Preclinical 1H-MRS neurochemical profiling in neurological and psychiatric disorders

Bioanalysis

Volumn 4, Issue 14, 2012, Pages 1787-1804

  Lee, Moonnoh R ^a   Denic, Aleksandar ^a   Hinton, David J ^a   Mishra, Prasanna K ^a   Choi, Doo Sup ^a   Pirko, Istvan ^a   Rodriguez, Moses ^a   MacUra, Slobodan I ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOLISM; ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; HUNTINGTON CHOREA; IMAGE ANALYSIS; IMAGE PROCESSING; IMAGE QUALITY; MAGNETIC FIELD; MENTAL DISEASE; METABOLITE; MOOD DISORDER; MULTIPLE SCLEROSIS; NEUROCHEMISTRY; NEUROIMAGING; NEUROLOGIC DISEASE; NONHUMAN; PARKINSON DISEASE; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; SCHIZOPHRENIA; SIGNAL DETECTION; SIGNAL NOISE RATIO;

ALCOHOLISM; ANIMALS; BIOLOGICAL MARKERS; BRAIN; BRAIN CHEMISTRY; DISEASE MODELS, ANIMAL; HUMANS; MAGNETIC RESONANCE IMAGING; MENTAL DISORDERS; MICE; MICE, KNOCKOUT; MOOD DISORDERS; MULTIPLE SCLEROSIS; NERVOUS SYSTEM DISEASES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; RATS;

EID: 84865039289     PISSN: 17576180     EISSN: 17576199     Source Type: Journal    
DOI: 10.4155/bio.12.129     Document Type: Review

References (146)

1. Choi JK, Kustermann E, Dedeoglu A, Jenkins BG. Magnetic resonance spectroscopy of regional brain metabolite markers in FALS mice and the effects of dietary creatine supplementation. Eur. J. Neurosci. 30(11), 2143-2150 (2009
2. Denic A, Bieber A, Warrington A, Mishra PK, Macura S, Rodriguez M. Brainstem 1H nuclear magnetic resonance (NMR) spectroscopy: marker of demyelination and repair in spinal cord. Ann. Neurol. 66(4), 559-564 (2009
3. Licata SC, Renshaw PF. Neurochemistry of drug action: Insights from proton magnetic resonance spectroscopic imaging and their relevance to addiction. Ann. NY Acad. Sci. 1187, 148-171 (2010
4. Choi JK, Dedeoglu A, Jenkins BG. Application of MRS to mouse models of neurodegenerative illness. NMR Biomed. 20(3), 216-237 (2007
5. Pirko I, Fricke ST, Johnson AJ, Rodriguez M, Macura SI. Magnetic resonance imaging, microscopy, and spectroscopy of the central nervous system in experimental animals. NeuroRx 2(2), 250-264 (2005
6. Chen J, Nam HW, Lee MR et al. Altered glutamatergic neurotransmission in the striatum regulates ethanol sensitivity and intake in mice lacking ENT1. Behav. Brain Res. 208(2), 636-642 (2010
7. Nam HW, Lee MR, Zhu Y et al. Type 1 equilibrative nucleoside transporter regulates ethanol drinking through accumbal N-methyl-d-aspartate receptor signaling. Biol. Psychiatry 69(11), 1043-1051 (2011
8. Griessenauer CJ, Chang SY, Tye SJ et al. Wireless instantaneous neurotransmitter concentration system: Electrochemical monitoring of serotonin using fast-scan cyclic voltammetry - a proof-of-principle study. J. Neurosurgery 113(3), 656-665 (2010
9. Hermann D, Weber-Fahr W, Sartorius A et al. Translational magnetic resonance spectroscopy reveals excessive central glutamate levels during alcohol withdrawal in humans and rats. Biol. Psychiatry doi:10.1016/j.biopsych.2011.07. 034 (2011) (Epub ahead of print
10. Lee MR, Hinton DJ, Wu J et al. Acamprosate reduces ethanol drinking behaviors and alters the metabolite profile in mice lacking ENT1. Neurosci. Lett. 490(2), 90-95 (2011
11. Tkac I, Henry PG, Andersen P, Keene CD, Low WC, Gruetter R. Highly resolved in vivo 1H NMR spectroscopy of the mouse brain at 9.4 T. Magn. Reson. Med. 52(3), 478-484 (2004
12. Duarte JMN, Lei H, Mlynarik V, Gruetter R. The neurochemical profile quantified by in vivo 1H NMR spectroscopy. NeuroImage doi:10.1016/j.neuroimage. 2011.12.038 (2011) (Epub ahead of print
13. Barker PB, Lin DDM. In vivo proton MR spectroscopy of the human brain. Prog. Nucl. Mag. Res. Sp. 49(2), 99-128 (2006
14. Jansen JF, Backes WH, Nicolay K, Kooi ME. 1H-MR spectroscopy of the brain: Absolute quantification of metabolites. Radiology 240(2), 318-332 (2006
15. Alger JR. Quantitative proton magnetic resonance spectroscopy and spectroscopic imaging of the brain: A didactic review. Top. Magn. Res. Imaging 21(2), 115-128 (2010
16. Andjus RK, Dzakula Z, Markley JL, Macura S. Brain energetics and tolerance to anoxia in deep hypothermia. Ann. NY Acad. Sci. 1048, 10-35 (2005
17. Mangia S, Liimatainen T, Garwood M et al. Frequency offset dependence of adiabatic rotating frame relaxation rate constants: Relevance to MRS investigations of metabolite dynamics in vivo. NMR Biomed. 24(7), 807-814 (2011
18. Shestov AA, Emir UE, Kumar A, Henry PG, Seaquist ER, Oz G. Simultaneous measurement of glucose transport and utilization in the human brain. Am. J. Physiol. Endocrinol. Metab. 301(5), E1040-E1049 (2011
19. Duarte JM, Gruetter R. Characterization of cerebral glucose dynamics in vivo with a four-state conformational model of transport at the blood-brain barrier. J. Neurochem. doi:10.1111/j.1471-4159.2012.07688.x (2012) (Epub ahead of print
20. Provencher SW. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn. Reson. Med. 30(6), 672-679 (1993
21. Provencher SW. Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed. 14(4), 260-264 (2001
22. Cui Q, Lewis IA, Hegeman AD et al. Metabolite identification via the Madison Metabolomics Consortium Database. Nat. Biotechnol. 26(2), 162-164 (2008
23. Wishart DS, Tzur D, Knox C et al. HMDB: The human metabolome database. Nucleic Acids Res. 35(Database issue), D521-D526 (2007
24. Wishart DS, Knox C, Guo AC et al. HMDB: A knowledge base for the human metabolome. Nucleic Acids Res. 37, D603-D610 (2009
25. Braakman N, Oerther T, de Groot HJM, Alia A. High resolution localized two-dimensional MR spectroscopy in mouse brain in vivo. Magn. Reson. Med. 60(2), 449-456 (2008
26. Dreher W, Leibfritz D. Detection of homonuclear decoupled in vivo proton NMR spectra using constant time chemical shift encoding: CT-PRESS. Magn. Reson. Imaging 17(1), 141-150 (1999
27. Deelchand DK, Van de Moortele PF, Adriany G et al. In vivo 1H NMR spectroscopy of the human brain at 9.4 T: Initial results. J. Magn. Reson. 206(1), 74-80 (2010
28. Pfeuffer J, Tkac I, Provencher SW, Gruetter R. Toward an in vivo neurochemical profile: quantification of 18 metabolites in short-echo-time 1H NMR spectra of the rat brain. J. Magn. Reson. 141(1), 104-120 (1999
29. Alf MF, Lei H, Berthet C, Hirt L, Gruetter R, Mlynarik V. High-resolution spatial mapping of changes in the neurochemical profile after focal ischemia in mice. NMR Biomed. 25(2), 247-254 (2011
30. Edelstein WA, Bottomley PA, Pfeifer LM. A signal-to-noise calibration procedure for NMR imaging systems. Med. Phys. 11(2), 180-185 (1984
31. Wolthuis R, van Aken M, Fountas K, Robinson JS Jr, Bruining HA, Puppels GJ. Determination of water concentration in brain tissue by Raman spectroscopy. Anal. Chem. 73(16), 3915-3920 (2001
32. Vanhamme L, Van Huffel S, Van Hecke P, van Ormondt D. Time-domain quantification of series of biomedical magnetic resonance spectroscopy signals. J. Magn. Reson. 140(1), 120-130 (1999
33. Stefan D, Di Cesare F, Andrasescu A et al. Quantitation of magnetic resonance spectroscopy signals: The jMRUI software package. Meas. Sci. Technol. 20(10), 104035 (2009
34. Sriram S, Steiner I. Experimental allergic encephalomyelitis: A misleading model of multiple sclerosis. Ann. Neurol. 58(6), 939-945 (2005
35. Govindaraju V, Young K, Maudsley AA. Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed. 13(3), 129-153 (2000
36. Schuckit MA. Alcohol-use disorders. Lancet 373(9662), 492-501 (2009
37. Nutt DJ, King LA, Phillips LD. Drug harms in the UK: A multicriteria decision analysis. Lancet 376(9752), 1558-1565 (2010
38. Harwood HJ, Fountain D, Livermore G. Economic costs of alcohol abuse and alcoholism. Recent Dev. Alcohol 14, 307-330 (1998
39. Collins PY, Patel V, Joestl SS et al. Grand challenges in global mental health. Nature 475(7354), 27-30 (2011
40. Lopez AD, Murray CC. The global burden of disease, 1990-2020. Nat. Med. 4(11), 1241-1243 (1998
41. Behar KL, Rothman DL, Petersen KF et al. Preliminary evidence of low cortical GABA levels in localized 1H MR spectra of alcohol-dependent and hepatic encephalopathy patients. Am. J. Psychiatry 156(6), 952-954 (1999
42. Lee E, Jang DP, Kim JJ et al. Alteration of brain metabolites in young alcoholics without structural changes. Neuroreport 18(14), 1511-1514 (2007
43. Miese F, Kircheis G, Wittsack HJ et al. 1H MR spectroscopy, magnetization transfer, and diffusion-weighted imaging in alcoholic and nonalcoholic patients with cirrhosis with hepatic encephalopathy. AJNR Am. J. Neuroradiol. 27(5), 1019-1026 (2006
44. Hinton DJ, Lee MR, Jacobson TL et al. Ethanol withdrawal-induced brain metabolites and the pharmacological effects of acamprosate in mice lacking ENT1. Neuropharmacology doi:10.1016/j. neuropharm.2012.02.022 (2012) (Epub ahead of print
45. Meyerhoff DJ, Blumenfeld R, Truran D et al. Effects of heavy drinking, binge drinking, and family history of alcoholism on regional brain metabolites. Alcohol. Clin. Exp. Res. 28(4), 650-661 (2004
46. Ende G, Walter S, Welzel H et al. Alcohol consumption significantly influences the MR signal of frontal choline-containing compounds. NeuroImage 32(2), 740-746 (2006
47. Zahr NM, Mayer D, Rohlfing T et al. Brain injury and recovery following binge ethanol: Evidence from in vivo magnetic resonance spectroscopy. Biol. Psychiatry 67(9), 846-854 (2010
48. Zahr NM, Mayer D, Vinco S et al. In vivo evidence for alcohol-induced neurochemical changes in rat brain without protracted withdrawal, pronounced thiamine deficiency, or severe liver damage. Neuropsychopharmacology 34(6), 1427-1442 (2009
49. Roberto M, Schweitzer P, Madamba SG, Stouffer DG, Parsons LH, Siggins GR. Acute and chronic ethanol alter glutamatergic transmission in rat central amygdala: An in vitro and in vivo analysis. J. Neurosci. 24(7), 1594-1603 (2004
50. Rossetti ZL, Carboni S. Ethanol withdrawal is associated with increased extracellular glutamate in the rat striatum. Eur. J. Pharmacol. 283(1-3), 177-183 (1995
51. Nagy LE, Diamond I, Casso DJ, Franklin C, Gordon AS. Ethanol increases extracellular adenosine by inhibiting adenosine uptake via the nucleoside transporter. J. Biol. Chem. 265, 1946-1951 (1990
52. Choi DS, Cascini MG, Mailliard W et al. The type 1 equilibrative nucleoside transporter regulates ethanol intoxication and preference. Nat. Neurosci. 7(8), 855-861 (2004
53. Nam HW, Lee MR, Hinton DJ, Choi D-S. Reduced effect of NMDA glutamate receptor antagonist on ethanol-induced ataxia and striatal glutamate levels in mice lacking ENT1. Neurosci. Lett. 479(3), 277-281 (2010
54. Holmes A. Merger fever: Can two separate mechanisms work together to explain why we drink? Biol. Psychiatry 69(11), 1015-1016 (2011
55. Sullivan EV, Sable HJ, Strother WN et al. Neuroimaging of rodent and primate models of alcoholism: Initial reports from the integrative neuroscience initiative on alcoholism. Alcohol. Clin. Exp. Res. 29(2), 287-294 (2005
56. Pfefferbaum A, Adalsteinsson E, Bell RL, Sullivan EV. Development and resolution of brain lesions caused by pyrithiamine-and dietary-induced thiamine deficiency and alcohol exposure in the alcohol-preferring rat: A longitudinal magnetic resonance imaging and spectroscopy study. Neuropsychopharmacology 32(5), 1159-1177 (2007
57. Li TK, Lumeng L, McBride WJ, Waller MB. Progress toward a voluntary oral consumption model of alcoholism. Drug Alcohol Depend. 4(1-2), 45-60 (1979
58. Bell RL, Rodd ZA, Lumeng L, Murphy JM, McBride WJ. The alcohol-preferring P rat and animal models of excessive alcohol drinking. Addict. Biol. 11(3-4), 270-288 (2006
59. Lee H, Holburn GH, Price RR. Proton MR spectroscopic studies of chronic alcohol exposure on the rat brain. J. Magn. Reson. Imaging 18(2), 147-151 (2003
60. Heilig M, Thorsell A, Sommer WH et al. Translating the neuroscience of alcoholism into clinical treatments: From blocking the buzz to curing the blues. Neurosci. Biobehav. Rev. 35(2), 334-344 (2010
61. Rimondini R, Arlinde C, Sommer W, Heilig M. Long-lasting increase in voluntary ethanol consumption and transcriptional regulation in the rat brain after intermittent exposure to alcohol. FASEB J. 16(1), 27-35 (2002
62. Sommer WH, Rimondini R, Hansson AC et al. Upregulation of voluntary alcohol intake, behavioral sensitivity to stress, and amygdala crhr1 expression following a history of dependence. Biol. Psychiatry 63(2), 139-145 (2008
63. Kim JH, Karpyak VM, Biernacka JM et al. Functional role of the polymorphic 647 T/C variant of ENT1 (SLC29A1) and its association with alcohol withdrawal seizures. PloS One 6(1), e16331 (2011
64. Krishnan V, Nestler EJ. Linking molecules to mood: new insight into the biology of depression. Am. J. Psychiatry 167(11), 1305-1320 (2010
65. Li X, Frye MA, Shelton RC. Review of pharmacological treatment in mood disorders and future directions for drug development. Neuropsychopharmacology 37(1), 77-101 (2012
66. Frye MA, Watzl J, Banakar S et al. Increased anterior cingulate/medial prefrontal cortical glutamate and creatine in bipolar depression. Neuropsychopharmacology 32(12), 2490-2499 (2007
67. Yuksel C, Ongur D. Magnetic resonance spectroscopy studies of glutamate-related abnormalities in mood disorders. Biol. Psychiatry 68(9), 785-794 (2010
68. Menke A, Samann P, Kloiber S et al. Polymorphisms within the metabotropic glutamate receptor 1 gene are associated with depression phenotypes. Psychoneuroendocrinology 37(4), 565-575 (2011
69. Delgado y Palacios R, Campo A, Henningsen K et al. Magnetic resonance imaging and spectroscopy reveal differential hippocampal changes in anhedonic and resilient subtypes of the chronic mild stress rat model. Biol. Psychiatry 70(5), 449-457 (2011
70. Frye MA, Thomas MA, Yue K et al. Reduced concentrations of N-acetylaspartate (NAA) and the NAA-creatine ratio in the basal ganglia in bipolar disorder: A study using 3-Tesla proton magnetic resonance spectroscopy. Psychiatry Res. 154(3), 259-265 (2007
71. Xi G, Hui J, Zhang Z et al. Learning and memory alterations are associated with hippocampal N-acetylaspartate in a rat model of depression as measured by 1H MRS. PloS One 6(12), e28686 (2011
72. Ende G, Braus DF, Walter S, Weber-Fahr W, Henn FA. The hippocampus in patients treated with electroconvulsive therapy: A proton magnetic resonance spectroscopic imaging study. Arch. Gen. Psychiatry 57(10), 937-943 (2000
73. Sartorius A, Neumann-Haefelin C, Vollmayr B, Hoehn M, Henn FA. Choline rise in the rat hippocampus induced by electroconvulsive shock treatment. Biol. Psychiatry 53(7), 620-623 (2003
74. Willner P. Validity, reliability and utility of the chronic mild stress model of depression: A 10 year review and evaluation. Psychopharmacology 134(4), 319-329 (1997
75. Willner P, Towell A, Sampson D, Sophokleous S, Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology 93(3), 358-364 (1987
76. Jayatissa MN, Bisgaard C, Tingstrom A, Papp M, Wiborg O. Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression. Neuropsychopharmacology 31(11), 2395-2404 (2006
77. Lan MJ, McLoughlin GA, Griffin JL et al. Metabonomic analysis identifies molecular changes associated with the pathophysiology and drug treatment of bipolar disorder. Mol. Psychiatry 14(3), 269-279 (2009
78. McLoughlin GA, Ma D, Tsang TM et al. Analyzing the effects of psychotropic drugs on metabolite profiles in rat brain using 1H NMR spectroscopy. J. Proteome Res. 8(4), 1943-1952 (2009
79. Yang J, Shen J. In vivo evidence for reduced cortical glutamate-glutamine cycling in rats treated with the antidepressant/antipanic drug phenelzine. Neuroscience 135(3), 927-937 (2005
80. Port JD, Agarwal N. MR spectroscopy in schizophrenia. J. Magn. Reson. Imaging 34(6), 1251-1261 (2011
81. Kasai K, Iwanami A, Yamasue H, Kuroki N, Nakagome K, Fukuda M. Neuroanatomy and neurophysiology in schizophrenia. Neurosci. Res. 43(2), 93-110 (2002
82. van Os J, Kapur S. Schizophrenia. Lancet 374(9690), 635-645 (2009
83. Lewis DA, Lieberman JA. Catching up on schizophrenia: natural history and neurobiology. Neuron 28(2), 325-334 (2000
84. Maddock RJ, Buonocore MH. MR spectroscopic studies of the brain in psychiatric disorders. Curr. Top. Behav. Neurosci. doi:10.1007/7854-2011-197 (2012) (Epub ahead of print
85. Jessen F, Fingerhut N, Sprinkart AM et al. N-acetylaspartylglutamate (NAAG) and N-acetylaspartate (NAA) in patients with schizophrenia. Schizophr. Bull. doi:10.1093/ schbul/sbr127 (2011) (Epub ahead of print
86. Klar AA, Ballmaier M, Leopold K et al. Interaction of hippocampal volume and N-acetylaspartate concentration deficits in schizophrenia: A combined MRI and 1H MRS study. NeuroImage 53(1), 51-57 (2010
87. Torres G, Hallas BH, Gross KW, Spernyak JA, Horowitz JM. Magnetic resonance imaging and spectroscopy in a mouse model of schizophrenia. Brain Res. Bull. 75(5), 556-561 (2008
88. Marsman A, van den Heuvel MP, Klomp DW, Kahn RS, Luijten PR, Hulshoff Pol HE. Glutamate in schizophrenia: A focused review and meta-analysis of 1H MRS studies. Schizophr. Bull. doi:10.1093/schbul/ sbr069 (2011) (Epub ahead of print
89. van Elst LT, Valerius G, Buchert M et al. Increased prefrontal and hippocampal glutamate concentration in schizophrenia: Evidence from a magnetic resonance spectroscopy study. Biol. Psychiatry 58(9), 724-730 (2005
90. Olbrich HM, Valerius G, Rusch N et al. Frontolimbic glutamate alterations in first episode schizophrenia: Evidence from a magnetic resonance spectroscopy study. World J. Biol. Psychiatry 9(1), 59-63 (2008
91. Purdon SE, Valiakalayil A, Hanstock CC, Seres P, Tibbo P. Elevated 3T proton MRS glutamate levels associated with poor Continuous Performance Test (CPT-0X) scores and genetic risk for schizophrenia. Schizophr. Res. 99(1-3), 218-224 (2008
92. de la Fuente-Sandoval C, Leon-Ortiz P, Favila R et al. Higher levels of glutamate in the associative-striatum of subjects with prodromal symptoms of schizophrenia and patients with first-episode psychosis. Neuropsychopharmacology 36(9), 1781-1791 (2011
93. Kim SY, Lee H, Kim HJ et al. In vivo and ex vivo evidence for ketamine-induced hyperglutamatergic activity in the cerebral cortex of the rat: Potential relevance to schizophrenia. NMR Biomed. 24(10), 1235-1242 (2011
94. Theberge J, Al-Semaan Y, Williamson PC et al. Glutamate and glutamine in the anterior cingulate and thalamus of medicated patients with chronic schizophrenia and healthy comparison subjects measured with 4.0-T proton MRS. Am. J. Psychiatry 160(12), 2231-2233 (2003
95. Stone JM, Day F, Tsagaraki H et al. Glutamate dysfunction in people with prodromal symptoms of psychosis: Relationship to gray matter volume. Biol. Psychiatry 66(6), 533-539 (2009
96. Stone JM, Howes OD, Egerton A et al. Altered relationship between hippocampal glutamate levels and striatal dopamine function in subjects at ultra high risk of psychosis. Biol. Psychiatry 68(7), 599-602 (2010
97. Lutkenhoff ES, van Erp TG, Thomas MA et al. Proton MRS in twin pairs discordant for schizophrenia. Mol. Psychiatry 15(3), 308-318 (2010
98. Iltis I, Koski DM, Eberly LE et al. Neurochemical changes in the rat prefrontal cortex following acute phencyclidine treatment: An in vivo localized (1)H MRS study. NMR Biomed. 22(7), 737-744 (2009
99. Bartha R, Williamson PC, Drost DJ et al. Measurement of glutamate and glutamine in the medial prefrontal cortex of never-treated schizophrenic patients and healthy controls by proton magnetic resonance spectroscopy. Arch. Gen. Psychiatry 54(10), 959-965 (1997
100. Theberge J, Bartha R, Drost DJ et al. Glutamate and glutamine measured with 4.0 T proton MRS in never-treated patients with schizophrenia and healthy volunteers. Am. J. Psychiatry 159(11), 1944-1946 (2002
101. Theberge J, Williamson KE, Aoyama N et al. Longitudinal grey-matter and glutamatergic losses in first-episode schizophrenia. Br. J. Psychiatry 191, 325-334 (2007
102. Wood SJ, Kennedy D, Phillips LJ et al. Hippocampal pathology in individuals at ultra-high risk for psychosis: A multi-modal magnetic resonance study. NeuroImage 52(1), 62-68 (2010
103. Bustillo JR, Chen H, Gasparovic C et al. Glutamate as a marker of cognitive function in schizophrenia: A proton spectroscopic imaging study at 4 Tesla. Biol. Psychiatry 69(1), 19-27 (2011
104. Do KQ, Trabesinger AH, Kirsten-Kruger M et al. Schizophrenia: glutathione deficit in cerebrospinal fluid and prefrontal cortex in vivo. Eur. J. Neurosci. 12(10), 3721-3728 (2000
105. Matsuzawa D, Obata T, Shirayama Y et al. Negative correlation between brain glutathione level and negative symptoms in schizophrenia: A 3T 1H MRS study. PloS One 3(4), e1944 (2008
106. Matsuzawa D, Hashimoto K. Magnetic resonance spectroscopy study of the antioxidant defense system in schizophrenia. Antioxid. Redox. Signal. 15(7), 2057-2065 (2011
107. Duarte JM, Kulak A, Gholam-Razaee MM, Cuenod M, Gruetter R, Do KQ. N-acetylcysteine normalizes neurochemical changes in the glutathione-deficient schizophrenia mouse model during development. Biol. Psychiatry doi:10.1016/j. biopsych.2011.07.035 (2011) (Epub ahead of print
108. Ratty AK, Fitzgerald LW, Titeler M, Glick SD, Mullins JJ, Gross KW. Circling behavior exhibited by a transgenic insertional mutant. Brain Res. Mol. Brain Res. 8(4), 355-358 (1990
109. Torres G, Hallas BH, Vernace VA, Jones C, Gross KW, Horowitz JM. A neurobehavioral screening of the ckr mouse mutant: Implications for an animal model of schizophrenia. Brain Res. Bull. 62(4), 315-326 (2004
110. Torres G, Meeder BA, Hallas BH, Gross KW, Horowitz JM. Preliminary evidence for reduced social interactions in Chakragati mutants modeling certain symptoms of schizophrenia. Brain Res. 1046(1-2), 180-186 (2005
111. Narayana PA. Magnetic resonance spectroscopy in the monitoring of multiple sclerosis. J. Neuroimaging 15(4 Suppl.), 46S-57S (2005
112. De Stefano N, Filippi M. MR spectroscopy in multiple sclerosis. J. Neuroimaging 17(Suppl. 1), 31S-35S (2007
113. Denic A, Johnson AJ, Bieber AJ, Warrington AE, Rodriguez M, Pirko I. The relevance of animal models in multiple sclerosis research. Pathophysiology 18(1), 21-29 (2011
114. s-Gravenmade EJ, Minderhoud JM. [MRI and MRS diagnosis. Application in multiple sclerosis patients and research animals with experimental allergic encephalomyelitis]. Ned. Tijdschr. Tandheelkd. 100(4), 195-200 (1993
115. Richards TL. Separation of lipids from lactate in experimental allergic encephalomyelitis by zero quantum NMR techniques. Invest. Radiol. 24(12), 955-957 (1989
116. Brenner RE, Munro PM, Williams SC et al. The proton NMR spectrum in acute EAE: The significance of the change in the Cho:Cr ratio. Magn. Reson. Med. 29(6), 737-745 (1993
117. Preece NE, Amor S, Baker D, Gadian DG, O'Neill JK, Urenjak J. Experimental encephalomyelitis modulates inositol and taurine in the spinal cord of Biozzi mice. Magn. Reson. Med. 32(6), 692-697 (1994
118. Butter C, Baker D, O'Neill JK, Turk JL. Mononuclear cell trafficking and plasma protein extravasation into the CNS during chronic relapsing experimental allergic encephalomyelitis in Biozzi AB/H mice. J. Neurol. Sci. 104(1), 9-12 (1991
119. Seamer J, Randles WJ, Fitzgeorge R. The course of Semliki Forest virus infection in mice. Br. J. Exp. Pathol. 48(4), 395-402 (1967
120. t'Hart BA, Vogels JT, Spijksma G, Brok HP, Polman C, van der Greef J. 1H NMR spectroscopy combined with pattern recognition analysis reveals characteristic chemical patterns in urines of MS patients and non-human primates with MS-like disease. J. Neurol. Sci. 212(1-2), 21-30 (2003
121. Smolinska A, Attali A, Blanchet L et al. NMR and pattern recognition can distinguish neuroinflammation and peripheral inflammation. J. Proteome. Res. 10(10), 4428-4438 (2011
122. Pirko I, Johnson A, Gamez J, Macura SI, Rodriguez M. Disappearing "T1 black holes" in an animal model of multiple sclerosis. Front. Biosci. 9, 1222-1227 (2004
123. Denic A, Pirko I, Wootla B, Bieber A, Macura S, Rodriguez M. Deletion of beta2-microglobulin ameliorates spinal cord lesion load and promotes recovery of brainstem NAA levels in a murine model of multiple sclerosis. Brain Pathology doi: 10.1111/j.1750-3639.2012.00576.x (2012) (Epub ahead of print
124. Niessen HG, Debska-Vielhaber G, Sander K et al. Metabolic progression markers of neurodegeneration in the transgenic G93A-SOD1 mouse model of amyotrophic lateral sclerosis. Eur. J. Neurosci. 25(6), 1669-1677 (2007
125. Tsang TM, Woodman B, McLoughlin GA et al. Metabolic characterization of the R6/2 transgenic mouse model of Huntington's disease by high-resolution MAS 1H NMR spectroscopy. J. Proteome Res. 5(3), 483-492 (2006
126. Tkac I, Dubinsky JM, Keene CD, Gruetter R, Low WC. Neurochemical changes in Huntington R6/2 mouse striatum detected by in vivo 1H NMR spectroscopy. J. Neurochem. 100(5), 1397-1406 (2007
127. Jenkins BG, Klivenyi P, Kustermann E et al. Nonlinear decrease over time in N-acetyl aspartate levels in the absence of neuronal loss and increases in glutamine and glucose in transgenic Huntington's disease mice. J. Neurochem. 74(5), 2108-2119 (2000
128. Zacharoff L, Tkac I, Song Q et al. Cortical metabolites as biomarkers in the R6/2 model of Huntington's disease. J. Cereb. Blood Flow Metab. 32(3), 502-514 (2011
129. Chou SY, Lee YC, Chen HM et al. CGS21680 attenuates symptoms of Huntington's disease in a transgenic mouse model. J. Neurochem. 93(2), 310-320 (2005
130. Jenkins BG, Andreassen OA, Dedeoglu A et al. Effects of CAG repeat length, HTT protein length and protein context on cerebral metabolism measured using magnetic resonance spectroscopy in transgenic mouse models of Huntington's disease. J. Neurochem. 95(2), 553-562 (2005
131. Block W, Jessen F, Traber F et al. Regional N-acetylaspartate reduction in the hippocampus detected with fast proton magnetic resonance spectroscopic imaging in patients with Alzheimer disease. Arch. Neurol. 59(5), 828-834 (2002
132. Block W, Traber F, Flacke S, Jessen F, Pohl C, Schild H. In vivo proton MR-spectroscopy of the human brain: Assessment of N-acetylaspartate (NAA) reduction as a marker for neurodegeneration. Amino Acids 23(1-3), 317-323 (2002
133. Dedeoglu A, Choi JK, Cormier K, Kowall NW, Jenkins BG. Magnetic resonance spectroscopic analysis of Alzheimer's disease mouse brain that express mutant human APP shows altered neurochemical profile. Brain Res. 1012(1-2), 60-65 (2004
134. Marjanska M, Curran GL, Wengenack TM et al. Monitoring disease progression in transgenic mouse models of Alzheimer's disease with proton magnetic resonance spectroscopy. Proc. Natl Acad. Sci. USA 102(33), 11906-11910 (2005
135. von Kienlin M, Kunnecke B, Metzger F et al. Altered metabolic profile in the frontal cortex of PS2APP transgenic mice, monitored throughout their life span. Neurobiol. Dis. 18(1), 32-39 (2005
136. Marsden CD. Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 57(6), 672-681 (1994
137. Oz G, Terpstra M, Tkac I et al. Proton MRS of the unilateral substantia nigra in the human brain at 4 tesla: Detection of high GABA concentrations. Magn. Reson. Med. 55(2), 296-301 (2006
138. Koga K, Mori A, Ohashi S et al. H-MRS identifies lactate rise in the striatum of MPTP-treated C57BL/6 mice. Eur. J. Neurosci. 23(4), 1077-1081 (2006
139. Chassain C, Bielicki G, Durand E et al. Metabolic changes detected by proton magnetic resonance spectroscopy in vivo and in vitro in a murin model of Parkinson's disease, the MPTP-intoxicated mouse. J. Neurochem. 105(3), 874-882 (2008
140. Boska MD, Lewis TB, Destache CJ et al. Quantitative 1H magnetic resonance spectroscopic imaging determines therapeutic immunization efficacy in an animal model of Parkinson's disease. J. Neurosci. 25(7), 1691-1700 (2005
141. Remy C, Arus C, Ziegler A et al. 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(1), 166-179 (1994
142. Doblas S, He T, Saunders D et al. In vivo characterization of several rodent glioma models by (1) H-MRS. NMR Biomed. 25(4), 685-694 (2011
143. Hekmatyar SK, Wilson M, Jerome N et al. 1H nuclear magnetic resonance spectroscopy characterisation of metabolic phenotypes in the medulloblastoma of the SMO transgenic mice. Br. J. Cancer 103(8), 1297-1304 (2010
144. Nemutlu E, Juranic NO, Zhang S et al. Electron spray ionization mass spectrometry and 2D 31P NMR for monitoring 18O/16O isotope exchange and turnover rates of metabolic oligophosphates. Anal. Bioanal. Chem. doi:10.1007/s00216- 012-5899-5895 (2012) (Epub ahead of print
145. Nemutlu E, Zhang S, Gupta A et al. Dynamic phosphometabolomic profiling of human tissues and transgenic models by 18O-assisted 31P NMR and mass spectrometry. Physiological Genomics doi:10.1152/physiolgenomics.00152.2011 (2012) (Epub ahead of print
146. Franklin KBJ, Paxinos D. The Mouse Brain Stereotaxic Coordinates (3rd Edition). Elsevier Academic Press, San Diego, CA, USA 2007