Up-regulation of NMDA receptor subunit and post-synaptic density protein expression in the thalamus of elderly patients with schizophrenia

Journal of Neurochemistry

Volumn 98, Issue 4, 2006, Pages 1114-1125

  Clinton, Sarah M ^a,c   Haroutunian, Vahram ^b   Meador Woodruff, James H ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Glutamate; Mediodorsal nucleus; NMDA receptor subunit 2B; Post synaptic density protein 95

Indexed keywords

BRAIN PROTEIN; CELL PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NEUROFILAMENT PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95; SYNAPSE ASSOCIATED PROTEIN 102; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; BRAIN LEVEL; BRAIN REGION; BRAIN TISSUE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; MALE; NERVE PROJECTION; NEUROBIOLOGY; NEUROCHEMISTRY; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DETERMINATION; PROTEIN EXPRESSION; SCHIZOPHRENIA; THALAMUS ANTERIOR NUCLEUS; THALAMUS DORSOMEDIAL NUCLEUS; THALAMUS MEDIALIS CENTRALIS NUCLEUS; THALAMUS NUCLEUS; THALAMUS VENTRAL NUCLEUS; UPREGULATION; WESTERN BLOTTING;

AGED; AGED, 80 AND OVER; BLOTTING, WESTERN; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IN SITU HYBRIDIZATION; MALE; MIDDLE AGED; NERVE TISSUE PROTEINS; RECEPTORS, N-METHYL-D-ASPARTATE; SCHIZOPHRENIA; SYNAPSES; THALAMUS; TUBULIN; UP-REGULATION;

EID: 33746391983     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03954.x     Document Type: Article

References (95)

1. Andreasen N. C., Ehrhardt J. C., Swayze V. W., 2nd, Alliger R. J., Yuh W. T., Cohen G. and Ziebell S. (1990) Magnetic resonance imaging of the brain in schizophrenia: the pathophysiologic significance of structural abnormalities. Arch. Gen. Psychiatry 47, 35-44.
2. Andreasen N. C., Arndt S., Swayze V., 2nd, Cizadlo T., Flaum M., O'Leary D., Ehrhardt J. C. and Yuh W. T. (1994) Thalamic abnormalities in schizophrenia visualized through magnetic resonance image averaging. Science 266, 294-298.
3. Andreasen N. C., O'Leary D. S., Cizadlo T., Arndt S., Rezai K., Ponto L. L., Watkins G. L. and Hichwa R. D. (1996) Schizophrenia and cognitive dysmetria: a positron-emission tomography study of dysfunctional prefrontal-thalamic- cerebellar circuitry. Proc. Natl Acad. Sci. USA 93, 9985-9990.
4. Barria A. and Malinow R. (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35, 345-353.
5. Braus D. F., Weber-Fahr W., Tost H., Ruf M. and Henn F. A. (2002) Sensory information processing in neuroleptic-naive first-episode schizophrenic patients: a functional magnetic resonance imaging study. Arch. Gen. Psychiatry 59, 696-701.
6. Buchsbaum M. S. and Hazlett E. A. (1998) Positron emission tomography studies of abnormal glucose metabolism In schizophrenia. Schizophrenia Bull. 24, 343-364.
7. Buchsbaum M. S., Someya T., Teng C. Y., Abel L., Chin S., Najafi A., Haier R. J., Wu J. and Bunney W. E., Jr (1996) PET and MRI of the thalamus in never-medicated patients with schizophrenia. Am. J. Psychiatry 153, 191-199.
8. Butler P. D., Zemon V., Schechter I., Saperstein A. M., Hoptman M. J., Lim K. O., Revheim N., Silipo G. and Javitt D. C. (2005) Early-stage visual processing and cortical amplification deficits in schizophrenia. Arch. Gen. Psychiatry 62, 495-504.
9. Byne W., Buchsbaum M. S., Kemether E., Hazlett E. A., Shinwari A., Mitropoulou V. and Siever L. J. (2001) Magnetic resonance imaging of the thalamic mediodorsal nucleus and pulvinar in schizophrenia and schizotypal personality disorder. Arch. Gen. Psychiatry 58, 133-140.
10. Byne W., Buchsbaum M. S., Mattiace L. A., Hazlett E. A., Kemether E., Elhakem S. L., Purohit D. P., Haroutunian V. and Jones L. (2002) Postmortem assessment of thalamic nuclear volumes in subjects with schizophrenia. Am. J. Psychiatry 159, 59-65.
11. Carroll R. C. and Zukin R. S. (2002) NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci. 25, 571-577.
12. Clinton S. M. and Meador-Woodruff J. H. (2004a) Thalamic dysfunction in schizophrenia: neurochemical, neuropathological, and in vivo imaging abnormalities. Schizophrenia Res. 69, 237-253.
13. Clinton S. M. and Meador-Woodruff J. H. (2004b) Abnormalities of the NMDA receptor and associated intracellular molecules in the thalamus in schizophrenia and bipolar disorder. Neuropsychopharmacology 29, 1353-1362.
14. Clinton S. M., Haroutunian Y., Davis K. L. and Meador-Woodruff J. H. (2003) Altered expression of NMDA receptor-associated postsynaptic density proteins in the thalamus in schizophrenia. Am. J. Psychiatry 160, 1100-1109.
15. Clinton S. M., Abelson S., Haroutunian V., Davis K. L. and Meador-Woodruff J. H. (2004) Neurofilament subunit protein abnormalities in the thalamus in schizophrenia. Thalamus & Related Syst. 2, 265-272.
16. Clinton S. M., Ibrahim H., Frey K. A., Davis K. L., Haroutunian V. and Meador-Woodruff J. H. (2005) Dopaminergic abnormalities in the thalamus in schizophrenia involve the intracellular signal integrating proteins calcyon and spinophilin. Am. J. Psychiatry 162, 1859-1871.
17. Cohen B. and Wan W. (1996) The thalamus as a site of action of antipsychotic drugs. Am. J. Psychiatry 153, 104-106.
18. Cohen B. M. and Yurgelun-Todd D. (2001) Alterations of thalamic activity in schizophrenia and in response to antipsychotic drugs. Neuropsychopharmacology 25, 305-312.
19. Cullen T. J., Walker M. A., Parkinson N., Craven R., Crow T. J., Esiri M. M. and Harrison P. J. (2003) A postmortem study of the mediodorsal nucleus of the thalamus in schizophrenia. Schizophrenia Res. 60, 157-166.
20. Danos P., Baumann B., Bernstein H. G., Franz M., Stauch R., Northoff G., Krell D., Falkai P. and Bogerts B. (1998) Schizophrenia and anteroventral thalamic nucleus: selective decrease of parvalbumin-immunoreactive thalamocortical projection neurons. Psychiatry Res. 82, 1-10.
21. Danos P., Baumann B., Bernstein H. G., Stauch R., Krell D., Falkai P. and Bogerts B. (2002) The ventral lateral posterior nucleus of the thalamus in schizophrenia: a post-mortem study. Psychiatry Res. 114, 1-9.
22. Danos P., Baumann B., Kramer A., Bernstein H. G., Stauch R., Krell D., Falkai P. and Bogerts B. (2003) Volumes of association thalamic nuclei in schizophrenia: a postmortem study. Schizophrenia Res. 60, 141-155.
23. Dasari M., Friedman L., Jesberger J., Stuve T. A., Findling R. L., Swales T. P. and Schulz S. C. (1999) A magnetic resonance imaging study of thalamic area in adolescent patients with either schizophrenia or bipolar disorder as compared to healthy controls. Psychiatry Res. 91, 155-162.
24. Dean B., Scan E., Bradbury R. and Copolov D. (1999) Decreased hippocampal (CA3) NMDA receptors in schizophrenia. Synapse 32, 67-69.
25. Deutch A., Ongur D. and Duman R. (1995) Antipsychotic drugs induce Fos protein in the thalamic paraventricular nucleus: a novel antipsychotic drug action. Neuroscience 66, 337-346.
26. Domino E. and Luby E. (1981) Abnormal mental states induced by phencyclidine as a model of schizophrenia, in PCP (Phencyclidine): Historical and Current Perspectives (Domino E., ed.), pp. 401-418. NPP Books, Ann. Arbor, MI.
27. Dorph-Petersen K. A., Pierri J. N., Sun Z., Sampson A. R. and Lewis D. A. (2004) Stereological analysis of the mediodorsal thalamic nucleus in schizophrenia: volume, neuron number, and cell types. J. Comp. Neurol. 472, 449-462.
28. Dracheva S., Marras S. A., Elhakem S. L., Kramer F. R., Davis K. L. and Haroutunian V. (2001) N-methyl-D-aspartic acid receptor expression in the dorsolateral prefrontal cortex of elderly patients with schizophrenia. Am. J. Psychiatry 158, 1400-1410.
29. Ehlers M., Fung E., O'Brien R. and Huganir R. (1998) Splice variant-specific interaction of the NMDA receptor subunit NR1 with neuronal intermediate filaments. J. Neurosci. 18, 720-730.
30. Emamian E. S., Karayiorgou M. and Gogos J. A. (2004) Decreased phosphorylation of NMDA receptor type 1 at serine 897 in brains of patients with schizophrenia. J. Neurosci. 24, 1561-1564.
31. Ettinger U., Chitnis X. A., Kumari V., Fannon D. G., Sumich A. L., O'Ceallaigh S., Doku V. C. and Sharma T. (2001) Magnetic resonance imaging of the thalamus in first-episode psychosis. Am. J. Psychiatry 158, 116-118.
32. Flaum M., Swayze V. W., 2nd, O'Leary D. S., Yuh W. T., Ehrhardt J. C., Arndt S. V. and Andreasen N. C. (1995) Effects of diagnosis, laterality, and gender on brain morphology in schizophrenia. Am. J. Psychiatry 152, 704-714.
33. Fukaya M., Kato A., Lovett C., Tonegawa S. and Watanabe M. (2003) Retention of NMDA receptor NR2 subunits in the lumen of endoplasmic reticulum in targeted NR1 knockout mice. Proc. Natl Acad. Sci. USA 100, 4855-4860.
34. Gao X. M., Sakai K., Roberts R. C., Conley R. R., Dean B. and Tamminga C. A. (2000) Ionotropic glutamate receptors and expression of N-methyl-D-aspartate receptor subunits in subregions of human hippocampus: effects of schizophrenia. Am. J. Psychiatry 157, 1141-1149.
35. Gilbert A. R., Rosenberg D. R., Harenski K., Spencer S., Sweeney J. A. and Keshavan M. S. (2001) Thalamic volumes in patients with first-episode schizophrenia. Am. J. Psychiatry 158, 618-624.
36. Goff D. C. and Coyle J. T. (2001) The emerging role of glutamate in the pathophysiology and treatment of schizophrenia. Am. J. Psychiatry 158, 1367-1377.
37. Goff D. C., Tsai G., Manoach D. S. and Coyle J. T. (1995) Dose-finding trial of D-cycloserine added to neuroleptics for negative symptoms in schizophrenia. Am. J. Psychiatry 152, 1213-1215.
38. Grimwood S., Slater P., Deakin J. F. W. and Hutson P. H. (1999) NR2B-containing NMDA receptors are upregulated in temporal cortex in schizophrenia. Neuroreport 10, 461-465.
39. Guillaud L., Setou M. and Hirokawa N. (2003) KIF17 dynamics and regulation of NR2B trafficking in hippocampal neurons. J. Neurosci. 23, 131-140.
40. Gur R. E., Maany V., Mozley P. D., Swanson C., Bilker W. and Gur R. C. (1998) Subcortical MRI volumes in neuroleptic-naive and treated patients with schizophrenia. Am. J. Psychiatry 155, 1711-1717.
41. Harrison P. J. and Weinberger D. R. (2005) Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol. Psychiatry 10, 40-68; image 45.
42. Hazlett E. A., Buchsbaum M. S., Byne W., Wei T. C., Spiegel-Cohen J., Geneve C., Kinderlehrer R., Haznedar M. M., Shihabuddin L. and Siever L. J. (1999) Three-dimensional analysis with MRI and PET of the size, shape, and function of the thalamus in the schizophrenia spectrum. Am. J. Psychiatry 156, 1190-1199.
43. Heckers S., Rauch S. L., Goff D., Savage C. R., Schacter D. L., Fischman A. J. and Alpert N. M. (1998) Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nat. Neurosci. 1, 318-323.
44. Hirai T. and Jones E. G. (1989) A new parcellation of the human thalamus on the basis of histochemical staining. Brain Res. Brain Res. Rev. 14, 1-34.
45. Holcomb H., Cascella N., Thaker G., Medoff D., Dannals R. and Tamminga C. (1996) Functional sites of neuroleptic drug action in the human brain: PET/FDG studies with and without haloperidol. Am. J. Psychiatry 153, 41-49.
46. Hollmann M. and Heinemann S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci.17, 31-108.
47. Ibrahim H. M., Hogg A. J., Healy D. J., Haroutunian V., Davis K. L. and Meador-Woodruff J. H. (2000) Ionotropic glutamate receptor binding and subunit mRNA expression in thalamic nuclei in schizophrenia. Am. J. Psychiatry 157, 1811-1823.
48. Javitt D. C. (2004) Glutamate as a therapeutic target in psychiatric disorders. Mol. Psychiatry 9, 979.
49. Javitt D., Zylberman I., Zukin S., Heresco-Levy U. and Lindenmayer J. (1994) Amelioration of negative symptoms in schizophrenia by glycine. Am. J. Psychiatry 151, 1234-1336.
50. Jones E. G. (1998) The thalamus of primates, in The Primate Nervous System, Part II, Vol. 14 (Bloom F. E., Bjorklund A. and Hokfelt T., eds), pp. 1-246. Elsevier, New York.
51. Kiehl K. A., Stevens M. C., Celone K., Kurtz M. and Krystal J. H. (2005) Abnormal hemodynamics in schizophrenia during an auditory oddball task. Biol. Psychiatry 57, 1029-1040.
52. Koh P. O., Bergson C., Undie A. S., Goldman-Rakic P. S. and Lidow M. S. (2003) Up-regulation of the D1 dopamine receptor-interacting protein, calcyon, in patients with schizophrenia. Arch. Gen. Psychiatry 60, 311-319.
53. Konick L. C. and Friedman L. (2001) Meta-analysis of thalamic size in schizophrenia. Biol. Psychiatry 49, 28-38.
54. Krystal J. H., D'Souza D. C., Petrakis I. L., Belger A., Berman R. M., Charney D. S., Abi-Saab W. and Madonick S. (1999) NMDA agonists and antagonists as probes of glutamatergic dysfunction and pharmacotherapies in neuropsychiatric disorders. Harvard Rev. Psychiatry 1, 125-143.
55. Lahti A., Holcomb H., Medoff D. and Tamminga C. (1995) Ketamine activates psychosis and alters limbic blood flow in schizophrenia. Neuroreport 6, 869-872.
56. Lau L., Mammen A., Ehlers M., Kindler S., Chung W., Garner C. and Huganir R. (1996) Interaction of the N-methyl-D-aspartate receptor complex with a novel synapse-associated protein, SAP102. J. Biol. Chem. 271, 21 622-21 628.
57. Lezcano N., Mrzljak L., Eubanks S., Levenson R., Goldman-Rakic P. and Bergson C. (2000) Dual signaling regulated by calcyon, a D1 dopamine receptor interacting protein. Science 287, 1660-1664.
58. Lidow M. S., Roberts A., Zhang L., Koh P. O., Lezcano N. and Bergson C. (2001) Receptor crosstalk protein, calcyon, regulates affinity state of dopamine D1 receptors. Eur. J. Pharmacol. 427, 187-193.
59. Linden A. M., Vasanen J., Storvik M., Lakso M., Korpi E. R., Wong G. and Castren E. (2001) Uncompetitive antagonists of the N-methyl-D-aspartate (NMDA) receptors alter the mRNA expression of proteins associated with the NMDA receptor complex. Pharmacol. Toxicol. 88, 98-105.
60. Mai J., Assheuer J. and Paxinos G. (1997) Atlas of the Human Brain. Academic Press, San Diego.
61. McIlhinney R. A., Le Bourdelles B., Molnar E., Tricaud N., Streit P. and Whiting P. J. (1998) Assembly intracellular targeting and cell surface expression of the human N-methyl-D-aspartate receptor subunits NR1a and NR2A in transfected cells. Neuropharmacology 37, 1355-1367.
62. Mueller H. T. and Meador-Woodruff J. H. (2004) NR3A NMDA receptor subunit mRNA expression in schizophrenia, depression and bipolar disorder. Schizophrenia Res. 71, 361-370.
63. Mueller H. T., Haroutunian V., Davis K. L. and Meador-Woodruff J. H. (2004) Expression of the ionotropic glutamate receptor subunits and NMDA receptor-associated intracellular proteins in the substantia nigra in schizophrenia. Mol. Brain Res. 121(1-2), 60-69.
64. Muller B., Kistner U., Kindler S. et al. (1996) SAP102, a novel postsynaptic protein that interacts with NMDA receptor complexes in vivo. Neuron 17, 255-265.
65. Nudmamud-Thanoi S. and Reynolds G. P. (2004) The NR1 subunit of the glutamate/NMDA receptor in the superior temporal cortex in schizophrenia and affective disorders. Neuroscience Lett. 372, 173-177.
66. Pakkenberg B. (1990) Pronounced reduction of total neuron number in mediodorsal thalamic nucleus and nucleus accumbens in schizophrenics. Arch. Gen. Psychiatry 47, 1023-1028.
67. Pakkenberg B. (1992) The volume of the mediodorsal thalamic nucleus in treated and untreated schizophrenics. Schizophrenia Res. 7, 95-100.
68. Pakkenberg B. (1993) Leucotomized schizophrenics lose neurons in the mediodorsal thalamic nucleus. Neuropathol. Appl. Neurobiol. 19, 373-380.
69. Popken G. J., Bunney W. E., Jr, Potkin S. G. and Jones E. G. (2000) Subnucleus-specific loss of neurons in medial thalamus of schizophrenics. Proc. Natl Acad. Sci. USA 97, 9276-9280.
70. Resnick S. M., Gur R. E., Alavi A., Gur R. C. and Reivich M. (1988) Positron emission tomography and subcortical glucose metabolism in schizophrenia. Psychiatry Res. 24, 1-11.
71. Richardson-Burns S. M., Haroutunian V., Davis K. L., Watson S. J. and Meador-Woodruff J. H. (2000) Metabotropic glutamate receptor mRNA expression in the schizophrenic thalamus. Biol. Psychiatry 47, 22-28.
72. Rutter A. and Stephenson F. (2000) Coexpression of postsynaptic density-95 protein with NMDA receptors results in enhanced receptor expression together with a decreased sensitivity to L-glutamate. J. Neurochem. 75, 2501-2510.
73. Sans N., Prybylowski K., Petralia R. S., Chang K., Wang Y. X., Racca C., Vicini S. and Wenthold R. J. (2003) NMDA receptor trafficking through an interaction between PDZ proteins and the exocyst complex. Nat. Cell Biol. 5, 520-530.
74. Scott D. B., Blanpied T. A., Swanson G. T., Zhang C. and Ehlers M. D. (2001) An NMDA receptor ER retention signal regulated by phosphorylation and alternative splicing. J. Neurosci. 21, 3063-3072.
75. Setou M., Nakagawa T., Seog D. H. and Hirokawa N. (2000) Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288, 1796-1802.
76. Sheng M. H.-T. (2001) The postsynaptic specialization, in Synapses (Cowan W. M., Sudhof T. C. and Stevens C. F., eds), pp. 315-355. The Johns Hopkins University Press, Baltimore.
77. Sheng M. and Pak D. (2000) Ligand-gated ion channel interactions with cytoskeletal and signaling proteins. Annu. Rev. Physiol. 62, 755-778.
78. Silbersweig D. A., Stern E., Frith C. et al. (1995) A functional neuroanatomy of hallucinations in schizophrenia. Nature 378, 176-179.
79. Smith R. E., Haroutunian V., Davis K. L. and Meador-Woodruff J. H. (2001a) Vesicular glutamate transporter transcript expression in the thalamus in schizophrenia. Neuroreport 12, 2885-2887.
80. Smith R. E., Haroutunian V., Davis K. L. and Meador-Woodruff J. H. (2001b) Expression of excitatory amino acid transporter transcripts in the thalamus of subjects with schizophrenia. Am. J. Psychiatry 158, 1393-1399.
81. Staal W. G., Hulshoff Pol H. E., Schnack H., van der Schot A. C. and Kahn R. S. (1998) Partial volume decrease of the thalamus in relatives of patients with schizophrenia. Am. J. Psychiatry 155, 1784-1786.
82. Standley S., Roche K. W., McCallum J., Sans N. and Wenthold R. J. (2000) PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 28, 887-898.
83. Steigerwald F., Schulz T. W., Schenker L. T., Kennedy M. B., Seeburg P. H. and Kohr G. (2000) C-Terminal truncation of NR2A subunits impairs synaptic but not extrasynaptic localization of NMDA receptors. J. Neurosci. 20, 4573-4581.
84. Steriade M., Jones E. G. and McCormick D. A. (1997) Thalamus: Organization and Function, Vol. 1. Elsevier, Amsterdam.
85. Symond M. P., Harris A. W., Gordon E. and Williams L. M. (2005) 'Gamma synchrony' in first-episode schizophrenia: a disorder of temporal connectivity? Am. J. Psychiatry 162, 459-465.
86. Takahashi H., Koeda M., Oda K., Matsuda T., Matsushima E., Matsuura M., Asai K. and Okubo Y. (2004) An fMRI study of differential neural response to affective pictures in schizophrenia. Neuroimage 22, 1247-1254.
87. Tamminga C. A., Thaker G. K., Buchanan R., Kirkpatrick B., Alphs L. D., Chase T. N. and Carpenter W. T. (1992) Limbic system abnormalities identified in schizophrenia using positron emission tomography with fluorodeoxyglucose and neocortical alterations with deficit syndrome. Arch. Gen. Psychiatry 49, 522-530.
88. Toro C. and Deakin J. F. (2005) NMDA receptor subunit NRI and postsynaptic protein PSD-95 in hippocampus and orbitofrontal cortex in schizophrenia and mood disorder. Schizophrenia Res. 80, 323-330.
89. Toyooka K., Iritani S., Makifuchi T. et al. (2002) Selective reduction of a PDZ protein, SAP-97, in the prefrontal cortex of patients with chronic schizophrenia. J. Neurochem. 83, 797-806.
90. Tsai G., Yang P., Chung L. C., Lange N. and Coyle J. T. (1998) D-serine added to antipsychotics for the treatment of schizophrenia. Biol. Psychiatry 44, 1081-1089.
91. Ulas J., Nguyen L. and Cotman C. W. (1993) Chronic haloperidol treatment enhances binding to NMDA receptors in rat cortex. Neuroreport 4, 1049-1051.
92. Vita A., Bressi S., Perani D., Invernizzi G., Giobbio G. M., Dieci M., Garbarini M., Del Sole A. and Fazio F. (1995) High-resolution SPECT study of regional cerebral blood flow in drug-free and drug-naive schizophrenic patients. Am. J. Psychiatry 152, 876-882.
93. Washbourne P., Liu X. B., Jones E. G. and McAllister A. K. (2004) Cycling of NMDA receptors during trafficking in neurons before synapse formation. J. Neurosci. 24, 8253-8264.
94. Wyneken U., Smalla K. H., Marengo J. J. et al. (2001) Kainate-induced seizures alter protein composition and N-methyl-D-aspartate receptor function of rat forebrain postsynaptic densities. Neuroscience 102, 65-74.
95. Young K., Manaye K., Liang C., Hicks P. and German D. (2000) Reduced number of mediodorsal and anterior thalamic neurons in schizophrenia. Biol. Psychiatry 47, 944-953.