In vivo neurochemistry of the brain in schizophrenia as revealed by magnetic resonance spectroscopy

Biological Psychiatry

Volumn 44, Issue 6, 1998, Pages 382-398

  Kegeles, Lawrence S ^a,b   Humaran, Teresa J ^a,b   Mann, J John ^a,b  

^a Columbia University ^*  (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

Functional brain imaging; Magnetic resonance spectroscopy; Neurochemistry; Schizophrenia

Indexed keywords

4 AMINOBUTYRIC ACID; CARBON 13; GLUTAMIC ACID; GLUTAMINE; N ACETYLASPARTIC ACID;

CLINICAL ARTICLE; DIAGNOSTIC ACCURACY; DIAGNOSTIC VALUE; HUMAN; HUMAN CELL; NEUROCHEMISTRY; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; TISSUE DISTRIBUTION;

BRAIN CHEMISTRY; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; SCHIZOPHRENIA;

EID: 0032530498     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3223(97)00425-3     Document Type: Review

References (138)

1. 31P using surface coils. Nature. 283:1980;167.
2. Andrews E.R. A historical review of NMR and its clinical applications. Br Med Bull. 40:1984;115-119.
3. Baldessarini R.J., Cohen B.M., Teicher M.H. Significance of neuroleptic dose and plasma level in the pharmacological treatment of psychoses. Arch Gen Psychiatry. 45:1988;79-91.
4. Barta P.E., Pearlson G.D., Powers R.E., et al. Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. Am J Psychiatry. 147:1990;1457-1462.
5. 19F nuclear magnetic resonance spectroscopy of neuroleptics The first in vivo pharmacokinetics of trifluoperazine in the rat brain and the first in vivo spectrum of fluphenazine in the human brain . Biol Psychiatry. 30:1991;656-662.
6. 1H NMR spectra of human brain. Magn Reson Med. 32:1994;294-302.
7. Berridge M.J. Inositol triphosphate and diacylglycerol as intracellular messengers. Biochem J. 220:1984;345-360.
8. Bertolino A., Callicott J.H., Elman I., et al. Proton magnetic resonance spectroscopic imaging in drug free patients with schizophrenia Regional neuronal damage [abstract] . Biol Psychiatry. 39:1996;634.
9. Bertolino A., Callicott J.H., Nawroz S., et al. Reproducibility of proton magnetic resonance spectroscopic imaging in patients with schizophrenia and normal controls [abstract]. Biol Psychiatry. 39:1996;634.
10. Bigelow L.B., Nasrallah H.A., Rauscher F.P. Corpus callosum thickness in chronic schizophrenia. Br J Psychiatry. 142:1983;284-287.
11. Bloch F., Hansen W.W., Packard M.E. Nuclear induction. Phys Rev. 69:1946;127.
12. Bogerts B., Meertz E., Schonfeldt-Bausch R. Basal ganglia and limbic system pathology in schizophrenia A morphometric study of brain volume and shrinkage . Arch Gen Psychiatry. 42:1985;784-791.
13. Bottomley P.A. Human in vivo NMR spectroscopy in diagnostic medicine Clinical tool or research probe? Radiology. 170:1989;1-15.
14. Bottomley P.A., Hart H.R., Edelstein W.A., et al. Anatomy and metabolism of the normal human brain studied by magnetic resonance at 1.5 Tesla. Radiology. 150:1984;441-446.
15. 13C NMR. J Magn Reson Imaging. 59:1984;338-342.
16. Bottomley P.A., Edelstein W.A., Foster T.H., Adams W.A. In vivo solvent-suppressed localized hydrogen nuclear magnetic resonance (NMR) A new window to metabolism? Proc Natl Acad Sci USA. 82:1985;2148-2152.
17. Brown T.R., Kincaid B.M., Ugurbil K. NMR chemical shift imaging in three dimensions. Proc Natl Acad Sci USA. 79:1982;3523-3526.
18. Brown R., Colter N., Corsellis J.A.N., et al. Postmortem evidence of structural brain changes in schizophrenia. Arch Gen Psychiatry. 43:1986;36-42.
19. Buchsbaum M.S., Ingvar D.H., Kessler R., et al. Cerebral glucography with positron tomography. Arch Gen Psychiatry. 39:1982;251-259.
20. Buckley P., Waddington J.L. Magnetic resonance spectroscopy in schizophrenia A nascent technology for a neurodevelopmental disorder? Biol Psychiatry. 36:1994;789-791.
21. 1H Magnetic resonance spectroscopy of the left temporal and frontal lobes in schizophrenia Clinical, neurodevelopmental, and cognitive correlates . Biol Psychiatry. 36:1994;792-800.
22. Cady E.B., Costello A.M., Dawson M.J. Noninvasive investigation of cerebral metabolism in newborn infants by phosphorus nuclear magnetic resonance spectroscopy. Lancet. i:1983;1059-1063.
23. 31Phosphorous magnetic resonance spectroscopy of the temporal lobes in schizophrenia. Biol Psychiatry. 32:1992;26-32.
24. Carlsson A. The current status of the dopamine hypothesis of schizophrenia. Neuropsychopharmacology. 1:1988;179-186.
25. Carlsson M., Carlsson A. Interactions between glutamatergic and monoaminergic systems within the basal ganglia - Implications for schizophrenia and Parkinson's disease. Trends Neurosci. 13:1990;272-276.
26. Chang J., Musser J., McGregor H. Phospholipase A2 Function and pharmacological regulation . Biochem Pharmacol. 36:1987;2429-2436.
27. 1H magnetic resonance spectroscopy characterization of neuronal dysfunction in drug-naive, chronic schizophrenia. Acad Radiol. 1:1994;211-216.
28. Collinge J., Curtis D. Decreased hippocampal expression of a glutamate receptor gene in schizophrenia. Br J Psychiatry. 159:1991;857-859.
29. D'Adamo A.F., Gidez L.I., Yatsu F.M. Acetyl transport mechanisms. Involvement of N-acetyl aspartic acid in de novo fatty acid biosynthesis in the developing rat brain. Exp Brain Res. 5:1968;267-273.
30. Deakin J.F.W., Slater P., Simpson M.D.C., et al. Frontal cortical and left temporal glutamatergic dysfunction in schizophrenia. J Neurochem. 52:1989;1781-1786.
31. 31P-MRS of the human brain in the study of schizophrenia. Nasrallah H.A., Pettegrew J.W. NMR Spectroscopy in Psychiatric Brain Disorders. 1995;79-106 American Psychiatric Press, Washington, DC.
32. 31Phosphorus magnetic resonance spectroscopy of the frontal and parietal lobes in chronic schizophrenia. Biol Psychiatry. 36:1994;503-510.
33. 31phosphorous magnetic resonance spectroscopic imaging study . Biol Psychiatry. 38:1995;279-286.
34. Deicken R.F., Calabrese G., Merrin E.L., Fein G., Weiner M.W. Basal ganglia phosphorous metabolism in chronic schizophrenia. Am J Psychiatry. 152:1995;126-129.
35. Deicken R.F., Fein G., Weiner M.W. Abnormal frontal lobe phosphorous metabolism in bipolar disorder. Am J Psychiatry. 152:1995;915-918.
36. Deicken R.F., Weiner M.W., Fein G. Decreased temporal lobe phosphomonoesters in bipolar disorder. J Affect Disord. 33:1995;195-199.
37. Deicken RF, Ling Z, Corwin F, et al (1996): Proton MRSI in schizophrenia [abstract]. American Psychiatric Association Annual Meeting, New Research Program and Abstracts, Washington, D.C.: American Psychiatric Association, p 195.
38. DeLisi L.E., Buchsbaum M.S., Holcomb H.H., et al. Increased temporal lobe glucose use in chronic schizophrenic patients. Biol Psychiatry. 25:1989;835-851.
39. DeStefano N., Francis G., Antel J.P., Arnold D.L. Reversible decreases of N-acetylaspartate in the brain of patients with relapsing remitting multiple sclerosis. Proc Soc Mag Reson Med. 1:1993;280.
40. Deutsch S.I., Mastropaolo J., Schwartz B.L., et al. A "glutamatergic hypothesis" of schizophrenia Rationale for pharmacotherapy with glycine . Clin Neuropharmacol. 12:1989;1-13.
41. 19F nuclear magnetic resonance spectroscopy. Psychiatry Res Neuroimaging. 35:1990;107-114.
42. Ernst T., Kreis R., Ross B.D. Absolute quantitation of water and metabolites in the human brain I. Compartments and water . J Magn Reson Series B. 102:1993;1-8.
43. Essali M.A., Das I., deBelleroche J., Hirsch S.R. The platelet polyphosphoinositide system in schizophrenia pathological and pharmacological implications [abstract] . Schizophr Res. 2:1989;148.
44. Falkai P., Bogerts B. Cell loss in the hippocampus of schizophrenics. Eur Arch Psychiatry Neurol Sci. 236:1986;154-161.
45. Feinberg I (1982/83): Schizophrenia: Caused by a fault in programmed synaptic elimination during adolescence? J Psychiat Res 17:319-334.
46. Fisher R.E., Morris E.D., Alpert N.M., Fischman A.J. In vivo imaging of neuromodulatory synaptic transmission using PET A review of relevant neurophysiology . Human Brain Mapping. 3:1995;24-34.
47. Frahm J., Merboldt K.D., Hanicke W., et al. Stimulated echo imaging. J Magn Reson Imaging. 64:1985;81-83.
48. Frahm J., Merboldt K.D., Hanicke W. Localized proton spectroscopy using stimulated echoes. J Magn Reson Imaging. 72:1987;502-508.
49. 31P magnetic resonance chemical shift imaging. Acta Psychiatr Scand. 86:1992;455-462.
50. Fujimoto T., Nakano T., Takano T., et al. Proton magnetic resonance spectroscopy of basal ganglia in chronic schizophrenia. Biol Psychiatry. 40:1996;14-18.
51. 31P Magnetic resonance spectroscopy of the medial temporal lobe of schizophrenic patients with neuroleptic-resistant marked positive symptoms. Eur Arch Psychiatry Clin Neurosci. 244:1994;236-240.
52. Fukuzako H., Takeuchi K., Hokazono Y., et al. Proton magnetic resonance spectroscopy of the left medial temporal and frontal lobes in chronic schizophrenia Preliminary report . Psychiatry Res Neuroimaging. 61:1995;193-200.
53. Gattaz W.F., Gasser T., Beckmann H. Multidimensional analysis of the concentrations of 17 substances in the CSF of schizophrenics and controls. Biol Psychiatry. 20:1985;360-366.
54. Gattaz W.F., Kollisch M., Thuren T., Virtanen J.A., Kinnunen P.K.J. Increased phospholipase A2 activity in schizophrenic patients Reduction after neuroleptic therapy . Biol Psychiatry. 22:1987;421-426.
55. Gattaz W.F., Hubner C.K., Nevalainen T.J., Thuren T., Kinnunen P.K.J. Increased serum phospholipase A2 activity in schizophrenia A replication study . Biol Psychiatry. 28:1990;495-501.
56. Grace A.A. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity A hypothesis for the etiology of schizophrenia . Neuroscience. 41:1991;1-24.
57. Gupta R.K., Gupta P., Moore R.D. NMR studies of intracellular metal ions in intact cells and tissues. Ann Rev Biophys Bioeng. 13:1984;221-246.
58. Gur R.E., Resnick S.M., Alavi A., et al. Regional brain function in schizophrenia I. A positron emission tomography study . Arch Gen Psychiatry. 44:1987;119-125.
59. 1H NMR spectra of metabolites in the human brain. Proc Natl Acad Sci USA. 85:1988;1821-1825.
60. Harrison P.J., McLaughlin D., Kerwin R.W. Decreased hippocampal expression of a glutamate receptor gene in schizophrenia. Lancet. 337:1991;450-452.
61. 19F-MRS A new tool for psychopharmacology . Nasrallah H.A., Pettegrew J.W. NMR Spectroscopy in Psychiatric Brain Disorders. 1995;213-234 American Psychiatric Press, Washington, DC.
62. Hope P.L., Costello A.M., Cady E.B., et al. Cerebral energy metabolism studied with phosphorous NMR spectroscopy in normal and birth-asphyxiated infants. Lancet. ii:1984;366-370.
63. Hoult D.I., Busby S.J.W., Gadian D.G., Radda G.K., Richards R.E., Seeley P.J. Observation of tissue metabolites using phosphorus nuclear magnetic resonance. Nature. 252:1974;285-287.
64. Howe F.A., Maxwell R.J., Saunders D.E., et al. Proton spectroscopy in vivo [review]. Magn Res Q. 9:1993;31-59.
65. Hudson C.J., Young L.T., Li P.P., Warsh J.J. CNS signal transduction in the pathophysiology and pharmacotherapy of affective disorders and schizophrenia. Synapse. 13:1993;278-293.
66. Hwang J.-H., Graham G.D., Behar K.L., et al. Short echo time proton magnetic resonance spectroscopic imaging of macromolecule and metabolite signal intensities in the human brain. Magn Reson Med. 35:1996;633-639.
67. Ingvar D.H., Franzen G. Abnormalities of cerebral blood flow distribution in patients with chronic schizophrenia. Acta Psychiatr Scand. 50:1974;616-622.
68. Jernigan T.L., Sargent T., Pfefferbaum A., et al. 18-Fluorodeoxyglucose PET in schizophrenia. Psychiatry Res. 16:1985;317-330.
69. 19F nuclear magnetic resonance spectroscopy study . Psychiatry Res Neuroimaging. 45:1992;95-104.
70. Kato T., Takahashi S., Shioiri T., Inubushi T. Brain phosphorous metabolism in depressive disorders detected by phosphorous-31 magnetic resonance spectroscopy. J Affect Disord. 26:1992;223-230.
71. 7Li magnetic resonance spectroscopy. J Affect Disord. 27:1993;53-60.
72. Keltner J.R., Wald L.L., Christensen J.D., et al. A technique for detecting GABA in the human brain with PRESS localization and optimized refocusing spectral editing radiofrequency pulses. Magn Reson Med. 36:1996;458-461.
73. Kerwin R.W., Patel S., Meldrum B.S., et al. Asymmetrical loss of glutamate receptor subtype in left hippocampus in schizophrenia. Lancet. i:1988;583-584.
74. Keshavan M.S., Pettegrew J.W. Phosphorus 31 magnetic resonance spectroscopy detects altered brain metabolism before onset of schizophrenia [letter]. Arch Gen Psychiatry. 48:1991;1112-1113.
75. Keshavan M.S., Kapur S., Pettegrew J.W. Magnetic resonance spectroscopy in schizophrenia Potentials, pitfalls, and promise . Am J Psychiatry. 148:1991;976-985.
76. 31P MRS and MRI studies . Schizophr Res. 10:1993;241-246.
77. Kim J.S., Kornhuber H.H., Schmid-Burgk W., et al. Low cerebrospinal fluid glutamate in schizophrenic patients and a new hypothesis on schizophrenia. Neurosci Lett. 20:1980;379-382.
78. 19F NMR spectroscopy. Bio Psychiatry. 29:1991;711-714.
79. Korpi E.R., Kaufmann C.A., Marnela K.-M., Weinberger D.R. Cerebrospinal fluid amino acid concentrations in chronic schizophrenia. Psychiatry Res. 20:1987;337-345.
80. Lock T., Abou-Saleh M.T., Edwards R.H.T. Psychiatry and the new magnetic resonance era. Br J Psychiatry. 157:(suppl 9):1990;38-55.
81. 2+ mobilization in Xenopus oocytes. Proc Natl Acad Sci USA. 87:1990;2196-2200.
82. Maier M. In vivo magnetic resonance spectroscopy Applications in psychiatry . Br J Psychiatry. 167:1995;299-306.
83. Maier M., Ron M.A., Barker G.J., Tofts P.S. Proton magnetic resonance spectroscopy An in vivo method of estimating hippocampal neuronal depletion in schizophrenia . Psychol Med. 25:1995;1201-1209.
84. Mason G.F., Pan J.W., Ponder S.L., et al. Detection of brain glutamate and glutamine in spectroscopic images at 4.1 T. Magn Reson Med. 32:1994;142-145.
85. McIntosh J.C., Cooper J.R. Studies on the function of N-acetyl aspartate in the brain. J Neurochem. 12:1965;825-835.
86. Michaelis T., Merkboldt K.D., Bruhn H., Hanicke W., Frahm J. Absolute concentrations of metabolites in the adult human brain in vivo: Quantification of localized proton MR spectra. Radiology. 187:1993;219-227.
87. Minshew N.J., Panchalingam K., Dombrowski S.M., Pettegrew J.W. Developmentally regulated changes in brain membrane metabolism [abstract]. Biol Psychiatry. 31:1992;62A.
88. 31P magnetic resonance. J Biol Chem. 248:1973;7276-7278.
89. Moonen C.T.W., von Kienlen M., van Zijl P.C.M., et al. Comparison of single shot localization methods (STEAM and PRESS) for in vivo proton NMR spectroscopy. NMR Biomed. 2:1989;201-208.
90. 31P NMR spectra in vivo. Magn Reson Med. 12:1989;282-289.
91. Murphy-Boesch J., Stoyanova R., Srinivasan R., et al. Proton-decoupled 31P chemical shift imaging of the human brain in normal volunteers. NMR Biomed. 6:1993;173-180.
92. Nasrallah H.A., Andreasen N.C., Coffman J.A., et al. A controlled magnetic resonance imaging study of corpus callosum thickness in schizophrenia. Biol Psychiatry. 21:1986;274-282.
93. 1H nuclear magnetic resonance spectroscopy of the hippocampus in schizophrenia. Presentation at the annual meeting the American Psychiatric Association, Washington, DC.
94. 1H MRS) of the hippocampal formation in schizophrenia A pilot study . Br J Psychiatry. 165:1994;481-485.
95. 1H-NMR-spectroscopy of the limbic temporal lobe in patients with schizophrenia. Nasrallah H.A., Pettegrew J.W. NMR Spectroscopy in Psychiatric Brain Disorders. 1995;1-20 American Psychiatric Press, Washington, DC.
96. Negendank W.G., Padavic-Shaller K.A., Li C.-W., et al. Metabolic characterization of human non-Hodgkin's lymphomas in vivo with the use of proton-decoupled phosphorus magnetic resonance spectroscopy. Cancer Res. 55:1995;3286-3294.
97. 31P magnetic resonance spectroscopy. Biol Psychiatry. 29:1991;1149-1152.
98. Ordidge R.J., Bendall M.R., Gordon R.E., et al. Volume selection for in-vivo biological spectroscopy. Govil G., Khetrapal C.L., Saran A. Magnetic Resonance in Biology and Medicine. 1985;387-397 Tata McGraw-Hill, New Delhi.
99. Ordidge R.J., Connelly A., Lohman J.A.B. Image selected in vivo spectroscopy (ISIS) A new technique for spatially selective NMR spectroscopy . J Magn Reson Imaging. 66:1986;283-294.
100. 31P in vivo NMR spectroscopy [abstract]. Soc Neurosci Abstr. 16:1990;843.
101. Perry T.L. Normal cerebrospinal fluid and brain glutamate levels in schizophrenia do not support the hypothesis of glutamatergic neuronal dysfunction. Neurosci Lett. 28:1982;81-85.
102. 31P NMR. Magn Reson Med. 6:1988;135-142.
103. Pettegrew J.W., Keshavan M.S., Panchalingam K., et al. Alterations in brain high-energy phosphate and membrane phospholipid metabolism in first-episode, drug-naive schizophrenics. Arch Gen Psychiatry. 48:1991;563-568.
104. 31P MRS of metabolic alterations in schizophrenia and neurodevelopment. Nasrallah H.A., Pettegrew J.W. NMR Spectroscopy in Psychiatric Brain Disorders. 1995;45-77 American Psychiatric Press, Washington, DC.
105. Piomelli D., Pilon C., Giros B., et al. Dopamine activation of the arachidonic acid cascade as a basis for D1/D2 receptor synergism. Nature. 353:1991;164-167.
106. Post R.M., DeLisi L.E., Holcomb H.H., et al. Glucose utilization in the temporal cortex of affectively ill patients Positron emission tomography . Biol Psychiatry. 22:1987;545-553.
107. 1H decoupling of medicated schizophrenics and healthy controls [abstract]. Proc Int Soc Magn Reson Med. 2:1997;1224.
108. Purcell E.M., Torrey H.C., Pound R.V. Resonance absorption by nuclear magnetic moments in a solid. Phys Rev. 69:1946;37-38.
109. 31P NMR spectroscopy. Br Med Bull. 40:1984;155-159.
110. Renshaw P., Yurgelun-Todd D., Tohen M., Gruber S., Cohen B. Temporal lobe proton magnetic resonance spectroscopy of patients with first-episode psychosis. Am J Psychiatry. 152:1995;444-446.
111. Rosenthal R., Bigelow L.B. Quantitative brain measurements in chronic schizophrenia. Br J Psychiatry. 121:1972;259-264.
112. 13C]glutamate turnover in human brain. Proc Natl Acad Sci USA. 89:1992;9603-9606.
113. 1H NMR measurements of γ-aminobutyric acid in human brain in vivo. Proc Natl Acad Sci USA. 90:1993;5662-5666.
114. Rotrosen J., Wolkin A. Phospholipid and prostaglandin hypothesis in schizophrenia. Meltzer H.Y. Psychopharmacology The Third Generation of Progress . 1987;759-764 Raven Press, New York.
115. Sachs G.S., Renshaw P.F., Lafer B., et al. Variability of brain lithium levels during maintenance treatment A magnetic resonance spectroscopy study . Biol Psychiatry. 38:1995;422-428.
116. Sharma R., Venkatasubramanian P.N., Barany M., Davis J.M. Proton magnetic resonance spectroscopy of the brain in schizophrenic and affective patients. Schizophr Res. 8:1992;43-49.
117. Shenton M.E., Kikinis R., Jolesz F.A., et al. Abnormalities of the left temporal lobe and thought disorder in schizophrenia A quantitative magnetic resonance imaging study . N Engl J Med. 327:1992;604-612.
118. Shioiri T., Kato T., Inubushi T., Murashita J., Takahashi S. Correlations of phosphomonoesters measured by phosphorus-31 magnetic resonance spectroscopy in the frontal lobes and negative symptoms in schizophrenia. Psychiatry Res Neuroimaging. 55:1994;223-235.
119. Shulman R.G., Blamire A.M., Rothman D.L., McCarthy G. Nuclear magnetic resonance imaging and spectroscopy of human brain function. Proc Natl Acad Sci USA. 90:1993;3127-3133.
120. 2H NMR spectroscopy using water as an internal intensity reference. Mag Reson Med. 28:1992;105-121.
121. Simmons M.L., Frondoza C.G., Coyle J.T. Immunocytochemical localization of N-acetyl-aspartate with monoclonal antibodies. Neuroscience. 45:1991;37-45.
122. Stanley JA, Williamson PC, Drost DJ, et al (1992): In vivo proton MRS in never treated schizophrenics. Presentation at the annual meeting of the American Psychiatric Association, Washington, DC.
123. 31P-MR spectroscopy study . Schizophr Res. 13:1994;209-215.
124. Stanley J.A., Williamson P.C., Drost D.J., et al. An in vivo study of the prefrontal cortex of schizophrenic patients at different stages of illness via phosphorus magnetic resonance spectroscopy. Arch Gen Psychiatry. 52:1995;399-406.
125. Stanley J.A., Drost D.J., Williamson P.C., et al. In vivo proton MRS study of glutamate and schizophrenia. Nasrallah H.A., Pettegrew J.W. NMR Spectroscopy in Psychiatric Brain Disorders. 1995;21-44 American Psychiatric Press, Washington, DC.
126. 1H MR spectra. Mag Reson Med. 34:1995;17-24.
127. Stevens J.D. The distribution of phospholipid fractions in the red cell membranes of schizophrenics. Schizophr Bull. 6:1972;60-61.
128. Suddath R.L., Casanova M.F., Goldberg T.E., et al. Temporal lobe pathology in schizophrenia A quantitative magnetic resonance imaging study . Am J Psychiatry. 146:1989;464-472.
129. Tofts P.S., Wray S. A critical assessment of methods of measuring metabolite concentrations by NMR spectroscopy. NMR Biomed. 1:1988;1-10.
130. Tsai G., Coyle J.T. N-Acetylaspartate in neuropsychiatric disorders. Prog Neurobiol. 46:1995;531-540.
131. Ulas J., Cotman C.W. Excitatory amino acid receptors in schizophrenia. Schizophr Bull. 19:1993;105-117.
132. Urenjak J., Williams S.R., Gadian D.G., Noble M. Proton nuclear magnetic resonance spectroscopy unambiguously identifies different neural cell types. J Neurosci. 13:1993;981-989.
133. Waddington J.L., O'Callaghan E., Larkin C., Redmond O., Stack J., Ennis J.T. Magnetic resonance imaging and spectroscopy in schizophrenia. Br J Psychiatry. 157:(suppl):1990;56-65.
134. Weinberger D.R., Berman K.F., Zec R.F. Physiological dysfunction of dorsolateral prefrontal cortex in schizophrenia I. Regional cerebral blood flow evidence . Arch Gen Psychiatry. 43:1986;114-124.
135. Williamson P.C., Drost D.J., Stanley J.A., Carr T.J., Morrison S., Mersky H. Localized phosphorus 31 magnetic resonance spectroscopy in chronic schizophrenic patients and normal controls [letter]. Arch Gen Psychiatry. 48:1991;578.
136. 31P-MRS in the study of schizophrenia. Nasrallah H.A., Pettegrew J.W. NMR Spectroscopy in Psychiatric Brain Disorders. 1995;107-129 American Psychiatric Press, Washington, DC.
137. Wolkin A., Barouche F., Wolf A.P., et al. Dopamine blockade and clinical response Evidence for two biological subgroups of schizophrenia . Am J Psychiatry. 146:1989;905-908.
138. Yurgelun-Todd D.A., Renshaw P.F., Gruber S.A., et al. Proton magnetic resonance spectroscopy of the temporal lobes in schizophrenics and normal controls. Schizophr Res. 19:1996;55-59.