SpringerProtocols: Abstract: 10. Application of Magnetic Resonance Imaging to Study Pathophysiology in Brain Disease Models

10. Application of Magnetic Resonance Imaging to Study Pathophysiology in Brain Disease Models

By: Rick M. Dijkhuizen²

Abstract

Full Text

Download PDF (1259K)

Magnetic resonance imaging (MRI) provides a noninvasive and multimodal tool to study neurological disorders in experimental models. MRI experiments can be sensitized to various contrast parameters and, hence, enable comprehensive assessment of normal and abnormal brain physiology. Different conventional and novel MRI techniques have been developed that supply specific information on lesion location and size (e.g., T₂- and diffusion-weighted MRI), alterations in tissue structure (e.g., magnetization transfer imaging and diffusion tensor imaging), perfusion deficits (perfusion MRI), brain activation (functional MRI), cell migration (cellular MRI), gene expression (molecular MRI), and more. The advantages of in vivo, longitudinal, and multiparametric studies with MRI provide unique opportunities for characterizing and delineating experimental models of neurological diseases and pathophysiological mechanisms, as well as spontaneous and treatment-induced recovery mechanisms.

Affiliation(s): (2) Department of Medical Imaging, Image Sciences Institute, University Medical Center Utrecht, Utrecht, The Netherlands

Book Title: Magnetic Resonance Imaging: Methods and Biologic Applications

Series: Methods in Molecular Medicine | Volume: 124 | Pub. Date: Nov-01-2005 | Page Range: 251-278 | DOI: 10.1385/1-59745-010-3:249

Subject: Imaging/Radiology

Key Words: Magnetic resonance imaging - brain diseases - physiopathology - animal models - diffusion - perfusion - fMRI - brain ischemia - neurodegenerative diseases - therapy

References

Download References

1.	Buonanno F. S., Pykett I. L., Kistler J. P., et al. (1982) Cranial anatomy and detection of ischemic stroke in the cat by nuclear magnetic resonance imaging. Radiology 143, 187–193.

2.	Levy R. M., Mano I., Brito A., and Hosobuchi Y. (1983) NMR imaging of acute experimental cerebral ischemia: time course and pharmacologic manipulations. Am. J. Neuroradiol. 4, 238–241.

3.	Stewart W. A., Alvord E. C., Hruby S., Hall L. D., and Paty D. W. (1985) Early detection of experimental allergic encephalomyelitis by magnetic resonance imaging. Lancet 2, 898.

4.	Bederson J. B., Bartkowski H. M., Moon K., et al. (1986) Nuclear magnetic resonance imaging and spectroscopy in experimental brain edema in a rat model. J. Neurosurg. 64, 795–802.

5.	O’Brien J. T., Noseworthy J. H., Gilbert J. J., and Karlik S. J. (1987) NMR changes in experimental allergic encephalomyelitis: NMR changes precede clinical and pathological events. Magn. Reson. Med. 5, 109–117.

6.	van Bruggen N., Roberts T. P., and Cremer J. E. (1994) The application of magnetic resonance imaging to the study of experimental cerebral ischaemia. Cerebrovasc. Brain Metab. Rev. 6, 180–210.

7.	Kato H., Kogure K., Ohtomo H., et al. (1986) Characterization of experimental ischemic brain edema utilizing proton nuclear magnetic resonance imaging. J. Cereb. Blood Flow Metab. 6, 212–221.

8.	Eis M., Els T., and Hoehn-Berlage M. (1995) High resolution quantitative relaxation and diffusion MRI of three different experimental brain tumors in rat. Magn. Reson. Med. 34, 835–844.

9.	Hoehn-Berlage M., Eis M., Back T., Kohno K., and Yamashita K. (1995) Changes of relaxation times (T1, T₂) and apparent diffusion coefficient after permanent middle cerebral artery occlusion in the rat: temporal evolution, regional extent, and comparison with histology. Magn. Reson. Med. 34, 824–834.

10.	Bose B., Jones S. C., Lorig R., Friel H. T., Weinstein M., and Little J. R. (1988) Evolving focal cerebral ischemia in cats: spatial correlation of nuclear magnetic resonance imaging, cerebral blood flow, tetrazolium staining, and histopathology. Stroke 19, 28–37.

11.	Allegrini P. R. and Sauer D. (1992) Application of magnetic resonance imaging to the measurement of neurodegeneration in rat brain: MRI data correlate strongly with histology and enzymatic analysis. Magn. Reson. Imaging 10, 773–778.

12.	Palmer G. C., Peeling J., Corbett D., Del Bigio M. R., and Hudzik T. J. (2001) T₂-weighted MRI correlates with long-term histopathology, neurology scores, and skilled motor behavior in a rat stroke model. Ann. N. Y. Acad. Sci. 939, 283–296.

13.	Calamante F., Lythgoe M. F., Pell G. S., et al. (1999) Early changes in water diffusion, perfusion, T1, and T₂ during focal cerebral ischemia in the rat studied at 8.5 T. Magn. Reson. Med. 41, 479–485.

14.	Kettunen M. I., Grohn O. H., Lukkarinen J. A., Vainio P., Silvennoinen M. J., and Kauppinen R. A. (2000) Interrelations of T(1) and diffusion of water in acute cerebral ischemia of the rat. Magn. Reson. Med. 44, 833–839.

15.	Quast M. J., Huang N. C., Hillman G. R., and Kent T. A. (1993) The evolution of acute stroke recorded by multimodal magnetic resonance imaging. Magn. Reson. Imaging 11, 465–471.

16.	van der Toorn A., Verheul H. B., Berkelbach van der Sprenkel J. W., Tulleken C. A., and Nicolay K. (1994) Changes in metabolites and tissue water status after focal ischemia in cat brain assessed with localized proton MR spectroscopy. Magn. Reson. Med. 32, 685–69

17.	Ogawa S., Lee T. M., Kay A. R., and Tank D. W. (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc. Natl. Acad. Sci. USA 87, 9868–9872.

18.	Gustafsson O., Rossitti S., Ericsson A., and Raininko R. (1999) MR imaging of experimentally induced intracranial hemorrhage in rabbits during the first 6 hours. Acta Radiol. 40, 360–36

19.	Moseley M. E., de Crespigny A. J., Roberts T. P., Kozniewska E., and Kucharczyk J. (1993) Early detection of regional cerebral ischemia using highspeed MRI. Stroke 24, 160–165.

20.	Ono Y., Morikawa S., Inubushi T., Shimizu H., and Yoshimoto T. (1997) T₂-weighted magnetic resonance imaging of cerebrovascular reactivity in rat reversible focal cerebral ischemia. Brain Res.* 744, 207–215.

21.	Mazurchuk R., Zhou R., Straubinger R. M., Chau R. I., and Grossman Z. (1999) Functional magnetic resonance (fMR) imaging of a rat brain tumor model: implications for evaluation of tumor microvasculature and therapeutic response. Magn. Reson. Imaging 17, 537–548.

22.	Runge V. M., Price A. C., Wehr C. J., Atkinson J. B., and Tweedle M. F. (1985) Contrast enhanced MRI. Evaluation of a canine model of osmotic bloodbrain barrier disruption. Invest. Radiol. 20, 830–844.

23.	Whelan H. T., Clanton J. A., Moore P. M., Tolner D. J., Kessler R. M., and Whetsell W. O., Jr. (1987) Magnetic resonance brain tumor imaging in canine glioma. Neurology 37, 1235–1239.

24.	Wilkins D. E., Raaphorst G. P., Saunders J. K., Sutherland G. R., and Smith I. C. (1995) Correlation between Gd-enhanced MR imaging and histopathology in treated and untreated 9L rat brain tumors. Magn. Reson. Imaging 13, 89–96.

25.	McNamara M. T., Brant-Zawadzki M., Berry I., et al. (1986) Acute experimental cerebral ischemia: MR enhancement using Gd-DTPA. Radiology 158, 701–705.

26.	Van de Vyver F. L. and Peersman G. V. (1990) Experimental cerebral infarction in the rat: utility of Gd-DOTA for MR imaging. Magn. Reson. Imaging 8, 333–340.

27.	Hawkins C. P., Munro P. M., MacKenzie F., et al. (1990) Duration and selectivity of blood-brain barrier breakdown in chronic relapsing experimental allergic encephalomyelitis studied by gadolinium-DTPA and protein markers. Brain 113 (Pt 2), 365–378.

28.	Namer I. J., Steibel J., Poulet P., Armspach J. P., Mauss Y., and Chambron J. (1992) In vivo dynamic MR imaging of MBP-induced acute experimental allergic encephalomyelitis in Lewis rat. Magn. Reson. Med. 24, 325–334.

29.	Karlik S. J., Grant E. A., Lee D., and Noseworthy J. H. (1993) Gadolinium enhancement in acute and chronic-progressive experimental allergic encephalomyelitis in the guinea pig. Magn. Reson. Med. 30, 326–331.

30.	van der Sanden B. P., Rozijn T. H., Rijken P. F., et al. (2000) Noninvasive assessment of the functional neovasculature in 9L-glioma growing in rat brain by dynamic 1H magnetic resonance imaging of gadolinium uptake. J. Cereb. Blood Flow Metab. 20, 861–870.

31.	Neumann-Haefelin T., Kastrup A., de Crespigny A., et al. (2000) Serial MRI after transient focal cerebral ischemia in rats: dynamics of tissue injury, bloodbrain barrier damage, and edema formation. Stroke 31, 1965–1972; discussion 1972-1963.

32.	Knight R. A., Barker P. B., Fagan S. C., Li Y., Jacobs M. A., and Welch K. M. (1998) Prediction of impending hemorrhagic transformation in ischemic stroke using magnetic resonance imaging in rats. Stroke 29, 144–151.

33.	Dijkhuizen R. M., Asahi M., Wu O., Rosen B. R., and Lo E. H. (2001) Delayed rt-PA treatment in a rat embolic stroke model: diagnosis and prognosis of ischemic injury and hemorrhagic transformation with magnetic resonance imaging. J. Cereb. Blood Flow Metab. 21, 964–971.

34.	Balaban R. S. and Ceckler T. L. (1992) Magnetization transfer contrast in magnetic resonance imaging. Magn. Reson. Q 8, 116–137.

35.	Brochet B. and Dousset V. (1999) Pathological correlates of magnetization transfer imaging abnormalities in animal models and humans with multiple sclerosis. Neurology 53, S12–S17.

36.	Dousset V., Brochet B., Vital A., et al. (1995) Lysolecithin-induced demyelination in primates: preliminary in vivo study with MR and magnetization transfer. Am. J. Neuroradiol. 16, 225–231.

37.	Deloire-Grassin M. S., Brochet B., Quesson B., et al. (2000) In vivo evaluation of remyelination in rat brain by magnetization transfer imaging. J. Neurol. Sci. 178, 10–16.

38.	Gareau P. J., Rutt B. K., Karlik S. J., and Mitchell J. R. (2000) Magnetization transfer and multicomponent T₂ relaxation measurements with histopathologic correlation in an experimental model of MS. J. Magn. Reson. Imaging 11, 586–59

39.	Ordidge R. J., Helpern J. A., Knight R. A., Qing Z. X., and Welch K. M. (1991) Investigation of cerebral ischemia using magnetization transfer contrast (MTC) MR imaging. Magn. Reson. Imaging 9, 895–902.

40.	Ewing J. R., Jiang Q., Boska M., et al. (1999) T1 and magnetization transfer at 7 Tesla in acute ischemic infarct in the rat. Magn. Reson. Med. 41, 696–705.

41.	Makela H. I., Kettunen M. I., Grohn O. H., and Kauppinen R. A. (2002) Quantitative T(1rho) and magnetization transfer magnetic resonance imaging of acute cerebral ischemia in the rat. J. Cereb. Blood Flow Metab. 22, 547–558.

42.	Ikezaki K., Takahashi M., Koga H., et al. (1997) Apparent diffusion coefficient (ADC) and magnetization transfer contrast (MTC) mapping of experimental brain tumor. Acta Neurochir. Suppl. (Wien) 70, 170–172.

43.	Quesson B., Bouzier A. K., Thiaudiere E., Delalande C., Merle M., and Canioni P. (1997) Magnetization transfer fast imaging of implanted glioma in the rat brain at 4.7 T: interpretation using a binary spin-bath model. J. Magn. Reson. Imaging 7, 1076–1083.

44.	Smith D. H., Meaney D. F., Lenkinski R. E., et al. (1995) New magnetic resonance imaging techniques for the evaluation of traumatic brain injury. J. Neurotrauma 12, 573–577.

45.	Kimura H., Meaney D. F., McGowan J. C., et al. (1996) Magnetization transfer imaging of diffuse axonal injury following experimental brain injury in the pig: characterization by magnetization transfer ratio with histopathologic correlation. J. Comput. Assist. Tomogr. 20, 540–546.

46.	Le Bihan D. (1988) Intravoxel incoherent motion imaging using steady-state free precession. Magn. Reson. Med. 7, 346–351.

47.	Moseley M. E., Cohen Y., Mintorovitch J., et al. (1990) Early detection of regional cerebral ischemia in cats: comparison of diffusion-and T₂-weighted MRI and spectroscopy. Magn. Reson. Med. 14, 330–346.

48.	Benveniste H., Hedlund L. W., and Johnson G. A. (1992) Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy. Stroke 23, 746–754.

49.	Verheul H. B., Balazs R., Berkelbach van der Sprenkel, et al. (1994) Comparison of diffusion-weighted MRI with changes in cell volume in a rat model of brain injury. NMR Biomed. 7, 96–100.

50.	van der Toorn A., Sykova E., Dijkhuizen R. M., et al. (1996) Dynamic changes in water ADC, energy metabolism, extracellular space volume, and tortuosity in neonatal rat brain during global ischemia. Magn. Reson. Med. 36, 52–60.

51.	Nicolay K., van der Toorn A., and Dijkhuizen R. M. (1995) In vivo diffusion spectroscopy. An overview. NMR Biomed. 8, 365–374.

52.	Nicolay K., Braun K. P., Graaf R. A., Dijkhuizen R. M., and Kruiskamp M. J. (2001) Diffusion NMR spectroscopy. N. M. R. Biomed. 14, 94–111.

53.	Gass A., Niendorf T., and Hirsch J. G. (2001) Acute and chronic changes of the apparent diffusion coefficient in neurological disorders-biophysical mechanisms and possible underlying histopathology. J. Neurol. Sci. 186 (Suppl. 1), S15–S23.

54.	Hoehn-Berlage M. (1995) Diffusion-weighted NMR imaging: application to experimental focal cerebral ischemia. NMR Biomed. 8, 345–358.

55.	Hoehn M., Nicolay K., Franke C., and van der Sanden B. (2001) Application of magnetic resonance to animal models of cerebral ischemia. J. Magn. Reson. Imaging 14, 491–509.

56.	Rumpel H., Nedelcu J., Aguzzi A., and Martin E. (1997) Late glial swelling after acute cerebral hypoxia-ischemia in the neonatal rat: a combined magnetic resonance and histochemical study. Pediatr. Res. 42, 54–59.

57.	Thornton J. S., Ordidge R. J., Penrice J., et al. (1997) Anisotropic water diffusion in white and gray matter of the neonatal piglet brain before and after transient hypoxia-ischaemia. Magn. Reson. Imaging 15, 433–440.

58.	D’Arceuil H. E., de Crespigny A. J., Rother J., et al. (1998) Diffusion and perfusion magnetic resonance imaging of the evolution of hypoxic ischemic encephalopathy in the neonatal rabbit. J. Magn. Reson. Imaging 8, 820–828.

59.	Hanstock C. C., Faden A. I., Bendall M. R., and Vink R. (1994) Diffusionweighted imaging differentiates ischemic tissue from traumatized tissue. Stroke 25, 843–848.

60.	Ito J., Marmarou A., Barzo P., Fatouros P., and Corwin F. (1996) Characterization of edema by diffusion-weighted imaging in experimental traumatic brain injury. J. Neurosurg. 84, 97–103.

61.	Busch E., Beaulieu C., de Crespigny A., and Moseley M. E. (1998) Diffusion MR imaging during acute subarachnoid hemorrhage in rats. Stroke 29, 2155–2161.

62.	Piepgras A., Elste V., Frietsch T., Schmiedek P., Reith W., and Schilling L. (2001) Effect of moderate hypothermia on experimental severe subarachnoid hemorrhage, as evaluated by apparent diffusion coefficient changes. Neurosurgery 48, 1128–1134; discussion 1134-1125.

63.	van den Bergh W. M., Zuur J. K., Kamerling N. A., et al. (2002) Role of magnesium in the reduction of ischemic depolarization and lesion volume after experimental subarachnoid hemorrhage. J. Neurosurg. 97, 416–422.

64.	Busza A. L., Allen K. L., King M. D., van Bruggen N., Williams S. R., and Gadian D. G. (1992) Diffusion-weighted imaging studies of cerebral ischemia in gerbils. Potential relevance to energy failure. Stroke 23, 1602–1612.

65.	Perez-Trepichio A. D., Xue M., Ng T. C., et al. (1995) Sensitivity of magnetic resonance diffusion-weighted imaging and regional relationship between the apparent diffusion coefficient and cerebral blood flow in rat focal cerebral ischemia. Stroke 26, 667–674; discussion 674-665.

66.	Verheul H. B., Tamminga K. S., Dijkhuizen R. M., et al. (1994) Focal ischemia in cat brain as studied by diffusion-weighted and dynamic susceptibility-contrast magnetic resonance imaging. MAGMA 2, 367–370.

67.	Kohno K., Hoehn-Berlage M., Mies G., Back T., and Hossmann K. A. (1995) Relationship between diffusion-weighted MR images, cerebral blood flow, and energy state in experimental brain infarction. Magn. Reson. Imaging 13, 73–80.

68.	Mancuso A., Karibe H., Rooney W. D., et al. (1995) Correlation of early reduction in the apparent diffusion coefficient of water with blood flow reduction during middle cerebral artery occlusion in rats. Magn. Reson. Med. 34, 368–377.

69.	Verheul H. B., Balazs R., Berkelbach van der Sprenkel J. W., Tulleken C. A., Nicolay K., and van Lookeren Campagne M. (1993) Temporal evolution of NMDA-induced excitotoxicity in the neonatal rat brain measured with 1H nuclear magnetic resonance imaging. Brain Res. 618, 203–212.

70.	Dijkhuizen R. M., van Lookeren Campagne M., Niendorf T., et al. (1996) Status of the neonatal rat brain after NMDA-induced excitotoxic injury as measured by MRI, MRS and metabolic imaging. NMR Biomed. 9, 84–92.

71.	Zhong J., Petroff O. A., Prichard J. W., and Gore J. C. (1993) Changes in water diffusion and relaxation properties of rat cerebrum during status epilepticus. Magn. Reson. Med. 30, 241–246.

72.	Righini A., Pierpaoli C., Alger J. R., and Di Chiro G. (1994) Brain parenchyma apparent diffusion coefficient alterations associated with experimental complex partial status epilepticus. Magn. Reson. Imaging 12, 865–871.

73.	Wall C. J., Kendall E. J., and Obenaus A. (2000) Rapid alterations in diffusionweighted images with anatomic correlates in a rodent model of status epilepticus Am. J. Neuroradiol. 21, 1841–1852.

74.	van Lookeren Campagne M., Verheul J. B., Nicolay K., and Balazs R. (1994) Early evolution and recovery from excitotoxic injury in the neonatal rat brain: a study combining magnetic resonance imaging, electrical impedance, and histology. J. Cereb. Blood Flow Metab. 14, 1011–1023.

75.	Zarow G. J., Graham S. H., Mintorovitch J., Chen J., Yang G., and Weinstein P. R. (1995) Diffusion-weighted magnetic resonance imaging during brief focal cerebral ischemia and early reperfusion: evolution of delayed infarction in rats. Neurol. Res. 17, 449–454.

76.	Dijkhuizen R. M., Knollema S., van der Worp H. B., et al. (1998) Dynamics of cerebral tissue injury and perfusion after temporary hypoxia-ischemia in the rat: evidence for region-specific sensitivity and delayed damage. Stroke 29, 695–704.

77.	Li F., Han S. S., Tatlisumak T., et al. (1999) Reversal of acute apparent diffusion coefficient abnormalities and delayed neuronal death following transient focal cerebral ischemia in rats. Ann. Neurol. 46, 333–342.

78.	van Lookeren Campagne M., Thomas G. R., Thibodeaux H., et al. (1999) Secondary reduction in the apparent diffusion coefficient of water, increase in cerebral blood volume, and delayed neuronal death after middle cerebral artery occlusion and early reperfusion in the rat. J. Cereb. Blood Flow Metab. 19, 1354–1364.

79.	Jiang Q., Zhang Z. G., Chopp M., et al. (1993) Temporal evolution and spatial distribution of the diffusion constant of water in rat brain after transient middle cerebral artery occlusion. J. Neurol. Sci. 120, 123–130.

80.	Verheul H. B., Berkelbach van der Sprenkel J. W., Tulleken C. A., Tamminga K. S., and Nicolay K. (1992) Temporal evolution of focal cerebral ischemia in the rat assessed by T₂-weighted and diffusion-weighted magnetic resonance imaging. Brain Topogr. 5, 171–176.

81.	Knight R. A., Dereski M. O., Helpern J. A., Ordidge R. J., and Chopp M. (1994) Magnetic resonance imaging assessment of evolving focal cerebral ischemia. Comparison with histopathology in rats. Stroke 25, 1252–1261; discussion 1261-1252.

82.	Pierpaoli C., Righini A., Linfante I., Tao-Cheng J. H., Alger J. R., and Di Chiro G. (1993) Histopathologic correlates of abnormal water diffusion in cerebral ischemia: diffusion-weighted MR imaging and light and electron microscopic study. Radiology 189, 439–448.

83.	Matsumoto K., Lo E. H., Pierce A. R., Wei H., Garrido L., and Kowall N. W. (1995) Role of vasogenic edema and tissue cavitation in ischemic evolution on diffusion-weighted imaging: comparison with multiparameter MR and immunohistochemistry. Am. J. Neuroradiol. 16, 1107–1115.

84.	Heide A. C., Richards T. L., Alvord E. C., Jr., Peterson J., and Rose L. M. (1993) Diffusion imaging of experimental allergic encephalomyelitis. Magn. Reson. Med. 29, 478–484.

85.	Richards T. L., Alvord E. C., Jr., He Y., et al. (1995) Experimental allergic encephalomyelitis in non-human primates: diffusion imaging of acute and chronic brain lesions. Mult. Scler. 1, 109–117.

86.	Braun K. P., Dijkhuizen R. M., de Graaf R. A., et al. (1997) Cerebral ischemia and white matter edema in experimental hydrocephalus: a combined in vivo MRI and MRS study. Brain Res. 757, 295–298.

87.	Kauppinen R. A. (2002) Monitoring cytotoxic tumour treatment response by diffusion magnetic resonance imaging and proton spectroscopy. NMR Biomed. 15, 6–17.

88.	Ross B. D., Chenevert T. L., and Rehemtulla A. (2002) Magnetic resonance imaging in cancer research. Eur. J. Cancer 38, 2147–2156.

89.	Chenevert T. L., McKeever P. E., and Ross B. D. (1997) Monitoring early response of experimental brain tumors to therapy using diffusion magnetic resonance imaging. Clin. Cancer Res. 3, 1457–1466.

90.	Basser P. J., Mattiello J., and LeBihan D. (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J. Magn. Reson. B 103, 247–254.

91.	van Gelderen P., de Vleeschouwer M. H., DesPres D., Pekar J., van Zijl P. C., and Moonen C. T. (1994) Water diffusion and acute stroke. Magn. Reson. Med. 31, 154–163.

92.	Lythgoe M. F., Busza A. L., Calamante F., et al. (1997) Effects of diffusion anisotropy on lesion delineation in a rat model of cerebral ischemia. Magn. Reson. Med. 38, 662–668.

93.	Basser P. J. and Pierpaoli C. (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. B 111, 209–219.

94.	Sotak C. H. (2002) The role of diffusion tensor imaging in the evaluation of ischemic brain injury-a review. NMR Biomed. 15, 561–569.

95.	Song S. K., Sun S. W., Ramsbottom M. J., Chang C., Russell J., and Cross A. H. (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17, 1429–1436.

96.	Xue R., van Zijl P. C., Crain B. J., Solaiyappan M., and Mori S. (1999) In vivo three-dimensional reconstruction of rat brain axonal projections by diffusion tensor imaging. Magn. Reson. Med. 42, 1123–1127.

97.	Zhang J., van Zijl P. C., and Mori S. (2002) Three-dimensional diffusion tensor magnetic resonance microimaging of adult mouse brain and hippocampus. Neuroimage 15, 892–901.

98.	Hossmann K. A. and Hoehn-Berlage M. (1995) Diffusion and perfusion MR imaging of cerebral ischemia. Cerebrovasc. Brain Metab. Rev. 7, 187–217.

99.	Calamante F., Thomas D. L., Pell G. S., Wiersma J., and Turner R. (1999) Measuring cerebral blood flow using magnetic resonance imaging techniques. J. Cereb. Blood Flow Metab. 19, 701–735.

100.	Rosen B. R., Belliveau J. W., Vevea J. M., and Brady T. J. (1990) Perfusion imaging with NMR contrast agents. Magn. Reson. Med. 14, 249–265.

101.	Ostergaard L., Weisskoff R. M., Chesler D. A., Gyldensted C., and Rosen B. R. (1996) High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis. Magn. Reson. Med. 36, 715–725.

102.	Wittlich F., Kohno K., Mies G., Norris D. G., and Hoehn-Berlage M. (1995) Quantitative measurement of regional blood flow with gadolinium diethylenetriaminepentaacetate bolus track NMR imaging in cerebral infarcts in rats: validation with the iodo[14C]antipyrine technique. Proc. Natl. Acad. Sci. USA 92, 1846–1850.

103.	Sakoh M., Rohl L., Gyldensted C., Gjedde A., and Ostergaard L. (2000) Cerebral blood flow and blood volume measured by magnetic resonance imaging bolus tracking after acute stroke in pigs: comparison with [(15)O]H(2)O positron emission tomography. Stroke 31, 1958–1964.

104.	Maeda M., Itoh S., Ide H., et al. (1993) Acute stroke in cats: comparison of dynamic susceptibility-contrast MR imaging with T₂-and diffusion-weighted MR imaging. Radiology 189, 227–232.

105.	Roberts T. P., Vexler Z., Derugin N., Moseley M. E., and Kucharczyk J. (1993) High-speed MR imaging of ischemic brain injury following stenosis of the middle cerebral artery. J. Cereb. Blood Flow Metab. 13, 940–946.

106.	Hamberg L. M., Macfarlane R., Tasdemiroglu E., et al. (1993) Measurement of cerebrovascular changes in cats after transient ischemia using dynamic magnetic resonance imaging. Stroke 24, 444–450; discussion 450-441.

107.	Kucharczyk J., Vexler Z. S., Roberts T. P., et al. (1993) Echo-planar perfusionsensitive MR imaging of acute cerebral ischemia. Radiology 188, 711–717.

108.	Minematsu K., Fisher M., Li L., and Sotak C. H. (1993) Diffusion and perfusion magnetic resonance imaging studies to evaluate a noncompetitive N-methyl-D-aspartate antagonist and reperfusion in experimental stroke in rats. Stroke 24, 2074–2081.

109.	Pathak A. P., Schmainda K. M., Ward B. D., Linderman J. R., Rebro K. J., and Greene A. S. (2001) MR-derived cerebral blood volume maps: issues regarding histological validation and assessment of tumor angio-genesis. Magn. Reson. Med. 46, 735–747.

110.	Cha S., Johnson G., Wadghiri Y. Z., et al. (2003) Dynamic, contrast-enhanced perfusion MRI in mouse gliomas: correlation with histopathology. Magn. Reson. Med. 49, 848–855.

111.	Hamberg L. M., Boccalini P., Stranjalis G., et al. (1996) Continuous assessment of relative cerebral blood volume in transient ischemia using steady state susceptibility-contrast MRI. Magn. Reson. Med. 35, 168–173.

112.	Mandeville J. B., Marota J. J., Kosofsky B. E., et al. (1998) Dynamic functional imaging of relative cerebral blood volume during rat forepaw stimulation. Magn. Reson. Med. 39, 615–624.

113.	Zaharchuk G., Yamada M., Sasamata M., Jenkins B. G., Moskowitz M. A., and Rosen B. R. (2000) Is all perfusion-weighted magnetic resonance imaging for stroke equal? The temporal evolution of multiple hemodynamic parameters after focal ischemia in rats correlated with evidence of infarction. J. Cereb. Blood Flow Metab. 20, 1341–1351.

114.	Boxerman J. L., Bandettini P. A., Kwong K. K., et al. (1995) The intravascular contribution to fMRI signal change: Monte Carlo modeling and diffusionweighted studies in vivo. Magn. Reson. Med. 34, 4–10.

115.	Dennie J., Mandeville J. B., Boxerman J. L., Packard S. D., Rosen B. R., and Weisskoff R. M. (1998) NMR imaging of changes in vascular morphology due to tumor angio-genesis. Magn. Reson. Med. 40, 793–799.

116.	Le Duc G., Peoc’h M., Remy C., et al. (1999) Use of T(2)-weighted susceptibility contrast MRI for mapping the blood volume in the glioma-bearing rat brain. Magn. Reson. Med. 42, 754–761.

117.	Jensen J. H. and Chandra R. (2000) MR imaging of microvasculature. Magn. Reson. Med. 44, 224–230.

118.	Detre J. A., Leigh J. S., Williams D. S., and Koretsky A. P. (1992) Perfusion imaging. Magn. Reson. Med. 23, 37–45.

119.	Kwong K. K., Belliveau J. W., Chesler D. A., et al. (1992) Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc. Natl. Acad. Sci. USA 89, 5675–5679.

120.	Kim S. G. (1995) Quantification of relative cerebral blood flow change by flowsensitive alternating inversion recovery (FAIR) technique: application to functional mapping. Magn. Reson. Med. 34, 293–301.

121.	Detre J. A., Zhang W., Roberts D. A., et al. (1994) Tissue specific perfusion imaging using arterial spin labeling. NMR Biomed. 7, 75–82.

122.	Tsekos N. V., Zhang F., Merkle H., Nagayama M., Iadecola C., and Kim S. G. (1998) Quantitative measurements of cerebral blood flow in rats using the FAIR technique: correlation with previous iodoantipyrine autoradiographic studies. Magn. Reson. Med. 39, 564–573.

123.	Zaharchuk G., Bogdanov A. A., Jr., Marota J. J., et al. (1998) Continuous assessment of perfusion by tagging including volume and water extraction (CAPTIVE): a steady-state contrast agent technique for measuring blood flow, relative blood volume fraction, and the water extraction fraction. Magn. Reson. Med. 40, 666–678.

124.	Pell G. S., Lythgoe M. F., Thomas D. L., et al. (1999) Reperfusion in a gerbil model of forebrain ischemia using serial magnetic resonance FAIR perfusion imaging. Stroke 30, 1263–1270.

125.	van Dorsten F. A., Hata R., Maeda K., et al. (1999) Diffusion-and perfusion-weighted MR imaging of transient focal cerebral ischaemia in mice. NMR Biomed. 12, 525–534.

126.	Forbes M. L., Hendrich K. S., Kochanek P. M., et al. (1997) Assessment of cerebral blood flow and CO2 reactivity after controlled cortical impact by perfusion magnetic resonance imaging using arterial spin-labeling in rats. J. Cereb. Blood Flow Metab. 17, 865–874.

127.	Silva A. C., Kim S. G., and Garwood M. (2000) Imaging blood flow in brain tumors using arterial spin labeling. Magn. Reson. Med. 44, 169–173.

128.	Schepers J., Veldhuis W. B., Pauw R. J., et al. (2004) Comparison of FAIR perfusion kinetics with DSC-MRI and functional histology in a model of transient ischemia. Magn. Reson. Med. 51, 312–320.

129.	Zhang W., Silva A. C., Williams D. S., and Koretsky A. P. (1995) NMR measurement of perfusion using arterial spin labeling without saturation of macromolecular spins. Magn. Reson. Med. 33, 370–376.

130.	Hyder F., Behar K. L., Martin M. A., Blamire A. M., and Shulman R. G. (1994) Dynamic magnetic resonance imaging of the rat brain during forepaw stimulation. J. Cereb. Blood Flow Metab. 14, 649–655.

131.	Silva A. C., Zhang W., Williams D. S., and Koretsky A. P. (1995) Multi-slice MRI of rat brain perfusion during amphetamine stimulation using arterial spin labeling. Magn. Reson. Med. 33, 209–214.

132.	Kerskens C. M., Hoehn-Berlage M., Schmitz B., et al. (1996) Ultrafast perfusion-weighted MRI of functional brain activation in rats during forepaw stimulation: comparison with T₂-weighted MRI. N. M. R. Biomed. 9, 20–23.

133.	Kennan R. P., Scanley B. E., Innis R. B., and Gore J. C. (1998) Physiological basis for BOLD MR signal changes due to neuronal stimulation: separation of blood volume and magnetic susceptibility effects. Magn. Reson. Med. 40, 840–846.

134.	van Bruggen N., Busch E., Palmer J. T., Williams S. P., and de Crespigny A. J. (1998) High-resolution functional magnetic resonance imaging of the rat brain: mapping changes in cerebral blood volume using iron oxide contrast media. J. Cereb. Blood Flow Metab. 18, 1178–1183.

135.	Lin Y. J. and Koretsky A. P. (1997) Manganese ion enhances T₁-weighted MRI during brain activation: an approach to direct imaging of brain function. Magn. Reson. Med. 38, 378–388.

136.	Pautler R. G., Silva A. C., and Koretsky A. P. (1998) In vivo neuronal tract tracing using manganese-enhanced magnetic resonance imaging. Magn. Reson. Med. 40, 740–748.

137.	Schmitz B., Bock C., Hoehn-Berlage M., Kerskens C. M., Bottiger B. W., and Hossmann K. A. (1998) Recovery of the rodent brain after cardiac arrest: a functional MRI study. Magn. Reson. Med. 39, 783–788.

138.	Reese T., Porszasz R., Baumann D., et al. (2000) Cytoprotection does not preserve brain functionality in rats during the acute post-stroke phase despite evidence of non-infarction provided by MRI. NMR Biomed. 13, 361–370.

139.	Abo M., Chen Z., Lai L. J., Reese T., and Bjelke B. (2001) Functional recovery after brain lesion-contralateral neuromodulation: an fMRI study. Neuroreport 12, 1543–1547.

140.	Dijkhuizen R. M., Ren J., Mandeville J. B., Wu O., et al. (2001) Functional magnetic resonance imaging of reorganization in rat brain after stroke. Proc. Natl. Acad. Sci. U. S. A. 98, 12,766–12,771.

141.	Tuor U. I., Hudzik T. J., Malisza K., Sydserff S., Kozlowski P., and Del Bigio M. R. (2001) Long-term deficits following cerebral hypoxia-ischemia in fourweek-old rats: correspondence between behavioral, histological, and magnetic resonance imaging assessments. Exp. Neurol. 167, 272–281.

142.	Dijkhuizen R. M., Singhal A. B., Mandeville J. B., et al. (2003) Correlation between brain reorganization, ischemic damage, and neurologic status after transient focal cerebral ischemia in rats: a functional magnetic resonance imaging study. J. Neurosci. 23, 510–517.

143.	Pelled G., Bergman H., and Goelman G. (2002) Bilateral overactivation of the sensorimotor cortex in the unilateral rodent model of Parkinson’s disease-a functional magnetic resonance imaging study. Eur. J. Neurosci. 15, 389–394.

144.	Opdam H. I., Federico P., Jackson G. D., et al. (2002) A sheep model for the study of focal epilepsy with concurrent intracranial EEG and functional MRI. Epilepsia 43, 779–7

145.	Chen Q., Andersen A. H., Zhang Z., Ovadia A., Gash D. M., and Avison M. J. (1996) Mapping drug-induced changes in cerebral R2* by multiple gradient recalled echo functional MRI. Magn. Reson. Imaging 14, 469–476.

146.	Chen Y. C., Galpern W. R., Brownell A. L., et al. (1997) Detection of dopaminergic neurotransmitter activity using pharmacologic MRI: correlation with PET, microdialysis, and behavioral data. Magn. Reson. Med. 38, 389–398.

147.	Chen Y. I., Brownell A. L., Galpern W., et al. (1999) Detection of dopaminergic cell loss and neural transplantation using pharmacological MRI, PET and behavioral assessment. Neuroreport 10, 2881–2886.

148.	Chen Q., Andersen A. H., Zhang Z., et al. (1999) Functional MRI of basal ganglia responsiveness to levodopa in parkinsonian rhesus monkeys. Exp. Neurol. 158, 63–75.

149.	Reese T., Bochelen D., Baumann D., Rausch M., Sauter A., and Rudin M. (2002) Impaired functionality of reperfused brain tissue following short transient focal ischemia in rats. Magn. Reson. Imaging 20, 447–454.

150.	Mueggler T., Sturchler-Pierrat C., Baumann D., Rausch M., Staufenbiel M., and Rudin M. (2002) Compromised hemodynamic response in amyloid precursor protein transgenic mice. J. Neurosci. 22, 7218–7224.

151.	Norman A. B., Thomas S. R., Pratt R. G., Lu S. Y., and Norgren R. B. (1992) Magnetic resonance imaging of neural transplants in rat brain using a superparamagnetic contrast agent. Brain Res. 594, 279–283.

152.	Bulte J. W., Duncan I. D., and Frank J. A. (2002) In vivo magnetic resonance tracking of magnetically labeled cells after transplantation. J. Cereb. Blood Flow Metab. 22, 899–907.

153.	Zimmer C., Weissleder R., Poss K., Bogdanova A., Wright S. C., Jr., and Enochs W. S. (1995) MR imaging of phagocytosis in experimental gliomas. Radiology 197, 533–538.

154.	Dousset V., Delalande C., Ballarino L., et al. (1999) In vivo macrophage activity imaging in the central nervous system detected by magnetic resonance. Magn. Reson. Med. 41, 329–333.

155.	Floris S., Blezer E. L., Schreibelt G., et al. (2004) Blood-brain barrier permeability and monocyte infiltration in experimental allergic encephalomyelitis: a quantitative MRI study. Brain 127, 616–627.

156.	Hoehn M., Kustermann E., Blunk J., et al. (2002) Monitoring of implanted stem cell migration in vivo: a highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proc. Natl. Acad. Sci. USA 99, 16,267–16,272.

157.	Modo M., Mellodew K., Cash D., et al. (2004) Mapping transplanted stem cell migration after a stroke: a serial, in vivo magnetic resonance imaging study. Neuroimage 21, 311–317.

158.	Weissleder R. and Mahmood U. (2001) Molecular imaging. Radiology 219, 316–333.

159.	Blasberg R. (2002) Imaging gene expression and endogenous molecular processes: molecular imaging. J. Cereb. Blood Flow Metab. 22, 1157–1164.

160.	Remsen L. G., McCormick C. I., Roman-Goldstein S., et al. (1996) MR of carcinoma-specific monoclonal antibody conjugated to monocrystalline iron oxide nanoparticles: the potential for noninvasive diagnosis. Am. J. Neuroradiol. 17, 411–418.

161.	Sipkins D. A., Gijbels K., Tropper F. D., Bednarski M., Li K. C., and Steinman L. (2000) ICAM-1 expression in autoimmune encephalitis visualized using magnetic resonance imaging. J. Neuroimmunol. 104, 1–9.

162.	Sibson N. R., Blamire A. M., Bernades-Silva M., et al. (2004) MRI detection of early endothelial activation in brain inflammation. Magn. Reson. Med. 51, 248–252.

163.	Poduslo J. F., Wengenack T. M., Curran G. L., et al. (2002) Molecular targeting of Alzheimer’s amyloid plaques for contrast-enhanced magnetic resonance imaging. Neurobiol. Dis. 11, 315–329.

Comments (Loading...)

Post comment/View all comments