: the methods (Toga AW, Mazziotta JC, eds), pp 55-97. London: Academic.
7. Boxerman JL, Bandettini PA, Kwong KK, Baker JR, Davis TL, Rosen BR, Weisskoff RM (1995) The intravascular contribution to fMRI signal change: Monte Carlo modeling and diffusion-weighted studies in vivo. Magn Reson Med 34:4-10.
8. Buchbinder BR, Cosgrove GR (1998) Cortical activation MR studies in brain disorders. Magn Reson Imaging Clin N Am 6:67-93.
9. Burdett NG, Menon DK, Carpenter TA, Jones JG, Hall LD (1995) Visualisation of changes in regional cerebral blood flow (rCBF) produced by ketamine using long TE gradient-echo sequences: preliminary results. Magn Reson Imaging 13:549-553.
10. 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.
11. 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.
12. Cannestra AF, Blood AJ, Black KL, Toga AW (1996) The evolution of optical signals in human and rodent cortex. NeuroImage 3:202-208.
13. Chen-Bee CH, Kwon MC, Masino SA, Frostig RD (1996) Areal extent quantification of functional representations using intrinsic signal optical imaging. J Neurosci Methods 68:27-37.
14. Cohen MS, Bookheimer SY (1994) Localization of brain function using magnetic resonance imaging. Trends Neurosci 17:268-277.
15. 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.
16. Dale AM, Buckner RL (1997) Selective averaging of rapidly presented individual trials using fMRI. Human Brain Mapp 5:329-340.
17. Davis TL, Kwong KK, Weisskoff RM, Rosen BR (1998) Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc Natl Acad Sci USA 95:1834-1839.
18. DeYoe EA, Bandettini P, Neitz J, Miller D, Winans P (1994) Functional magnetic resonance imaging (FMRI) of the human brain. J Neurosci Methods 54:171-187.
19. Frahm J, Merboldt KD, Hanicke W. Kleinschmidt A, Boecker H (1994) Brain or vein-oxygenation or flow? On signal physiology in functional MRI of human brain activation. NMR Biomed 7:45-53.
20. Fransson P, Kruger G, Merboldt KD, Frahm J (1997) A comparative FLASH and EPI study of repetitive and sustained visual activation. NMR Biomed 10:204-207.
21. Fransson P, Kruger G, Merboldt KD, Frahm J (1998) Temporal characteristics of oxygenation-sensitive MRI responses to visual activation in humans. Magn Reson Med 39:912-919.
22. Friston KJ, Jezzard P, Turner R (1994) Analysis of functional MRI time-series. Human Brain Mapp 1:153-171.
23. Frostig RD, Licke 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.
24. Fujibayashi T, Sugiura Y, Yanagimoto M, Harada J, Goto Y (1994) Brain energy metabolism and blood flow during sevofluranc and halothane anesthesia: effects of hypocapnia and blood pressure fluctuations [corrected and republished article originally printed in Acta Anaesthesiol Scand (1993) 37:806-810]. Acta Anaesthesiol Scand 38:413-418.
25. Gaschler B, Baumgart F, Tempelman C, Stiller D, Heinze HJ, Scheich H (1997) Statistical methods in functional magnetic resonance imaging with respect to non-stationary time series - auditory cortex activity. Magn Reson Med 38:811-820.
26. Gati JS, Menon RS, Ugurbil K, Rutt BK (1997) Experimental determination of the BOLD field strength dependence in vessels and tissue. Magn Reson Med 38:296-302.
27. Goldreich D, Peterson BE, Merzenich MM (1998) Optical imaging and electrophysiology of rat barrel cortex. II. Responses to paired-vibrissa deflections. Cereb Cortex 8:184-192.
28. 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.
29. Haacke M, Lai S, Reichenbach J, Kuppusamy F, Hoogenraad F, Takeichi H, Lin W (1997) In vivo measurement of blood oxygen saturation using magnetic resonance imaging: a direct validation of the blood oxygen level dependent concept in functional brain imaging. Human Brain Mapp 5:341-346.
30. Hennig J, Nauerth A, Friedburg H (1986) RARE imaging: a fast imaging method for clinical MR. Magn Reson Med 3:823-833.
31. Hennig J, Janz C, Speck O, Ernst T (1997) Is there a different type of MR-contrast in the early phase of functional activation? Adv Exp Med Biol 413:35-42.
32. Hess A, Scheich H (1996) Optical and FDG mapping of frequency-specific activity in auditory cortex. NeuroReport 7:2643-2647.
33. Hess A, Lohmann K, Gundelfinger ED, Scheich H (1998) A new method for reliable and efficient reconstruction of 3-dimensional images from autoradiographs of brain sections. J Neurosci Methods 84:77-86.
34. Hoge RD, Atkinson J, Gill B, Crelier GR, Marrett S, Pike GB (1999) Investigation of BOLD signal dependence on cerebral blood flow and oxygen consumption: the deoxyhemoglobin dilution model [in process citation]. Magn Reson Med 42:849-863.
35. Howseman AM, Bowtell RW (1999) Functional magnetic resonance imaging: imaging techniques and contrast mechanisms. Philos Trans R Soc Lond B Biol Sci 354:1179-1194.
36. 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.
37. Jones RA (1999) Origin of the signal undershoot in BOLD studies of the visual cortex [in process citation]. NMR Biomed 12:299-308.
38. Jones RA, Schirmer T, Lipinski B, Elbel GK, Auer DP (1998) Signal undershoots following visual stimulation: a comparison of gradient and spin-echo BOLD sequences. Magn Reson Med 40:112-118.
39. Josephs O. Henson RN (1999) Event-related functional magnetic resonance imaging: modelling, inference and optimization. Philos Trans R Soc Lond B Biol Sci 354:1215-1228.
40. Kato T, Takashima S, Kamada K, Kishibayashi J, Sunohara N, Ozaki T (1993) Advantage of near-infrared spectroscopy in the human functional MR imaging in brain. Proceedings of the SMRM, 12th annual meeting, New York, August.
41. Kato T, Yamashita Y, Sugihara K, Furusho J, Tazaki I, Tanaka D, Maki A, Yamamoto T, Koizumi H, Ichikawa N, Iikura Y (1999) Cerebral autonomic functional test using human functional near-infraredgraphy (FNIR). NeuroImage 9:221.
42. Kim DS, Duong TQ, Kim SG (2000) High-resolution mapping of isoorientation columns by fMRI. Nat Neurosci 3:164-169.
43. Kim SG, Ugurbil K (1997) Comparison of blood oxygenation and cerebral blood flow effects in fMRI: estimation of relative oxygen consumption change. Magn Reson Med 38:59-65.
44. Kim SG, Rostrup E, Larsson HB, Ogawa S, Paulson OB (1999) Determination of relative CMRO2 from CBF and BOLD changes: significant increase of oxygen consumption rate during visual stimulation. Magn Reson Med 41:1152-1161.
45. Kindermann SS, Karimi A, Symonds L, Brown GG, Jeste DV Kim SG, Ugurbil K (1997) Review of functional magnetic resonance imaging in schizophrenia. Schizophr Res 27:143-156.
46. Kossut M, Hand PJ, Greenberg J, Hand CL (1988) Single vibrissal cortical column in SI cortex of rat and its alterations in neonatal and adult vibrissa-deafferented animals: a quantitative 2DG study. J Neurophysiol 60:829-852.
47. Krubitzer LA, Sesma MA, Kaas JH (1986) Microelectrode maps, myeloarchitecture, and cortical connections of three somatotopically organized representations of the body surface in the parietal cortex of squirrels. J Comp Neurol 250:403-430.
48. Kwong KKB, Belliveau JW, Chesler DA (1992) Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci USA 89:5675-5679.
49. Lindauer U, Villringer A, Dirnagl U (1993) Characterization of CBF response to somatosensory stimulation: model and influence of anesthetics. Am J Physiol 264:H1223-H1228.
50. 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.
51. Mandeville JB, Marota JJA, Kosofsky BE, Keltner JR, Weissleder R, Rosen BR, Weisskoff RM (1998) Dynamic functional imaging of relative cerebral blood volume during rat forepaw stimulation. Magn Reson Med 39:615-624.
52. Marota JJ, Ayata C, Moskowitz MA, Weisskoff RM, Rosen BR, Mandeville JB (1999) Investigation of the early response to rat forepaw stimulation. Magn Reson Med 41:247-252.
53. Masino SA, Kwon MC, Dory Y, Frostig RD (1993) Characterization of functional-organization within rat barrel cortex using intrinsic signal optical imaging through a thinned skull. Proc Natl Acad Sci USA 90:9998-10002.
54. McCasland JS, Hibbard LS (1997) GABAergic neurons in barrel cortex show strong, whisker-dependent metabolic activation during normal behavior. J Neurosci 17:5509-5527.
55. Menon RS, Goodyear BG (1999) Submillimeter functional localization in human striate cortex using BOLD contrast at 4 Tesla: implications for the vascular point-spread function. Magn Reson Med 41:230-235.
56. Menon RS, Ogawa S, Hu X, Strupp JP, Anderson P, Ugurbil K (1995) BOLD based functional MRI at 4 Tesla includes a capillary bed contribution: echo-planar imaging correlates with previous optical imaging using intrinsic signals. Magn Reson Med 33:453-459.
57. Menon RS, Ogawa S, Tank DW, Ugurbil K (1993) Tesla gradient recalled echo characteristics of photic stimulation-induced signal changes in the human primary visual cortex. Magn Reson Med 30:380-386.
58. 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.
59. Narayan SM, Santori EM, Blood AJ, Burton JS, Toga AW (1994) Imaging optical reflectance in rodent barrel and forelimb sensory cortex. NeuroImage 1:181-190.
60. Ogawa S, Lee TM, Kay AR, Tank DW (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 87:9868-9872.
61. Ogawa S, Tank DW, Menon R, Ellermann JM, Kim S-G, Merkle H, Ugurbil K (1992) Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 89:5951-5955.
62. Ogawa S, Menon RS, Tank DW, Kim SG, Merkle H, Ellermann JM, Ugurbil K (1993) Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model. Biophys J 64:803-812.
63. Pauling L (1977) Magnetic properties and structure of oxyhemoglobin. Proc Natl Acad Sci USA 74:2612-2613.
64. Paxinos G (1995) The rat nervous system. London: Academic.
65. Peterson BE, Goldreich D, Merzenich MM (1998) Optical imaging and electrophysiology of rat barrel cortex. I. Responses to small single-vibrissa deflections. Cereb Cortex 8:173-183.
66. Ratzlaff EH, Grinvald A (1991) A tandem-lens epifluorescence macroscope: hundred-fold brightness advantage for wide-field imaging. J Neurosci Methods 36:127-137.
67. Richter K, Hess A, Scheich H (1999) Functional mapping of transsynaptic effects of local manipulation of inhibition in gerbil auditory cortex. Brain Res 831:184-199.
68. Scheich H, Heil P, Langner G (1993) Functional organization of auditory cortex in the mongolian gerbil (Meriones unguiculatus). II. Tonotopic 2-deoxyglucose. Eur J Neurosci 5:898-914.
69. Scheich H, Baumgart F, Gaschler-Markefski B, Tegeler C, Tempelmann C, Heinze HJ, Schindler F, Stiller D (1998) Functional magnetic resonance imaging of human auditory cortex area involved in foreground-background decomposition. Eur J Neurosci 10:803-809.
70. Schwarzbauer C, Heinke W (1999) Investigating the dependence of BOLD contrast on oxidative metabolism. Magn Reson Med 41:537-543.
71. Thomas H, Tillein J, Heil P, Scheich H (1993) Functional organization of auditory cortex in the mongolian gerbil (Meriones unguiculatus ). I. Electrophysiological mapping of frequency representation and distinction of fields. Eur J Neurosci 5:882-897.
72. Thulborn KR, Waterton JC, Matthews PM, Radda GK (1982) Oxygenation dependence of the transverse relaxation time of water protons in whole blood at high field. Biochim Biophys Acta 714:265-270.
73. Turner R, Howseman A, Rees GE, Josephs O, Friston K (1998) Functional magnetic resonance imaging of the human brain: data acquisition and analysis. Exp Brain Res 123:5-12.
74. Ugurbil K, Hu X, Chen W, Zhu XH, Kim SG, Georgopoulos A (1999) Functional mapping in the human brain using high magnetic fields. Philos Trans R Soc Lond B Biol Sci 354:1195-1213.
75. Welker C (1976) Receptive fields of barrels in the somatosensory neocortex of the rat. J Comp Neurol 166:173-189.
76. Welker E, Rao SB, Dorfl J, Melzer P, van der Loos H (1992) Plasticity in the barrel cortex of the adult mouse: effects of chronic stimulation upon deoxyglucose uptake in the behaving animal. J Neurosci 12:153-170.
77. Wong-Riley MT, Welt C (1980) Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. Proc Natl Acad Sci USA 77:2333-2347.
78. Woolsey TA, Welker C, Schwartz RH (1975) Comparative anatomical studies of the SmL face cortex with special reference to the occurrence of "barrels" in layer IV. J Comp Neurol 164:79-94.
79. Yang X, Hyder F, Shulman RG (1996) Activation of single whisker barrel in rat brain localized by functional magnetic resonance imaging. Proc Natl Acad Sci USA 93:475-478.
80. Yang X, Hyder F, Shulman RG (1997) Functional MRI BOLD signal coincides with electrical activity in the rat whisker barrels [in process citation]. Magn Reson Med 38:874-877.