Symbiosis between in vivo and in vitro NMR spectroscopy: The creatine, N-acetylaspartate, glutamate, and GABA content of the epileptic human brain

Behar, 1983, High-resolution 1H nuclear magnetic resonance study of cerebral hypoxia in vivo, 80, 4945 Behar, 1991, Assignment of resonances in the 1H spectrum of rat brain by two-dimensional shift correlated and J-resolved NMR spectroscopy, Magn. Reson. Med., 17, 285, 10.1002/mrm.1910170202 Behar, 1993, Characterization of macromolecule resonances in the 1H NMR spectrum of rat brain, Magn. Reson. Med., 30, 38, 10.1002/mrm.1910300107 Behar, 1993, Characterization of macromolecule resonances in the 1H NMR spectrum of rat brain, Magn. Reson. Med., 30, 44, 10.1002/mrm.1910300107 Behar, 1994, Analysis of macromolecule resonances in 1H NMR spectra of human brain, Magn. Reson. Med., 32, 294, 10.1002/mrm.1910320304 Graham, 1994, Spectroscopic assessment of alterations in lipid and small molecule metabolites in human brain after stroke, 187 Petroff, 1994, Metabolite and macromolecule changes within the MS plaque measured in vivo with serial 1H NMR spectroscopy, 586 Chang, 1994, In vivo 1H MRS and in vitro biochemical correlation of heterogeneous brain tumors, 1295 Petroff, 1989, High-field proton magnetic resonance spectroscopy of human cerebrum obtained during surgery for epilepsy, Neurology, 39, 1197, 10.1212/WNL.39.9.1197 Graham, 1993, Proton magnetic resonance spectroscopy in Creutzfeld-Jakob disease, Neurology, 43, 2065, 10.1212/WNL.43.10.2065 Matthews, 1990, A proton magnetic resonance spectroscopic study of focal epilepsy in humans, Neurology, 40, 985, 10.1212/WNL.40.6.985 Hugg, 1992, Lateralization of human focal epilepsy by 31P magnetic resonance spectroscopic imaging, Neurology, 42, 2011, 10.1212/WNL.42.10.2011 Hugg, 1993, Neuron loss localizes human temporal lobe epilepsy by in vivo proton magnetic resonance spectroscopic imaging, Ann. Neurol., 34, 788, 10.1002/ana.410340606 Kuzniecky, 1992, In vivo 31P nuclear magnetic resonance spectroscopy of human temporal lobe epilepsy, Neurology, 42, 1586, 10.1212/WNL.42.8.1586 Cendes, 1994, Lateralization of temporal lobe epilepsy based on regional metabolic abnormalities in proton magnetic resonance spectroscopic images, Ann. Neurol., 35, 211, 10.1002/ana.410350213 Garcia, 1994, Phosphorus magnetic resonance spectroscopic imaging in patients with frontal lobe epilepsy, Ann. Neurol., 35, 217, 10.1002/ana.410350214 Jackson, 1994, Functional magnetic resonance imaging of focal seizures, Neurology, 44, 850, 10.1212/WNL.44.5.850 Connelly, 1994, Magnetic resonance spectroscopy in temporal lobe epilepsy, Neurology, 44, 1411, 10.1212/WNL.44.8.1411 Kuzniecky, 1995 Rothman, 1993, Localized 1H NMR measurements of GABA levels in human brain in vivo, 90, 5662 Mattson, 1994, Vigabatrin: Effects on human brain GABA levels by nuclear magnetic resonance spectroscopy, Epilepsia, 53, S29, 10.1111/j.1528-1157.1994.tb05963.x Rothman, 1992, Localized 1H NMR measurements of glutamate in the human brain, Magn. Reson. Med., 25, 94, 10.1002/mrm.1910250110 Petroff, 1994, In vivo GABA, glutamate, and glutamine concentrations of human brain, J. Neurochem., 62, S97 Petroff, 1995, Initial observations on the effect of vigabatrin on the in vivo 1H spectroscopic measurements of GABA, glutamate, and glutamine in human brain, Epilepsia, 36, 457, 10.1111/j.1528-1157.1995.tb00486.x Petroff, 1992, Spectroscopic imaging of stroke in man: Histopathology correlates of spectral changes, Neurology, 42, 1349, 10.1212/WNL.42.7.1349 Spencer, 1985, Surgery for epilepsy, Neurol. Clin., 3, 313, 10.1016/S0733-8619(18)31039-9 Spencer, 1986, Surgical options for uncontrolled epilepsy, Neurol. Clin., 4, 669, 10.1016/S0733-8619(18)30969-1 Gray, 1962, The isolation of nerve endings from brain; An electron microscopic study of the cell fragments derived by homogenization and centrifugation, J. Anat. (London), 96, 79 Whittaker, 1984, The synaptosome, 1 Petroff, 1991, Metabolism of 1-13C-glucose in a synaptosomally enriched fraction of rat cerebrum studied by 1H/13C magnetic resonance spectroscopy, Neurochem. Res., 16, 1245, 10.1007/BF00966703 Farooq, 1978, A modified procedure for isolation of astrocyte- and neuron-enriched fractions from rat brain, J. Neurochem., 31, 887, 10.1111/j.1471-4159.1978.tb00124.x Petroff, 1993, Metabolic assessment of a neuron enriched fraction of rat cerebrum using high-resolution 1H and 13C NMR spectroscopy, Magn. Reson. Med., 30, 1, 10.1002/mrm.1910300506 Petroff, 1988, High-resolution proton magnetic resonance spectroscopy of rabbit brain: Regional metabolite levels and postmortem changes, J. Neurochem., 51, 163, 10.1111/j.1471-4159.1988.tb04850.x Petroff, 1990, In vivo measurements of ethanol concentration in rabbit brain by 1H magnetic resonance spectroscopy, J. Neurochem., 54, 1188, 10.1111/j.1471-4159.1990.tb01947.x Dagani, 1987, Relationships among ATP synthesis, K+ gradients, and neurotransmitter amino acid levels in isolated rat brain synaptosomes, J. Neurochem., 49, 1229, 10.1111/j.1471-4159.1987.tb10015.x Urenjak, 1992, Specific expression of N-acetylaspartate in neurons, oligodendrocytes-type-2 astrocyte progenitors, and immature oligodendrocytes in vitro, J. Neurochem., 59, 55, 10.1111/j.1471-4159.1992.tb08875.x Urenjak, 1993, Proton nuclear magnetic resonance spectroscopy unambiguously identifies different neural cell types, J. Neurosci., 13, 981, 10.1523/JNEUROSCI.13-03-00981.1993 Petroff, 1992, Quantitative analysis of rat synaptosomes and cerebrum using high resolution 1H magnetic resonance spectroscopy, Clin. Chim. Acta, 206, 137, 10.1016/0009-8981(92)90014-H Harding, 1924, The creatine content of brain, J. Biol. Chem., 60, 301, 10.1016/S0021-9258(18)85209-7 Avison, 1990, Proton NMR observation of phenylalanine and an aromatic metabolite in the rabbit brain in vivo, Pediatr. Res., 27, 566, 10.1203/00006450-199006000-00005 Swanson, 1992, Physiological coupling of glial glycogen metabolism to neuronal activity in brain, Can. J. Physiol. Pharmacol., 70, S138, 10.1139/y92-255 Young, 1987, In vivo 31P and in vitro 1H nuclear magnetic resonance study of hypoglycemia during neonatal seizure, Ann. Neurol., 22, 622, 10.1002/ana.410220511 Petroff, 1986, High-resolution proton magnetic resonance analysis of human cerebrospinal fluid, J. Neurochem., 47, 1270, 10.1111/j.1471-4159.1986.tb00750.x Sappey-Marinier, 1985, Perspectives d'emploi de la RMN pour l'etude biochimique de la substance blanche cerebrale, Arch. Int. Physiol. Biochim., 93, 129 Sappey-Marinier, 1990, High-resolution NMR spectroscopy of cerebral white matter in multiple sclerosis, Magn. Reson. Med., 15, 229, 10.1002/mrm.1910150206 Remy, 1994, In vivo, ex vivo, and in vitro one- and two-dimensional nuclear magnetic resonance spectroscopy of an intracerebral glioma in rat brain: Assignment of resonances, J. Neurochem., 62, 166, 10.1046/j.1471-4159.1994.62010166.x Kauppinen, 1993, Quantitative analysis of 1H NMR detected proteins in the rat cerebral cortex in vivo and in vitro, NMR Biomed., 6, 242, 10.1002/nbm.1940060403 Behar, 1985, The effect of hypoglycemic encephalopathy upon amino acids, high energy phosphates, and pHi in the rat brain in vivo: Detection by sequential 1H and 31P NMR spectroscopy, J. Neurochem., 44, 1045, 10.1111/j.1471-4159.1985.tb08723.x Gill, 1989, Brain metabolites as 1H NMR markers of neuronal and glial disorders, NMR Biomed., 2, 196, 10.1002/nbm.1940020505 Young, 1991, Brain energy state and lactate metabolism during status epilepticus in the neonatal dog: In vivo 31P and 1H NMR study, Pediatr. Res., 29, 191, 10.1203/00006450-199102000-00018 Huppi, 1991, Magnetic resonance in preterm and term newborns: 1H-spectroscopy in developing human brain, Pediatr. Res., 30, 574, 10.1203/00006450-199112000-00017 Connett, 1988, Analysis of metabolic control: new insights using scaled creatine kinase model, Am. J. Physiol., 254, R949 Heilig, 1989, Characterization of the major brain osmolytes that accumulate in salt loaded rats, Am. J. Physiol., 257, F1108 Lee, 1994, Brief report: Organic osmolytes in the brain of an infant with hypernatremia, N. Engl. J. Med., 331, 439, 10.1056/NEJM199408183310704 Defalco, 1961, The synthesis of creatine by the brain of the intact rat, J. Neurochem., 7, 308, 10.1111/j.1471-4159.1961.tb13518.x Manos, 1991, Creatine kinase activity in postnatal rat brain development and in cultured neurons, astrocytes, and oligodendrocytes, J. Neurochem., 56, 2101, 10.1111/j.1471-4159.1991.tb03472.x Lowry, 1977, Diversity of metabolic patterns in human brain tumorsand — I. High energy phosphate compounds and basic composition, J. Neurochem., 29, 959, 10.1111/j.1471-4159.1977.tb06500.x Gill, 1990, Proton MR spectroscopy of intracranial tumours: In vivo and in vitro studies, J. Comput. Assist. Tomogr., 14, 497, 10.1097/00004728-199007000-00001 Peeling, 1992, High-resolution 1H NMR spectroscopic studies of extracts of human cerebral neoplasms, Magn. Reson. Med., 24, 123, 10.1002/mrm.1910240113 Peeling, 1993, 1H magnetic resonance spectroscopy of extracts of human epileptic neocortex and hippocampus, Neurology, 43, 589, 10.1212/WNL.43.3_Part_1.589 Gruetter, 1994, Localized 13C NMR spectroscopy in the human brain of amino acid labeling from 13C glucose, J. Neurochem., 63, 1377, 10.1046/j.1471-4159.1994.63041377.x Michelis, 1993, Absolute concentrations of metabolites in adult human brain in vivo: Quantification of localized proton MR spectra, Radiology, 187, 219, 10.1148/radiology.187.1.8451417 Kreis, 1993, Absolute quantitation of water and metabolites in the human brain. II. Metabolite concentrations, J. Magn. Reson. Series B, 102, 9, 10.1006/jmrb.1993.1056 Hetherington, 1994, Evaluation of cerebral gray and white matter metabolite differences by spectroscopic imaging at 4.1 T, Magn. Reson. Med., 32, 565, 10.1002/mrm.1910320504 Alger, 1993, Absolute quantitation of short TE brain 1H-MR spectra and spectroscopic imaging data, J. Comput. Assist. Tomogr., 17, 191, 10.1097/00004728-199303000-00006 Narayana, 1989, Regional in vivo proton magnetic resonance spectroscopy of brain, J. Magn. Reson., 83, 44 Baldwin, 1994, The fornix in patients with seizures caused by unilateral hippocampal sclerosis: Detection of unilateral volume loss on MR images, Am. J. Radiol., 162, 1185 Kuhn, 1989, Wallerian degeneration after cerebral infarction: Evaluation with sequential MR imaging, Radiology, 172, 179, 10.1148/radiology.172.1.2740501 Sonoda, 1992, Extent of pyramidal tract Wallerian degeneration in the brain stem on MRI and degree of motor impairment after supratentorial stroke, Disabil. Rehabil., 14, 89, 10.3109/09638289209167077 Fukui, 1994, Extent of pontine pyramidal tract Wallerian degeneration and outcome after supratentorial hemorrhagic stroke, Stroke, 25, 1207, 10.1161/01.STR.25.6.1207 Stoeckler, 1994, Creatine deficiency in the brain: A new, treatable inborn error of metabolism, Pediatr. Res., 36, 409, 10.1203/00006450-199409000-00023 Nadler, 1972, N-acetyl-l-aspartic acid content of human neural tumours and bovine peripheral nervous tissues, J. Neurochem., 19, 313, 10.1111/j.1471-4159.1972.tb01341.x Koller, 1984, N-acetyl-aspartylglutamate: Regional levels in rat brain and the effects of brain lesions as determined by a new HPLC method, J. Neurochem., 43, 1136, 10.1111/j.1471-4159.1984.tb12854.x Moffett, 1991, Immunohistochemical localization of N-acetylaspartate in rat brain, Neuroreport, 2, 131, 10.1097/00001756-199103000-00005 Moffett, 1993, Enhanced carbodiimide fixation for immunohistochemistry: Application to the comparative distributions of N-acetylaspartylglutamate and N-acetylaspartate immunoreactivities in rat brain, J. Histochem. Cytochem., 41, 559, 10.1177/41.4.8450195 Moffett, 1991, Effect of optic nerve transection on N-acetylaspartylglutamate immunoreactivity in the primary and accessory optic projection systems in the rat, Brain Res., 538, 86, 10.1016/0006-8993(91)90380-E Hanstock, 1988, Spatially localized 1H NMR spectra of metabolites in the human brain, 85, 1821 Rango, 1992, Trans-synaptic degeneration following acute axonal injury: A 1-H magnetic resonance spectroscopy study, Neurology, 42, 475 D'Arcangelo, 1990, Distribution of N-acetylaspartate, N-acetylaspartylglutamate, free glutamate and aspartate following complete mesencephalic transection in rat neuraxis, Neurosci. Lett., 114, 82, 10.1016/0304-3940(90)90432-9 Graham, 1993, Early temporal variation of cerebral metabolites after human stroke: A proton magnetic resonance spectroscopy study, Stroke, 24, 1891, 10.1161/01.STR.24.12.1891 Graham, 1993, Clinical correlates of proton magnetic resonance spectroscopy findings after acute cerebral infarction, 1483 Blamire, 1994, Proton spectroscopy of human stroke: Assessment of transverse relaxation times and partial volume effects in single volume STEAM MRS, Magn. Reson. Imaging, 12, 1227, 10.1016/0730-725X(94)90087-8 Meyerhoff, 1994, Axonal injury and membrane alterations in Alzheimer's disease suggested by in vivo proton magnetic resonance spectroscopic imaging, Ann. Neurol., 36, 40, 10.1002/ana.410360110 Fulham, 1994, Transsynaptic reduction in N-acetylaspartate in cerebellar diaschisis: A proton MR spectroscopic imaging study, J. Comput. Assist. Tomogr., 18, 697, 10.1097/00004728-199409000-00004 Arnold, 1992, Proton magnetic resonance spectroscopic imaging for metabolic characterization of demyelinating plaques, Ann. Neurol., 31, 235, 10.1002/ana.410310302 Brenner, 1993, Abnormal neuronal mitochondria: A cause of reduction in NA in demyelinating disease, 281 Patel, 1979, Synthesis of N-acetyl-l-aspartate by rat brain mitochondria and its involvement in mitochondrial/cytosolic carbon transport, Biochem. J., 184, 539, 10.1042/bj1840539 Ebisu, 1994, N-acetylaspartate as an in vivo marker of neuronal viability in kainate-induced status epilepticus: 1H magnetic resonance spectroscopic imaging, J. Cereb. Blood Flow Metab., 14, 373, 10.1038/jcbfm.1994.48 Young, 1991, Effects of glutamate, quisqualate, and N-methyl-d-aspartate in neonatal brain, Exp. Neurol., 111, 362, 10.1016/0014-4886(91)90104-K Taylor, 1994, Extracellular N-acetylaspartate in the rat brain: In vivo determination of basal levels and changes evoked by high K+, J. Neurochem., 62, 2349, 10.1046/j.1471-4159.1994.62062349.x Matalon, 1989, Aspartoacylase deficiency: The enzyme defect in Canavan's disease, J. Inherit. Metab. Dis., 12, 329 Kaul, 1991, Purification, characterization, and localization of aspartoacylase from bovine brain, J. Neurochem., 56, 129, 10.1111/j.1471-4159.1991.tb02571.x Lloyd, 1986, Altered or GABA-mediated synaptic transmission in human epilepsy, Adv. Neurol., 44, 1033 Wood, 1979, Low cerebrospinal fluid γ-aminobutyric acid content in seizure patients, Neurology, 29, 1203, 10.1212/WNL.29.9_Part_1.1203 Sherwin, 1986, Amino acid and catecholamine markers of metabolic abnormalities in human focal epilepsy, Adv. Neurol., 44, 1011 Perry, 1982, Cerebral amino acid pools, Vol. 1, 151 Hamberger, 1991, Amino acids in the neuronal microenvironment of focal human epileptic lesions, Epilepsy Res., 9, 32, 10.1016/0920-1211(91)90044-G Sherwin, 1988, Excitatory aminoacids are elevated in human epileptic cerebral cortex, Neurology, 38, 920, 10.1212/WNL.38.6.920 Perry, 1981, Postmortem changes of amino compounds in human and rat brain, J. Neurochem., 36, 406, 10.1111/j.1471-4159.1981.tb01608.x Kälviäinen, 1993, Amino acid levels in the cerebrospinal fluid of newly diagnosed epileptic patients: Effect of vigabatrin and carbamazepine monotherapies, J. Neurochem., 60, 1244, 10.1111/j.1471-4159.1993.tb03283.x During, 1993, Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain, Lancet, 341, 1607, 10.1016/0140-6736(93)90754-5 Rimvall, 1994, The level of GAD67 protein is highly sensitive to small increases in intraneuronal γ-aminobutyric acid levels, J. Neurochem., 62, 1375, 10.1046/j.1471-4159.1994.62041375.x Gruetter, 1992, Localized 13C NMR spectroscopy of myoinositol in the human brain in vivo, Magn. Reson. Med., 25, 204, 10.1002/mrm.1910250121 Narumi, 1969, Gaschromatographic analysis of free myo- and scyllo-inositols in animal tissues, Jpn. J. Exp. Med., 39, 399 Perry, 1971, Regional distribution of amino acids in human brain obtained at autopsy, J. Neurochem., 18, 513, 10.1111/j.1471-4159.1971.tb11979.x