Functional and structural correlates of magnetic resonance patterns in a new in vitro model of cerebral ischemia by transient occlusion of the medial cerebral artery

Neurobiology of Disease

Volumn 39, Issue 2, 2010, Pages 181-191

  Breschi, Gian Luca ^a   Librizzi, Laura ^a   Pastori, Chiara ^a   Zucca, Ileana ^a   Mastropietro, Alfonso ^a,b   Cattalini, Alessandro ^a   de Curtis, Marco ^a  

^a DEPARTMENT OF NEUROSURGERY   (Italy)

^b POLITECNICO DI MILANO   (Italy)

Author keywords

Apparent diffusion coefficient; Cerebral ischemia; Guinea pig; Ischemic depression; Magnetic resonance imaging; Neurophysiology; Transient focal brain ischemia

Indexed keywords

ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN ISCHEMIA; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; EVOKED RESPONSE; FEASIBILITY STUDY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GUINEA PIG; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MIDDLE CEREBRAL ARTERY OCCLUSION; MORPHOLOGY; NERVE CELL MEMBRANE STEADY POTENTIAL; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; TISSUE INJURY;

ANIMALS; BRAIN; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGY; EVOKED POTENTIALS; GUINEA PIGS; INFARCTION, MIDDLE CEREBRAL ARTERY; MAGNETIC RESONANCE IMAGING; MICROTUBULE-ASSOCIATED PROTEINS; OXYGEN;

EID: 77953807900     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2010.04.005     Document Type: Article

References (56)

1. Astrup J., Symon L., Branston N.M., Lassen N. Thresholds of cerebral ischemia. Microsurgery for Stroke 1976, 16-21. Springer, Berlin. P. Schmiedek (Ed.).
2. Back T., Hemmen T., Schuler O.G. Lesion evolution in cerebral ischemia. J. Neurol. 2004, 251:388-397.
3. Biella G., de Curtis M. Associative synaptic potentials in the piriform cortex of the in vitro isolated guinea pig brain. Eur. J. NeuroSci. 1995, 7:54-64.
4. D'Arceuil H.E., Westmorel S., de Crespigny A.J. An approach to high resolution diffusion tensor imaging in fixed primate brain. Neuroimage 2007, 35:553-565.
5. de Curtis M., Pare' D., Llinas R.R. The electrophysiology of the olfactory hippocampal system in the isolated and perfused adult mammalian brain in vitro. Hippocampus 1991, 1:341-354.
6. de Curtis M., Biella G., Buccellati C., Folco G. Simultaneous investigation of the neuronal vascular compartments in the guinea pig brain isolated in vitro. Brain Res. Protoc. 1998, 3:221-228.
7. Dereski M.O., Chopp M., Knight R.A., Rodolosi L.C., Garcia J.H. The heterogeneous temporal evolution of focal ischemic neuronal damage in the rat. Acta Neuropathol. 1993, 85:327-333.
8. Dijkhuizen R.M., Beekwilder J.P., van der Worp H.B., Berkelbach van der Sprenkel J.W., Tulleken K.A., Nicolay K. Correlation between tissue depolarizations damage in focal ischemic rat brain. Brain Res. 1999, 840:194-205.
9. Dohmen C., Sakowitz O.W., Fabricius M., Bosche B., Reithmeier T., Ernestus R.I., Brinker G., Dreier J.P., Woitzik J., Strong A.J., Graf R., C.O.S.B.I.D. Spreading depolarization occur in human ischemic stroke with high incidence. Ann. Neurol. 2008, 63:720-728.
10. Dreier J.P., Major S., Manning A., Woitzik J., Drenckhahn C., Steinbrink J., Tolias C., Oliveira-Ferreira A.I., Fabricius M., Hartings J.A., Vajkoczy P., Lauritzen M., Dirnagl U., Bohner G., Strong A.J. Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 2009, 132:1866-1881.
11. Fiehler J., Foth M., Kucinski T., Knab R., von Bezold M., Weiller C., Zeumer H., Rother J. Severe ADC decreases do not predict irreversible tissue damage in humans. Stroke 2002, 33:79-86.
12. Garcia J.H., Yoshida Y., Chen H., Li Y., Zhang Z.G., Lian J., Chen S., Chopp M. Progression from ischemic injury to infarct following middle cerebral artery occlusion in the rat. Am. J. Pathol. 1993, 142:623-635.
13. Garcia J.H., Liu K.F., Ho K.L. Neuronal necrosis after middle cerebral artery occlusion in Wistar rats progresses at different time intervals in the caudoputamen and the cortex. Stroke 1995, 26:636-642.
14. Ginsberg M.D., Pulsinelli W.A. The ischemic penumbra, injury thresholds, the therapeutic window for acute stroke. Ann. Neurol. 1994, 36:553-554.
15. Ginsberg M.D. Adventures in the pathophysiology of brain ischemia: penumbra, gene expression, neuroprotection: the 2002 Thomas Willis Lecture. Stroke 2003, 34:214-223.
16. Guerrini U., Sironi L., Tremoli E., Cimino M., Pollo B., Calvio A.M., Paoletti R., Asdente M. New insights into brain damage in stroke-prone rats: a nuclear magnetic imaging study. Stroke 2002, 33:825-830.
17. Hansen A.J. Effect of anoxia on ion distribution in the brain. Physiol. Rev. 1985, 65:101-148.
18. Hartings J.A., Rolli M.L., Lu X.C., Tortella F.C. Delayed secondary phase of peri-infarct depolarizations after focal cerebral ischemia: relation to infarct growth neuroprotection. J. Neurosci. 2003, 23:11602-11610.
19. Hossmann K.A. Viability thresholds the penumbra of focal ischemia. Ann. Neurol. 1994, 36:557-565.
20. Hossmann K.A. Periinfarct Depolarizations. Cerebrovasc Brain Metab. Rev. 1996, 8:195-208.
21. Hossmann K.A. Cerebral ischemia: models, methods outcomes. Neuropharmacology 2008, 55:257-270.
22. Huh J.W., Raghupathi R., Laurer H.L., Helfaer M.A., Saatman K.E. Transient loss of microtubule-associated protein 2 immunoreactivity after moderate brain injury in mice. J. Neurotrauma 2003, 20:975-984.
23. Kidwell C.S., Alger J.R., Saver J.L. Beyond mismatch: evolving paradigms in imaging the ischemic penumbra with multimodal magnetic resonance imaging. Stroke 2003, 34:2729-2735.
24. Leao A.P. Spreading depression on activity in the cerebral cortex. J. Neurophysiol. 1944, 7:359-390.
25. Liu K.F., Silva M.D., Meng X., Gerriets T., Helmer K.G., Fenstermacher J.D., Sotak C.H., Fisher M. Acute postischemic renormalization of the apparent diffusion coefficient of water is not associated with reversal of astrocytic swelling neuronal shrinkage in rats. Am. J. Neuroradiol. 2002, 23:180-188.
26. Librizzi L., Biella G., Cimino C., de Curtis M. Arterial supply of limbic structures in the guinea pig. J. Comp. Neurol. 1999, 411:674-682.
27. Lipton P. Ischemic cell death in brain neurons. Physiol. Rev. 1999, 79:1431-1568.
28. Llinas R., Yarom Y., Sugimori M. Isolated mammalian brain in vitro: new technique for analysis of electrical activity of neuronal circuit function. Fed. Proc. 1981, 40:2240-2245.
29. Luparello T.J. Stereotaxic Atlas of the Forebrain of the Guinea Pig 1967, 80. Williams & Wilkins, Baltimore.
30. Martins-Ferreira H., Nedergaard M., Nicholson C. Perspectives on spreading depression. Brain Res. Rev. 2000, 32:215-234.
31. Mies G., Ishimaru S., Xie Y., Seo K., Hossmann K. A Ischemic thresholds of cerebral protein synthesis and energy state following middle cerebral artery occlusion in rat. J Cereb. Blood Flow Metab. 1991, 11:753-761.
32. Mies G., Kohno K., Hossmann K.A. Prevention of periinfarct direct current shifts with glutamate antagonist NBQX following occlusion of the middle cerebral artery in the rat. J. Cereb. Blood Flow Metab. 1994, 14:802-807.
33. Minematsu K., Li L., Sotak C.H., Davis M.A., Fisher M. Reversible focal ischemic injury demonstrated by diffusion-weighted magnetic resonance imaging in rats. Stroke 1992, 23:1304-1310.
34. Moseley M.E., de Crespigny A., Spielman D.M. Magnetic resonance imaging of human brain function. Surg. Neurol. 1996, 45:385-391.
35. Muhlethaler M., de Curtis M., Walton K., Llinas R. The isolated perfused brain of the guinea-pig in vitro. Eur. J. NeuroSci. 1993, 5:915-926.
36. Nallet H., MacKenzie E.T., Roussel S. The nature of penumbral depolarizations following focal cerebral ischemia in the rat. Brain Res. 1999, 842:148-158.
37. Nedergaard M., Hansen A.J. Characterization of cortical depolarizations evoked in focal cerebral ischemia. J. Cereb. Blood Flow Metab. 1993, 13:568-574.
38. Neumann-Haefelin T., Kastrup A., de Crespigny A., Yenari M.A., Ringer T., Sun G.H., Moseley M.E. Serial MRI after transient focal cerebral ischemia in rats: dynamics of tissue injury, blood-brain barrier damage, edema formation. Stroke 2000, 31:1965-1972.
39. Neumann-Haefelin T., Wittsack H.J., Wenserski F., Siebler M., Seitz R., Moder U., Freund H.J. Diffusion perfusion weighted MRI The DWI/PWI mismatch region in acute stroke. Stroke 1999, 30:1591-1597.
40. Oppenheim C., Stanescu R., Dormont D., Crozier S., Marro B., Samson Y., Rancurel G., Marsault C. False-negative diffusion-weighted MR findings in acute ischemic stroke. Am. J. Neuroradiol. 2000, 21:1434-1440.
41. Paschen W., Mies G., Hossmann K.-A. Threshold relationship between cerebral blood flow, glucose utilization, energy metabolites during development of stroke in gerbils. Exp. Neurol. 1992, 117:325-333.
42. Pastori C., Regondi M.C., Librizzi L., de Curtis M. Early excitability changes in a novel acute model of transient focal ischemia-reperfusion in the in vitro isolated guinea pig brain. Exp. Neurol. 2007, 204:95-105.
43. Pastori C., Librizzi L., Breschi G.L., Regondi C., Frassoni C., Panzica F., Frigerio S., Gelati M., Parati E., De Simoni M.G., de Curtis M. Arterially perfused neurosphere-derived cells distribute outside the ischemic core in a model of transient focal ischemia and reperfusion in vitro. Plos One 2008, 3:e2754.
44. Pettigrew L.C., Holtz M.L., Craddock S.D., Minger S.L., Hall N., Geddes J.W. Microtubular proteolysis in focal cerebral ischemia. J. Cereb. Blood Flow Metab. 1996, 16:1189-1202.
45. Pierpaoli C., Righini A., Linfante I., Tao-Cheng J.H., Alger J.R., Di Chiro G. Histopathologic correlates of abnormal water diffusion in cerebral ischemia: diffusion-weighted MR imaging light electron microscopic study. Radiology 1993, 189:439-448.
46. Rother J., de Crespigny A.J., D'Arceuil H., Mosley M.E. MR detection of cortical spreading depression immediately after focal ischemia in the rat. J. Cereb. Blood Flow Metab. 1996, 16:214-220.
47. Sakatani K., Iizuka H., Young W. Somatosensory evoked potentials in rat cerebral cortex before after middle cerebral artery occlusion. Stroke 1990, 21:124-132.
48. Somjen G. Ions in the Brain 2004, Oxford University Press.
49. Sotak C.H. Nuclear magnetic resonance (NMR) measurement of the apparent diffusion coefficient (ADC) of tissue water its relationship to cell volume changes in pathological states. Neurochem. Int. 2004, 45:569-582.
50. Strong A.J., Fabricius M., Boutelle M.G., Hibbins S.J., Hopwood S.E., Jones R., Parkin M.C., Lauritzen M. Spreading synchronous depressions of cortical activity in acutely injured human brain. Stroke 2002, 33:2738-2743.
51. Strong A.J., Dardis R. Depolarisation phenomena in traumatic ischaemic brain injury. Adv. Tech. Stand. Neurosurg. 2005, 30:3-49.
52. Sun S.W., Neil J.J., Liang H.F., He Y.Y., Schmidt R.E., Hsu C.Y., Song S.K. Formalin fixation alters water diffusion coefficient magnitude but not anisotropy in infarcted brain. Magn. Reson. Med. 2005, 53:1447-1451.
53. Symon L., Branston N.M., Strong A.J., Hope T.D. The concepts of thresholds of ischaemia in relation to brain structure and function. J. Clin. Pathol. Suppl. 1977, 11:149-154.
54. Umegaki M., Sanada Y., Waerzeggers Y., Rosner G., Yoshimine T., Heiss W.D., Graf R. Peri-infarct depolarizations reveal penumbra-like conditions in striatum. J. Neurosci. 2005, 25:1387-1394.
55. Windmuller O., Lindauer U., Foddis M., Einhaupl K.M., Dirnagl U., Heinemann U., Dreier J.P. Ion changes in spreading ischaemia induce rat middle cerebral artery constriction in the absence of NO. Brain 2005, 128:2042-2051.
56. Zucca I., Mastropietro A., Breschi G.L., Cattalini A., Bruzzone M., Spreafico R., de Curtis M. High field MRI on isolated ischemic brain model: comparison of MRI parameters at different time in paraformaldehyde role of diffusion imaging in the evaluation of brain injury in-vitro. Abstract Eur. Soc. Mag. Res. Med. Biol. Congress, Antalia, Turkey 2009.