In vivo glutamate decline associated with kainic acid-induced status epilepticus

Brain Research

Volumn 1300, Issue , 2009, Pages 65-78

  Zahr, Natalie M ^a,b   Crawford, Elena L Fasano ^c   Hsu, Oliver ^a,b   Vinco, Shara ^b   Mayer, Dirk ^b,d   Rohlfing, Torsten ^b   Sullivan, Edith V ^a   Pfefferbaum, Adolf ^b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SRI INTERNATIONAL   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Cerebellum; Glutamate; Hippocampus; Longitudinal; Rat; Status epilepticus

Indexed keywords

CASPASE 3; GLUTAMIC ACID; KAINIC ACID; LACTIC ACID; N ACETYLASPARTIC ACID; ASPARTIC ACID; DRUG DERIVATIVE; N-ACETYLASPARTATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN EDEMA; CELL LOSS; COMPUTED TOMOGRAPHY SCANNER; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; EPILEPTIC STATE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LIMBIC CORTEX; LONGITUDINAL STUDY; MALE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; RAT; SEIZURE; ANALYSIS OF VARIANCE; ANIMAL; CHEMICALLY INDUCED DISORDER; DISEASE COURSE; IMAGE PROCESSING; METABOLISM; NERVE CELL; ORGAN SIZE; PATHOLOGY; TIME; WISTAR RAT;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

ANALYSIS OF VARIANCE; ANIMALS; ASPARTIC ACID; DISEASE PROGRESSION; GLUTAMIC ACID; HIPPOCAMPUS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; KAINIC ACID; LACTIC ACID; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NEURONS; ORGAN SIZE; RATS; RATS, WISTAR; SEIZURES; STATUS EPILEPTICUS; TIME FACTORS;

EID: 73949089024     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.08.060     Document Type: Article

References (75)

1. Adalsteinsson E., Sullivan E.V., and Pfefferbaum A. Biochemical, functional and microstructural magnetic resonance imaging (MRI). In: Liu Y., and Lovinger D.M. (Eds). Methods in Alcohol-Related Neuroscience Research. Vol. (2002), CRC Press, Boca Raton, FL 345-372
2. Adalsteinsson E., Hurd R.E., Mayer D., Sailasuta N., Sullivan E.V., and Pfefferbaum A. In vivo 2D J-resolved magnetic resonance spectroscopy of rat brain with a 3-T clinical human scanner. NeuroImage 22 (2004) 381-386
3. Alvestad S., Hammer J., Eyjolfsson E., Qu H., Ottersen O.P., and Sonnewald U. Limbic structures show altered glial-neuronal metabolism in the chronic phase of kainate induced epilepsy. Neurochem. Res. 33 (2008) 257-266
4. Bates J.F., Peake L., Swearengen E.S., Hall T.W., and Standish L.J. CL 218-872 pretreatment and intervention block kainate-induced convulsions and neuropathology. Behav. Neurosci. 102 (1988) 84-92
5. Ben-Ari Y., Tremblay E., Riche D., Ghilini G., and Naquet R. Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 6 (1981) 1361-1391
6. Bouilleret V., Nehlig A., Marescaux C., and Namer I.J. Magnetic resonance imaging follow-up of progressive hippocampal changes in a mouse model of mesial temporal lobe epilepsy. Epilepsia 41 (2000) 642-650
7. Camara O., Schnabel J.A., Ridgway G.R., Crum W.R., Douiri A., Scahill R.I., Hill D.L., and Fox N.C. Accuracy assessment of global and local atrophy measurement techniques with realistic simulated longitudinal Alzheimer's disease images. NeuroImage 42 (2008) 696-709
8. Carlson H., Ronne-Engstrom E., Ungerstedt U., and Hillered L. Seizure related elevations of extracellular amino acids in human focal epilepsy. Neurosci Lett 140 (1992) 30-32
9. Chronik B., Alejski A., and Rutt B.K. Design and fabrication of a three-axis multilayer gradient coil for magnetic resonance microscopy of mice. Magma 10 (2000) 131-146
10. Chronik B., Alejski A., and Rutt B.K. Design and fabrication of a three-axis multilayer gradient coil for magnetic resonance microscopy of mice. Magma 10 (2000) 131-146
11. Dice L. Measures of the amount of ecologic association between species. Ecology 26 (1945) 297-302
12. Dreher W., and Leibfritz D. Detection of homonuclear decoupled in vivo proton NMR spectra using constant time chemical shift encoding: CT-PRESS. Magn. Reson. Imaging 17 (1999) 141-150
13. During M.J., and Spencer D.D. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341 (1993) 1607-1610
14. 1H magnetic resonance spectroscopic imaging. J. Cereb. Blood Flow Metab. 14 (1994) 373-382
15. Ebisu T., Rooney W.D., Graham S.H., Mancuso A., Weiner M.W., and Maudsley A.A. MR spectroscopic imaging and diffusion-weighted MRI for early detection of kainate-induced status epilepticus in the rat. Magn. Reson. Med. 36 (1996) 821-828
16. Faherty C.J., Xanthoudakis S., and Smeyne R.J. Caspase-3-dependent neuronal death in the hippocampus following kainic acid treatment. Brain Res. Mol. Brain Res. 70 (1999) 159-163
17. Ferkany J.W., Zaczek R., and Coyle J.T. Kainic acid stimulates excitatory amino acid neurotransmitter release at presynaptic receptors. Nature 298 (1982) 757-759
18. Govindaraju V., Young K., and Maudsley A.A. Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed. 13 (2000) 129-153
19. Hantraye P., Leroy-Willig A., Denys A., Riche D., Isacson O., Maziere M., and Syrota A. Magnetic resonance imaging to monitor pathology of caudate-putamen after excitotoxin-induced neuronal loss in the nonhuman primate brain. Exp. Neurol. 118 (1992) 18-23
20. Hellier J.L., and Dudek F.E. Chemoconvulsant model of chronic spontaneous seizures. In: Skolnick P. (Ed). Short Protocols in Neuroscience: Systems and Behavioral Method Vol (2006), John Wiley and Sons Ltd
21. Hellier J.L., Patrylo P.R., Buckmaster P.S., and Dudek F.E. Recurrent spontaneous motor seizures after repeated low-dose systemic treatment with kainate: assessment of a rat model of temporal lobe epilepsy. Epilepsy Res. 31 (1998) 73-84
22. Kondratyev A., and Gale K. Intracerebral injection of caspase-3 inhibitor prevents neuronal apoptosis after kainic acid-evoked status epilepticus. Brain Res. Mol. Brain Res. 75 (2000) 216-224
23. Kondratyev A., and Gale K. Latency to onset of status epilepticus determines molecular mechanisms of seizure-induced cell death. Brain Res. Mol. Brain Res. 121 (2004) 86-94
24. Koyama I. Amino acids in the cobalt-induced epileptogenic and nonepileptogenic cat's cortex. Can. J. Physiol. Pharmacol. 50 (1972) 740-752
25. Kramer R.E., Luders H., Lesser R.P., Weinstein M.R., Dinner D.S., Morris H.H., and Wyllie E. Transient focal abnormalities of neuroimaging studies during focal status epilepticus. Epilepsia 28 (1987) 528-532
26. Lassmann H., Petsche U., Kitz K., Baran H., Sperk G., Seitelberger F., and Hornykiewicz O. The role of brain edema in epileptic brain damage induced by systemic kainic acid injection. Neuroscience 13 (1984) 691-704
27. Liu Z., Stafstrom C.E., Sarkisian M.R., Yang Y., Hori A., Tandon P., and Holmes G.L. Seizure-induced glutamate release in mature and immature animals: an in vivo microdialysis study. NeuroReport 8 (1997) 2019-2023
28. Lothman E.W., and Collins R.C. Kainic acid induced limbic seizures: metabolic, behavioral, electroencephalographic and neuropathological correlates. Brain Res. 218 (1981) 299-318
29. Luna-Medina R., Cortes-Canteli M., Sanchez-Galiano S., Morales-Garcia J.A., Martinez A., Santos A., and Perez-Castillo A. NP031112, a thiadiazolidinone compound, prevents inflammation and neurodegeneration under excitotoxic conditions: potential therapeutic role in brain disorders. J. Neurosci. 27 (2007) 5766-5776
30. Magloczky Z., and Freund T.F. Selective neuronal death in the contralateral hippocampus following unilateral kainate injections into the CA3 subfield. Neuroscience 56 (1993) 317-335
31. Mao H., Toufexis D., Wang X., Lacreuse A., and Wu S. Changes of metabolite profile in kainic acid induced hippocampal injury in rats measured by HRMAS NMR. Exp. Brain Res. 183 (2007) 477-485
32. Mayer D., and Spielman D.M. Detection of glutamate in the human brain at 3 T using optimized constant time point resolved spectroscopy. Magn. Reson. Med. 54 (2005) 439-442
33. Mayer D., Zahr N.M., Sullivan E.V., and Pfefferbaum A. In vivo metabolite differences between the basal ganglia and cerebellum of the rat brain detected with proton MRS at 3T. Psychiatry Res 154 (2007) 267-273
34. Meldrum B.S. Excitotoxicity and selective neuronal loss in epilepsy. Brain Pathol. 3 (1993) 405-412
35. Meric P., Barrere B., Peres M., Gillet B., Berenger G., Beloeil J.C., and Seylaz J. Effects of kainate-induced seizures on cerebral metabolism: a combined H-1 and P-31 NMR study in rat. Brain Res. 638 (1994) 53-60
36. Moffett J.R., Ross B., Arun P., Madhavarao C.N., and Namboodiri A.M. N-Acetylaspartate in the CNS: from neurodiagnostics to neurobiology. Prog. Neurobiol. 81 (2007) 89-131
37. Nadler J.V., and Cuthbertson G.J. Kainic acid neurotoxicity toward hippocampal formation: dependence on specific excitatory pathways. Brain Res. 195 (1980) 47-56
38. Najm I.M., Wang Y., Hong S.C., Luders H.O., Ng T.C., and Comair Y.G. Temporal changes in proton MRS metabolites after kainic acid-induced seizures in rat brain. Epilepsia 38 (1997) 87-94
39. Najm I.M., Wang Y., Shedid D., Luders H.O., Ng T.C., and Comair Y.G. MRS metabolic markers of seizures and seizure-induced neuronal damage. Epilepsia 39 (1998) 244-250
40. Nixon K. Alcohol and adult neurogenesis: roles in neurodegeneration and recovery in chronic alcoholism. Hippocampus 16 (2006) 287-295
41. Norman A.B., Thomas S.R., Pratt R.G., Samaratunga R.C., and Sanberg P.R. T1 and T2 weighted magnetic resonance imaging of excitotoxin lesions and neural transplants in rat brain in vivo. Exp. Neurol. 109 (1990) 164-170
42. O'Shaughnessy D., and Gerber G.J. Damage induced by systemic kainic acid in rats is dependent upon seizure activity-a behavioral and morphological study. Neurotoxicology 7 (1986) 187-202
43. Olney J.W., Collins R.C., and Sloviter R.S. Excitotoxic mechanisms of epileptic brain damage. Adv. Neurol. 44 (1986) 857-877
44. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates, Vol. (2005), Elsevier Academic Press, London
45. 1H magnetic resonance spectroscopy of extracts of human epileptic neocortex and hippocampus. Neurology 43 (1993) 589-594
46. Petroff O.A., Errante L.D., Rothman D.L., Kim J.H., and Spencer D.D. Glutamate-glutamine cycling in the epileptic human hippocampus. Epilepsia 43 (2002) 703-710
47. Pfefferbaum A., Adalsteinsson E., and Sullivan E.V. In vivo structural imaging of the rat brain with a 3-T clinical human scanner. J. Magn. Reson. Imaging 20 (2004) 779-785
48. Pfefferbaum A., Sullivan E.V., and Carmelli D. Morphological changes in aging brain structures are differentially affected by time-linked environmental influences despite strong genetic stability. Neurobiol. Aging 25 (2004) 175-183
49. Pfefferbaum A., Zahr N.M., Mayer D., Vinco S., Orduna J., Rohlfing T., and Sullivan E.V. Ventricular expansion in wild-type Wistar rats after alcohol exposure by vapor chamber. Alcoholism, Clin. Exp. Res. 32 (2008) 1459-1467
50. Plock N., and Kloft C. Microdialysis-theoretical background and recent implementation in applied life-sciences. Eur. J. Pharm. Sci. 25 (2005) 1-24
51. Puig B., and Ferrer I. Caspase-3-associated apoptotic cell death in excitotoxic necrosis of the entorhinal cortex following intraperitoneal injection of kainic acid in the rat. Neurosci. Lett. 321 (2002) 182-186
52. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32 (1972) 281-294
53. Retz K.C., and Coyle J.T. Effects of kainic acid on high-energy metabolites in the mouse striatum. J. Neurochem. 38 (1982) 196-203
54. Righini A., Pierpaoli C., Alger J.R., and Di Chiro G. Brain parenchyma apparent diffusion coefficient alterations associated with experimental complex partial status epilepticus. Magn. Reson. Imaging 12 (1994) 865-871
55. Rohlfing T., and Maurer Jr. C.R. Nonrigid image registration in shared-memory multiprocessor environments with application to brains, breasts, and bees. IEEE Trans. Inf. Technol. Biomed. 7 (2003) 16-25
56. Rohlfing T., Brandt R., Menzel R., and Maurer Jr. C.R. Evaluation of atlas selection strategies for atlas-based image segmentation with application to confocal microscopy images of bee brains. NeuroImage 21 (2004) 1428-1442
57. Rohlfing T., Sullivan E.V., and Pfefferbaum A. Deformation-based brain morphometry to track the course of alcoholism: differences between intra-subject and inter-subject analysis. Psychiatry Res.: NeuroImaging 146 (2006) 157-170
58. Rohlfing T., Zahr N.M., Sullivan E.V., and Pfefferbaum A. The SRI24 multi-channel brain atlas: construction and applications. Medical Imaging 2008: Image Processing. Proc. SPIE (2008) 6914, EID 691409 (12 pages)
59. Roland J.J., and Savage L.M. Blunted hippocampal, but not striatal, acetylcholine efflux parallels learning impairment in diencephalic-lesioned rats. Neurobiol. Learn. Mem. 87 (2007) 123-132
60. Sagar H.J., and Oxbury J.M. Hippocampal neuron loss in temporal lobe epilepsy: correlation with early childhood convulsions. Ann. Neurol. 22 (1987) 334-340
61. Schwob J.E., Fuller T., Price J.L., and Olney J.W. Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience 5 (1980) 991-1014
62. Sierra-Paredes G., Galan-Valiente J., Vazquez-Illanes M.D., Aguilar-Veiga E., Soto-Otero R., Mendez-Alvarez E., and Sierra-Marcuno G. Extracellular amino acids in the rat hippocampus during picrotoxin threshold seizures in chronic microdialysis experiments. Neurosci. Lett. 248 (1998) 53-56
63. Sperk G. Kainic acid seizures in the rat. Prog. Neurobiol. 42 (1994) 1-32
64. Sperk G., Lassmann H., Baran H., Kish S.J., Seitelberger F., and Hornykiewicz O. Kainic acid induced seizures: neurochemical and histopathological changes. Neuroscience 10 (1983) 1301-1315
65. Stone J.L., Hughes J.R., Barr A., Tan W., Russell E., and Crowell R.M. Neuroradiological and electroencephalographic features in a case of temporal lobe status epilepticus. Neurosurgery 18 (1986) 212-216
66. Tanaka S., Tanaka T., Kondo S., Hori T., Fukuda H., Yonemasu Y., Tanaka M., and Shindo K. Magnetic resonance imaging in kainic acid-induced limbic seizure status in cats. Neurol. Med. Chir. (Tokyo) 33 (1993) 285-289
67. Tanaka K., Graham S.H., and Simon R.P. The role of excitatory neurotransmitters in seizure-induced neuronal injury in rats. Brain Res. 737 (1996) 59-63
68. Tokuhara D., Sakuma S., Hattori H., Matsuoka O., and Yamano T. Kainic acid dose affects delayed cell death mechanism after status epilepticus. Brain Dev. 29 (2007) 2-8
69. Tokumitsu T., Mancuso A., Weinstein P.R., Weiner M.W., Naruse S., and Maudsley A.A. Metabolic and pathological effects of temporal lobe epilepsy in rat brain detected by proton spectroscopy and imaging. Brain Res. 744 (1997) 57-67
70. Wade J.V., Samson F.E., Nelson S.R., and Pazdernik T.L. Changes in extracellular amino acids during soman- and kainic acid-induced seizures. J. Neurochem. 49 (1987) 645-650
71. Williams P.A., Hellier J.L., White A.M., Staley K.J., and Dudek F.E. Development of spontaneous seizures after experimental status epilepticus: implications for understanding epileptogenesis. Epilepsia 48 Suppl 5 (2007) 157-163
72. Wilson C.L., Maidment N.T., Shomer M.H., Behnke E.J., Ackerson L., Fried I., and Engel Jr. J. Comparison of seizure related amino acid release in human epileptic hippocampus versus a chronic, kainate rat model of hippocampal epilepsy. Epilepsy Res. 26 (1996) 245-254
73. Wolf O.T., Dyakin V., Patel A., Vadasz C., de Leon M.J., McEwen B.S., and Bulloch K. Volumetric structural magnetic resonance imaging (MRI) of the rat hippocampus following kainic acid (KA) treatment. Brain Res. 934 (2002) 87-96
74. Zahr N.M., Mayer D., Hsu O., Vinco S., Orduna J., Sullivan E.V., and Pfefferbaum A. In vivo neurochemical evidence for alcohol binge induced neural compromise and recovery in alcohol-preferring rats. Research Society on Alcoholism (2009) San Diego, CA
75. Zhang W.Q., Hudson P.M., Sobotka T.J., Hong J.S., and Tilson H.A. Extracellular concentrations of amino acid transmitters in ventral hippocampus during and after the development of kindling. Brain Res. 540 (1991) 315-318