H MRSI and social communication deficits in pediatric complex partial seizures

Epilepsia

Volumn 52, Issue 9, 2011, Pages 1705-1714

  O'Neill, Joseph ^a   Seese, Ronald ^a   Hudkins, Matthew ^a   Siddarth, Prabha ^a   Levitt, Jennifer ^a   Tseng, Pengju Benjamin ^a   Wu, Keng Nei ^a   Gurbani, Suresh ^b   Shields, W Donald ^c   Caplan, Rochelle ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Choline compounds; Complex partial seizures; Magnetic resonance spectroscopy; N Acetyl aspartate; Social communication

Indexed keywords

CHOLINE; N ACETYLASPARTIC ACID; N ACETYLASPARTYLGLUTAMIC ACID; ASPARTIC ACID; CREATINE; DIAGNOSTIC AGENT; DRUG DERIVATIVE; N-ACETYLASPARTATE; PROTON;

ADOLESCENT; ARTICLE; CHILD; CLINICAL ARTICLE; COMMUNICATION DISORDER; COMPLEX PARTIAL SEIZURE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; HUMAN; INFERIOR FRONTAL GYRUS; MALE; METABOLITE; NEUROIMAGING; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SCHOOL CHILD; SOCIAL COMMUNICATION DEFICIT; SUPERIOR TEMPORAL GYRUS; VIDEORECORDING; BRAIN CORTEX; CASE CONTROL STUDY; HEMISPHERIC DOMINANCE; METABOLISM; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOLOGY; SOCIOPATHY; TEMPORAL LOBE EPILEPSY;

ADOLESCENT; ASPARTIC ACID; CASE-CONTROL STUDIES; CEREBRAL CORTEX; CHILD; CHOLINE; COMMUNICATION DISORDERS; CREATINE; EPILEPSY, COMPLEX PARTIAL; FEMALE; FUNCTIONAL LATERALITY; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; PROTONS; SOCIAL BEHAVIOR DISORDERS;

EID: 80052516755     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2011.03114.x     Document Type: Article

References (91)

1. Assaf M, Rivkin PR, Kuzu CH, Calhoun VD, Kraut MA, Groth KM, Yassa MA, Hart J Jr, Pearlson GD,. (2006) Abnormal object recall and anterior cingulate overactivation correlate with formal thought disorder in schizophrenia. Biol Psychiatry 59: 452-459. (Pubitemid 43289226)
2. Baslow MH,. (1997) A review of phylogenetic and metabolic relationships between the acylamino acids, N-acetyl-l-aspartic acid and N-acetyl-l-histidine in the vertebrate nervous system. J Neurochem 68: 1335-1344. (Pubitemid 27133040)
3. Baslow MH,. (2000) Functions of N-acetyl-l-aspartate and N-acetyl-l-aspartyl-glutamate in the vertebrate brain: role in glial cell-specific signaling. J Neurochem 75: 453-459. (Pubitemid 30485425)
4. Baslow MH,. (2002) Evidence supporting a role for N-acetyl-l-aspartate as a molecular water pump in myelinated neurons in the central nervous system An analytical review. Neurochem Int 40: 295-300. (Pubitemid 34131602)
5. Bernasconi A, Bernasconi N, Natsume J, Antel SB, Andermann F, Arnold DL,. (2003) Magnetic resonance spectroscopy and imaging of the thalamus in idiopathic generalized epilepsy. Brain 126 (Pt 11): 2447-2454. (Pubitemid 37314434)
6. Bhakoo KK, Pearce D,. (2000) In vitro expression of N-acetyl aspartate by oligodendrocytes: implications for proton magnetic resonance spectroscopy signal in vivo. J Neurochem 74: 254-262. (Pubitemid 30012776)
7. Blanton RE, Levitt JG, Peterson JR, Fadale D, Sporty ML, Lee M, To D, Mormino EC, Thompson PM, McCracken JT, Toga AW,. (2004) Gender differences in the left inferior frontal gyrus in normal children. Neuroimage 22: 626-636. (Pubitemid 38759425)
8. Bleuler E,. (1983) Lehrbuch der Psychiatrie. 15th ed. Springer-Verlag, New York.
9. Borofsky L, McNealy K, Siddarth P, Wu KN, Dapretto M, Caplan R,. (2010) Semantic processing and thought disorder in childhood-onset schizophrenia: insights from fMRI. J Neurolinguistics 23: 204-222.
10. Brand A, Richter-Landsberg C, Leibfritz D,. (1993) Multinuclear NMR studies on the energy metabolism of glial and neuronal cells. Dev Neurosci 15: 289-298. (Pubitemid 24258162)
11. Briellmann RS, Wellard RM, Jackson GD,. (2005) MR spectroscopy in seizure disorders. In, Gillard J, Waldman A, Barker P, (Eds) Clinical MR imaging: diffusion, perfusion and spectroscopy. Cambridge University Press, Cambridge, pp. 488-508.
12. Cangro CB, Namboodiri MAA, Sklar LA, Corigliano-Murphy A, Neale JH,. (1987) Immunohistochemistry and biosynthesis of N-acetylaspartylglutamate in spinal sensory ganglia. J Neurochem 49: 1579-1588. (Pubitemid 17161382)
13. Capizzano AA, Vermathen P, Laxer KD, Matson GB, Maudsley AA, Soher BJ, Schuff NW, Weiner MW,. (2002) Multisection proton MR spectroscopy for mesial temporal lobe epilepsy. AJNR Am J Neuroradiol 23: 1359-1368. (Pubitemid 35033887)
14. Caplan R, Guthrie D, Fish B, Tanguay P, David-Lando G,. (1989) The Kiddie Formal Thought Disorder Rating Scale: clinical assessment, reliability, and validity. J Am Acad Child Adolesc Psychiatry 28: 408-416. (Pubitemid 19148335)
15. Caplan R, Guthrie D, Tang B, Komo S, Asarnow R,. (2000) Thought disorder in childhood schizophrenia: replication and update of concept. J Am Acad Child Adolesc Psychiatry 39: 771-778. (Pubitemid 30351228)
16. Caplan R, Guthrie D, Komo S, Siddarth P, Chayasirisobhon S, Kornblum H, Sankar R,. (2002) Social communication in pediatric epilepsy. J Child Psychol Psychiatry 43: 245-253.
17. Caplan R, Siddarth P, Bailey CE, Lanphier EK, Gurbani S, Shields WD, Sankar R,. (2006) Thought disorder: a developmental disability in pediatric epilepsy. Epilepsy Behav 8: 726-735.
18. Caplan R, Levitt J, Siddarth P, Taylor J, Daley M, Wu KN, Gurbani S, Shields WD, Sankar R,. (2008) Thought disorder and frontotemporal volumes in pediatric epilepsy. Epilepsy Behav 13: 593-599.
19. Cerullo M, Adler C, Strakowski S, Eliassen J, Nasrallah H, Nasrallah A,. (2007) Memantine normalizes brain activity in the inferior frontal gyrus: a controlled pilot fMRI study. Schizophr Res 97: 294-296. (Pubitemid 350088392)
20. Chakraborty G, Mekala P, Yahya D, Wu G, Ledeen RW,. (2001) Intraneuronal N-acetyl aspartate supplies acetyl groups for myelin lipid synthesis: evidence for myelin-associated aspartoacylase. J Neurochem 78: 736-745. (Pubitemid 32777975)
21. Commission on Classification and Terminology of the International League Against Epilepsy. (1981) Proposal for revised clinical and electroencephalographic classification of epileptic seizures. Epilepsia 22: 489-501.
22. Connelly A, van Paesschen W, Proter DA, Johnson CI, Duncan JS, Gadian DG,. (1998) Proton magnetic resonance spectroscopy in MRI-negative temporal lobe epilepsy. Neurology 51: 61-66. (Pubitemid 28345360)
23. Coyle JT,. (2006) Glutamate and schizophrenia: beyond the dopamine hypothesis. Cell Mol Neurobiol 26: 365-384.
24. Coyle JT, Tsai G, Goff D,. (2003) Converging evidence of NMDA receptor hypofunction in the pathophysiology of schizophrenia. Ann N Y Acad Sci 1003: 318-327. (Pubitemid 38083065)
25. Edden R, Pomper M, Barker P,. (2007) In vivo differentiation of N-acetyl aspartyl glutamate from N-acetyl aspartate at 3 Tesla. Magn Reson Med 57: 977-982. (Pubitemid 46911282)
26. Gardoni F, Di Luca M,. (2006) New targets for pharmacological intervention in the glutamatergic synapse. Eur J Pharmacol 545: 2-10. (Pubitemid 44215874)
27. Guye M, Le Fur Y, Confort-Gouny S, Ranjeva J-P, Bartolomei F, Régis J, Raybaud CA, Chauvel P, Cozzone PJ,. (2002) Metabolic and electrophysiological alterations in subtypes of temporal lobe epilepsy: a combined Proton magnetic resonance spectroscopic imaging and depth electrode study. Epilepsia 43: 1197-1209. (Pubitemid 35176128)
28. Hall J, Romaniuk L, McIntosh AM, Steele JD, Johnstone EC, Lawrie SM,. (2009) Associative learning and the genetics of schizophrenia. Trends Neurosci 32: 359-365.
29. Hattiangady B, Shetty AK,. (2009) Decreased neuronal differentiation of newly generated cells underlies reduced hippocampal neurogenesis in chronic temporal lobe epilepsy. Hippocampus 20: 97-112.
30. Helms G, Ciumas C, Kyaga S, Savic I,. (2006) Increased thalamus levels of glutamate and glutamine (Glx) in patients with idiopathic generalized epilepsy. J Neurol Neurosurg Psychiatry 77: 489-494.
31. Hetherington HP, Kuzniecky RI, Pan JW, Vaughan JT, Twieg DB, Pohost GM,. (1995) Application of high field spectroscopic imaging in the evaluation of temporal lobe epilepsy. Magn Reson Imaging 13: 1175-1180. (Pubitemid 26001919)
32. Holinger DP, Shenton ME, Wible CG, Donnino R, Kikinis R, Jolesz FA, McCarley RW,. (1999) Superior temporal gyrus volume abnormalities and thought disorder in left-handed schizophrenic men. Am J Psychiatry 156: 1730-1735. (Pubitemid 29517565)
33. Holopainen IE, Lundbom NM, Metsähonkala E-L, Komu ME, Sonninen PH, Haaparanta MT, Bergman JR, Sillanpää ML,. (1997) Temporal lobe pathology in epilepsy: proton magnetic resonance spectroscopy and positron emission tomography study. Pediatr Neurol 16: 98-104. (Pubitemid 27137444)
34. Holopainen I, Valtonen ME, Komu ME, Sonninen PH, Manner TE, Lundbom NMI, Sillanpää ML,. (1998) Proton spectroscopy in children with epilepsy and febrile convulsions. Pediatr Neurol 19: 93-99. (Pubitemid 28410384)
35. Honey GD, Corlett PR, Absalom AR, Lee M, Pomarol-Clotet E, Murray GK, MvKenna PJ, Bullmore ET, Menon DK, Fletcher PC,. (2008) Individual differences in psychotic effects of ketamine are predicted by brain function measured under placebo. J Neurosci 28: 6295-6303.
36. Itil T, Keskiner A, Kiremitci N, Holden JM,. (1967) Effect of phencyclidine in chronic schizophrenics. Can Psychiatr Asssoc J 12: 209-212.
37. Jung K-H, Chu K, Lee S-T, Kim J-H, Kang K-M, Song E-C, Kim S-J, Park H-K, Kim M, Lee SK, Roh J-K,. (2009) Region-specific plasticity in the epileptic rat brain: a hippocampal and extrahippocampal analysis. Epilepsia 50: 537-549.
38. 1H MRS and DWI in evaluation of temporal lobe epilepsy. Neurology 58: 1745-1753. (Pubitemid 34663572)
39. 1H-MRS in temporal lobe epilepsy and frontal lobe epilepsy. Psychiatry Clin Neurosci 54: 455-459.
40. Kircher T,. (2008) Neurobiologische Fundierung von Sprach- und Denkstörungen bei Patienten mit Schizophrenie. Fortschr Neurol Psychiatr 76 (Suppl. 1): S24-S32. (Pubitemid 351985530)
41. Kircher T, Liddle P, Brammer M, Murray R, McGuire P,. (2003) Neuronale Korrelate "negativer" formaler Denkstörungen. Nervenarzt 74: 748-754. (Pubitemid 37176304)
42. Klisch J, Juengling F, Spreer J, Koch D, Thiel T, Büchert M, Arnold S, Feuerhake F, Schumacher M,. (2001) Lhermitte- Duclos disease: assessment with MR imaging, positron emission tomography, single-photon emission CT, and Mr spectroscopy. AJNR Am J Neuroradiol 22: 824-830. (Pubitemid 32436221)
43. Li LM, Dubeau F, Andernann E, Arnold DL,. (2000) Proton magnetic resonance spectroscopic imaging studies in patients with newly diagnosed partial epilepsy. Epilepsia 41: 825-831. (Pubitemid 30439573)
44. Luby ED, Cohen BD, Rosenbaum G, Gottlieb JS, Kelley R,. (1959) Study of a new schizophrenomimetic drug; sernyl. AMA Arch Neurol Psychiatry 81: 363-369.
45. Lundbom N, Gaily E, Vuori K, Paetau R, Liukkonen E, Rajapakse JC, Valanne L, Häkkinen A-M, Granström M-L,. (2001) Proton spectroscopic imaging shows abnormalities in glial and neuronal cell pools in frontal lobe epilepsy. Epilepsia 42: 1507-1514. (Pubitemid 34020087)
46. Luszczki JJ, Mohamed M, Czuczwar SJ,. (2006) 2-Phosphonomethyl- pentanedioic acid (glutamate carboxypeptidase II inhibitor) increases threshold for electroconvulsions and enhances the antiseizure action of valproate against maximal electroshock-induced seizures in mice. Eur J Pharmacol 531: 66-73. (Pubitemid 43202217)
47. McGuire P, Quested D, Spence S, Murray R, Frith C, Liddle P,. (1998) Pathophysiology of 'positive' thought disorder in schizophrenia. Br J Psychiatry 173: 231-235. (Pubitemid 28407456)
48. Meador KJ,. (2007) The basic science of memory as it applies to epilepsy. Epilepsia 48 (Suppl. 9): 3-25.
49. Meyerhoff JL, Koller KJ, Walczak DD, Coyle JT,. (1985) Brain regional levels of N-acetyl-aspartyl-glutamate (NAAG): the effect of kindled seizures. Brain Res 346: 392-396. (Pubitemid 16241132)
50. Meyerhoff JL, Carter RE, Yourick DL, Slusher BS, Coyle JT,. (1992) Genetically epilepsy-prone rats have increased brain regional activity of an enzyme which liberates glutamate from N-acetyl-aspartyl-glutamate. Brain Res 593: 140-143.
51. Mueller SG, Suhy J, Laxer KD, Flenniken DL, Axelrad J, Capizzano AA, Weiner MW,. (2002) Reduced extrahippocampal NAA in mesial temporal lobe epilepsy. Epilepsia 43: 1210-1216. (Pubitemid 35176129)
52. Najm I, Wang Y, Shedid D, Lueders HO, Ng TC, Comair YG,. (1998) MRS metabolic markers of seizures and seizure-induced neuronal damage. Epilepsia 39: 244-250. (Pubitemid 28141302)
53. Najm I, Ying Z, Babb T, Crino PB, Macdonald R, Mathern GW, Spreafico R,. (2004) Mechanisms of epileptogenicity in cortical dysplasias. Neurology 62 (Suppl. 3): S9-S13. (Pubitemid 38419836)
54. Nevander G, Ingvar M, Auer R, Siesjo BK,. (1985) Status epilepticus in well-oxygenated rats causes neuronal necrosis. Ann Neurol 18: 281-290. (Pubitemid 15023100)
55. O'Neill J, Tseng P, Pagare R, Frew A, Tafazoli S, Alger J,. (2006) MRSI Voxel Picker (MVP): software for co-evaluation of structural and spectroscopic information. ISMRM Workshop on Data Processing for MR Spectroscopy and Imaging, Warrenton, VA, November 11-13.
56. Angür D, Pohlman J, Dow AL, Eisch AJ, Edwin F, Heckers S, Cohen BM, Patel TB, Carlezon WA Jr,. (2007) Electroconvulsive seizures stimulate glial proliferation and reduce expression of sprouty2 within the prefrontal cortex of rats. Biol Psychiatry 62: 505-512. (Pubitemid 47284031)
57. Passani L, Elkabes S, Coyle JT,. (1998) Evidence for the presence of N-acetylaspartylglutamate in cultured oligodendrocytes and LPS activated microglia. Brain Res 794: 143-145. (Pubitemid 28298875)
58. Patel TB, Clark JB,. (1979) Synthesis of N-acetyl-l-aspartate by rat mitochondria and its involvement in mitochondria/cytosolic carbon transport. Biochem J 184: 163-168.
59. Petroff OAC, Errante LD, Kim JH, Spencer DD,. (2003) N-acetyl-aspartate, total creatine, and myo-inositol in the epileptogenic human hippocampus. Neurology 60: 1646-1651. (Pubitemid 36618092)
60. 1H spectra with LCModel. NMR Biomed 14: 260-264. (Pubitemid 32611437)
61. Rho JM,. (2004) Basic science behind the catastrophic epilepsies. Epilepsia 45 (Suppl. 5): 5-11. (Pubitemid 39056296)
62. 1H magnetic resonance spectroscopy at 3 T in cryptogenic and mesial temporal lobe epilepsy. NMR Biomed 19: 544-553.
63. Robinson MB, Blakely RD, Couto R, Coyle JT,. (1987) Hydrolysis of the brain dipeptide N-acetyl-l-aspartyl-l-glutamate. Identification and characterization of a novel N-acetylated alpha-linked acidic dipeptidase activity from rat brain. J Biol Chem 262: 14498-14506. (Pubitemid 17157357)
64. Ross BD, Jacobson S, Villamil F, Korula J, Kreis R, Ernst T, Shonk T, Moats RA,. (1994) Subclinical hepatic encephalopathy: proton MR spectroscopic abnormalities. Radiology 193: 457-463. (Pubitemid 24338334)
65. Savic I, Thomas AM, Ke Y, Curran J, Fried I, Engel J Jr,. (2000) In vivo measurements of glutamine + glutamate (Glx) and N-acetyl aspartate (NAA) levels in human partial epilepsy. Acta Neurol Scand 102: 179-188. (Pubitemid 30645136)
66. Savic I, Asterman Y, Helms G,. (2004) MRS shows syndrome differentiated metabolite changes in human-generalized epilepsies. Neuroimage 21: 163-172. (Pubitemid 38120284)
67. Sekiguchi M, Okamoto K, Sakai Y,. (1989) Low-concentration Nacetylaspartylglutamate suppresses the climbing fiber response of Purkinje cells in guinea pig cerebellar slices and the responses to excitatory amino acids of Xenopus laevis oocytes injected with cerebellar mRNA. Brain Res 482: 87-96. (Pubitemid 19063153)
68. Serles W, Li LM, Antel SB, Cendes F, Gotman J, Olivier A, Andermann F, Dubeau F, Arnold DL,. (2001) Time course of postoperative recovery of N-Acetyl-Aspartate in temporal lobe epilepsy. Epilepsia 42: 190-197. (Pubitemid 32204798)
69. Shattuck D, Sandor-Leahy S, Schaper K, Rottenberg D, Leahy R,. (2001) Magnetic resonance image tissue classification using a partial volume model. Neuroimage 13: 856-876. (Pubitemid 32848331)
70. Shenton ME, Kikinis R, Jolesz FA, Pollak SD, LeMay M, Wible CG, Hokama H, Martin J, Metcalf D, Coleman M, McCarley RW,. (1992) Abnormalities of the left temporal lobe and thought disorder in schizophrenia. A quantitative magnetic resonance imaging study. N Engl J Med 327: 604-612.
71. Shih JJ, Weisand MP, Lewine J, Sanders J, Dermon J, Lee R,. (2004) Areas of interictal spiking are associated with metabolic dysfunction in MRI-negative temporal lobe epilepsy. Epilepsia 45: 223-229. (Pubitemid 38332748)
72. Simister RJ, McLean MA, Barker GJ, Duncan JS,. (2003) Proton MRS reveals frontal lobe metabolite abnormalities in idiopathic epilepsy. Neurology 61: 897-902. (Pubitemid 37248641)
73. Simister RJ, McLean MA, Barker GJ, Duncan JS,. (2007) Proton magnetic resonance spectroscopy of malformations of cortical development causing epilepsy. Epilepsy Res 74: 107-115. (Pubitemid 46667222)
74. Simmons ML, Frondoza CG, Coyle JT,. (1991) Immunocytochemical localization of N-acetyl-aspartate with monoclonal antibodies. Neuroscience 45: 37-45.
75. Stanley JA, Cendes F, Dubeau F, Andermann F, Arnold DL,. (1998) Proton magnetic resonance spectroscopic imaging in patients with extratemporal epilepsy. Epilepsia 39: 267-273. (Pubitemid 28141305)
76. 1H MRSI predicts surgical outcome in MRI-negative temporal lobe epilepsy. Neurology 58: 821-823. (Pubitemid 34211567)
77. Taylor JL, Blanton RE, Levitt JG, Caplan R, Nobel D, Toga AW,. (2005) Superior temporal gyrus differences in childhood-onset schizophrenia. Schizophr Res 73: 235-241. (Pubitemid 40093884)
78. Tsai G, Coyle JT,. (1995) N-acetyl aspartate in neuropsychiatric disorders. Prog Neurobiol 46: 531-540.
79. Tsai G, Slusher BS, Sim L, Coyle JT,. (1993) Immunocytochemical distribution of N-acetyl-aspartyl-glutamate in the rat forebrain and glutamatergic pathways. J Chem Neuroanat 6: 277-292. (Pubitemid 23300118)
80. Tsien J,. (2000) Linking Hebb's coincidence-detection to memory formation. Curr Opin Neurobiol 10: 266-273. (Pubitemid 30201122)
81. 13C]glucose. Neurosci Lett 251: 181-184. (Pubitemid 28381077)
82. Urenjak J, Williams SR, Gadian DG, Noble M,. (1993) Proton nuclear magnetic resonance spectroscopy unambiguously identifies different neural cell types. J Neurosci 13: 981-989. (Pubitemid 23067586)
83. Westmoreland BF,. (1998) The EEG findings in extratemporal seizures. Epilepsia 39 (Suppl. 4): S1-S8.
84. Williams AJ, Lu XM, Slusher B, Tortella FC,. (2001) Electroencephalogram analysis and neuroprotective profile of the N-acetylated- -linked acidic dipeptidase inhibitor, GPI5232, in normal and brain-injured rats. J Pharmacol Exp Ther 299: 48-57. (Pubitemid 32905117)
85. Witkin JM, Gasior M, Schad C, Zapata A, Shippenberg T, Hartman T, Slusher BS,. (2002) NAALADase (GCP II) inhibition prevents cocaine-kindled seizures. Neuropharmacology 43: 348-356. (Pubitemid 35257926)
86. 1H magnetic resonance spectroscopy in magnetic resonance imaging-negative temporal lobe epilepsy: different biochemical profile compared with hippocampal sclerosis. Ann Neurol 45: 369-376. (Pubitemid 29120042)
87. Wu W-C, Huang C-C, Chung H-W, Liou M, Hsuch C-J, Lee C-S, Wu M-L, Chen C-Y,. (2005) Hippocampal alterations in children with temporal lobe epilepsy with or without a history of febril convulsions: evaluations with MR volumetry and proton MR spectroscopy. AJNR Am J Neuroradiol 26: 1270-1275. (Pubitemid 43821985)
88. Yuan W, Szaflarski JP, Schmithorst VJ, Schapiro M, Byars AW, Strawsburg RH, Holland SK,. (2006) FMRI shows atypical language lateralization in pediatric epilepsy patients. Epilepsia 47: 593-600. (Pubitemid 43355040)
89. Yurgelun-Todd DA, Coyle JT, Gruber SA, Renshaw PF, Silveri MM, Amico E, Cohen B, Goff DC,. (2005) Functional magnetic resonance imaging studies of schizophrenic patients during word production: effects of d-cycloserine. Psychiatry Res 138: 23-31. (Pubitemid 40228959)
90. Zaczek R, Coyle JT,. (1982) Excitatory amino acid analogues: neurotoxicity and seizures. Neuropharmacology 21: 15-26. (Pubitemid 12222281)
91. Zaczek R, Koller K, Cotter R, Heller D, Coyle JT,. (1983) N-acetyl-aspartyl-glutamate: an endogenous peptide with high affinity for a brain 'glutamate' receptor. Proc Natl Acad Sci USA 80: 1116-1119. (Pubitemid 13118097)