Postnatal phencyclidine administration selectively reduces adult cortical parvalbumin-containing interneurons

Neuropsychopharmacology

Volumn 33, Issue 10, 2008, Pages 2442-2455

  Wang, Cheng Z ^a   Yang, San F ^a   Xia, Yan ^a   Johnson, Kenneth M ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

N methyl D aspartate receptor; Neuroapoptosis; Neurogenesis; Parvalbumin; Phencyclidine; Schizophrenia

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; BROXURIDINE; CALBINDIN; CALCIUM BINDING PROTEIN; CALRETININ; CASPASE 3; CELL MARKER; DIZOCILPINE; KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PARVALBUMIN; PHENCYCLIDINE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; CELL PROLIFERATION; CONTROLLED STUDY; DENSITOMETRY; IMMUNOHISTOCHEMISTRY; INTERNEURON; NERVOUS SYSTEM DEVELOPMENT; NEUROPATHOLOGY; NICK END LABELING; NONHUMAN; PERINATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SCHIZOPHRENIA;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BROMODEOXYURIDINE; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CASPASE 3; CELL COUNT; CELL PROLIFERATION; CELL SURVIVAL; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; INTERNEURONS; MALE; PARVALBUMINS; PHENCYCLIDINE; RATS; RATS, SPRAGUE-DAWLEY; SCHIZOPHRENIA; TIME;

EID: 49549088180     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1301647     Document Type: Article

References (110)

1. Abdul-Monim Z, Neill JC, Reynolds GP (2007). Sub-chronic psychotomimetic phencyclidine induces deficits in reversal learning and alterations in parvalbumin-immunoreactive expression in the rat. J Psychopharmacol 21: 198-205.
2. Abekawa T, Ito K, Nakagawa S, Koyama T (2007). Prenatal exposure to an NMDA receptor antagonist, MK-801 reduces density of parvalbumin-immunoreactive GABAergic neurons in the medial prefrontal cortex and enhances phencyclidine-induced hyperlocomotion but not behavioral sensitization to methamphetamine in postpubertal rats. Psychopharmacology (Berl) 192: 303-316.
3. Alcántara S, Ferrer I, Soriano E (1993). Postnatal development of parvalbumin and calbindin D28K immunoreactivities in the cerebral cortex of the rat. Anat Embryol (Berl) 188: 63-73.
4. Alexiades MR, Cepko C (1996). Quantitative analysis of proliferation and cell cycle length during development of the rat retina. Dev Dyn 205: 293-307.
5. Arnold SE, Hyman BT, Van Hoesen GW, Damasio AR (1991). Some cytoarchitectural abnormalities of the entorhinal cortex in schizophrenia. Arch Gen Psychiatry 48: 625-632.
6. Baimbridge KG, Celio MR, Rogers JH (1992). Calcium-binding proteins in the nervous system. TINS 15: 303-308.
7. Bayer SA, Altman J (2004). Chapter 2: development of the telencephalon, neuronal stem cells, neurogenesis, neuronal migration. In: Paxinous G (ed) The Rat Nervous System, 3rd edn. Academic Press: San Diego. pp 27-73.
8. Beasley CL, Reynolds GP (1997). Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics. Schiz Res 24: 349-355.
9. Benes FM, Berretta S (2001). GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology 25: 1-27.
10. Benes FM, Kwok EW, Vincent SL, Todtenkopf MS (1998). A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives. Biol Psychiatry 44: 88-97.
11. Benes FM, McSparren J, Bird ED, SanGiovanni JP, Vincent SL (1991). Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 48: 996-1001.
12. Benes FM, Vincent SL, Todtenkopf M (2001). The density of pyramidal and nonpyramidal neurons in anterior cingulate cortex of schizophrenic and bipolar subjects. Biol Psychiatry 50: 395-406.
13. Bhide PG (1996). Cell cycle kinetics in the embryonic mouse corpus striatum. J Comp Neurol 374: 506-522.
14. Byne W, Buchsbaum MS, Mattiace LA, Hazlett EA, Kemether E, Elhakem SL et al (2002). Postmortem assessment of thalamic nuclear volumes in subjects with schizophrenia. Am J Psychiatry 159: 59-65.
15. Carlsen J, De Olmos JS (1981). A modified cupric-silver technique for the impregnation of degenerating neurons and their processes. Brain Res 208: 426-431.
16. Chard PS, Bleakman D, Christakos S, Fullmer CS, Miller RJ (1993). Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. J Physiol 472: 341-357.
17. Cochran SM, Fujimura M, Morris BJ, Pratt JA (2002). Acute and delayed effects of phencyclidine upon mRNA levels of markers of glutamatergic and GABAergic neurotransmitter function in the rat brain. Synapse 46: 206-214.
18. Cochran SM, Kennedy M, McKerchar CE, Steward LJ, Pratt JA, Morris BJ (2003). Induction of metabolic hypofunction and neurochemical deficits after chronic intermittent exposure to phencyclidine: differential modulation by antipsychotic drugs. Neuropsychopharmacology 28: 265-275.
19. Condé F, Lund JS, Jacobowitz DM, Baimbridge KG, Lewis DA (1994). Local circuit neurons immunoreactive for calretinin, calbindin D-28k, or parvalbumin in monkey prefrontal cortex: distribution and morphology. J Comp Neurol 341: 95-116.
20. Cotter D, Landau S, Beasley C, Stevenson R, Chana G, MacMillan L et al (2002). The density and spatial distribution of GABAergic neurons, labelled using calcium binding proteins, in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia. Biol Psychiatry 51: 377-386.
21. Danos P, Baumann B, Bernstein HG, Franz M, Stauch R, Northoff G et al (1998). Schizophrenia and anteroventral thalamic nucleus: selective decrease of parvalbumin-immunoreactive thalamocortical projection neurons. Psychiatry Res 82: 1-10.
22. Danos P, Baumann B, Krämer A, Bernstein HG, Stauch R, Krell D et al (2003). Volumes of association thalamic nuclei in schizophrenia: a postmortem study. Schizophr Res 60: 141-155.
23. Davidson LL, Heinrichs RW (2003). Quantification of frontal and temporal lobe brain-imaging findings in schizophrenia: a metaanalysis. Psychiatry Res Neuroimaging 122: 69-87.
24. Daviss SR, Lewis DA (1995). Local circuit neurons of the prefrontal cortex in schizophrenia: selective increase in the density of calbindin-immunoreactive neurons. Psychiatry Res 59: 81-96.
25. Egerton A, Reid L, McKerchar CE, Morris BJ, Pratt JA (2005). Impairment in perceptual attentional set-shifting following PCP administration: a rodent model of set-shifting deficits in schizophrenia. Psychopharmacology (Berl) 179: 77-84.
26. Eldridge SR, Tilbury LF, Goldsworthy TL, Butterworth BE (1990). Measurement of chemically induced cell proliferation in rodent liver and kidney: a comparison of 5-bromo-2′-deoxyuridine and [3H]thymidine administered by injection or osmotic pump. Carcinogenesis 11: 2245-2251.
27. Eyles DW, McGrath JJ, Reynolds GP (2002). Neuronal calcium-binding proteins and schizophrenia. Schizophr Res 57: 27-34.
28. Falkai P, Schneider-Axmann T, Honer WG (2000). Entorhinal cortex prealpha cell clusters in schizophrenia: quantitative evidence of a developmental abnormality. Biol Psychiatry 47: 937-943.
29. D-amphetamine. Neurotox Res 5: 549-564.
30. Fredriksson A, Archer T (2004). Neurobehavioural deficits associated with apoptotic neurodegeneration and vulnerability for ADHD. Neurotox Res 6: 435-456.
31. Fredriksson A, Archer T, Alma H, Gordh T, Eriksson P (2004). Neurofunctional deficits and potentiated apoptosis by neonatal NMDA antagonist administration. Behav Brain Res 153: 367-376.
32. Gogtay N, Sporn A, Clasen LS, Nugent TF, Greenstein D, Nicolson R et al (2004). Comparison of progressive cortical gray matter loss in childhood-onset schizophrenia with that in childhood-onset atypical psychoses. Arch Gen Psychiatry 61: 17-22.
33. Granato A (2006). Altered organization of cortical interneurons in rats exposed to ethanol during neonatal life. Brain Res 1069: 23-30.
34. Gritti I, Manns ID, Mainville L, Jones BE (2003). Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat. J Comp Neurol 458: 11-31.
35. Gur RE, Cowell P, Turetsky BI, Gallacher F, Cannon T, Bilker W et al (1998). A follow-up magnetic resonance imaging study of schizophrenia. Relationship of neuroanatomical changes to clinical and neurobehavioral measures. Arch Gen Psychiatry 55: 145-152.
36. Harris LW, Sharp T, Gartlon J, Jones DN, Harrison PJ (2003). Long-term behavioural, molecular and morphological effects of neonatal NMDA receptor antagonism. Eur J Neurosci 18: 1706-1710.
37. Harrison PJ, Weinberger DR (2005). Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 10: 40-68.
38. Hashimoto T, Volk DW, Eggan SM, Mirnics K, Pierri JN, Sun Z et al (2003). Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci 23: 6315-6326.
39. Hayes NL, Nowakowski RS (2000). Exploiting the dynamics of S-phase tracers in developing brain: interkinetic nuclear migration for cells entering versus leaving the S-phase. Dev Neurosci 22: 44-55.
40. Hayes NL, Nowakowski RS (2002). Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice. Dev Brain Res 134: 77-85.
41. Heckers S (2001). Neuroimaging studies of the hippocampus in schizophrenia. Hippocampus 11: 520-528.
42. Heckers S, Heinsen H, Geiger B, Beckmann H (1991). Hippocampal neuron number in schizophrenia. A stereological study. Arch Gen Psychiatry 48: 1002-1008.
43. Hof PR, Glezer II, Conde F, Flagg RA, Rubin MB, Nimchinsky EA et al (1999). Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat 16: 77-116.
44. D-aspartate receptors and ethanol: inhibition of calcium flux and cyclic GMP production. J Neurochem 52: 1937-1940.
45. Ikonomidou C, Bittigau P, Ishimaru M, Wozniak DF, Koch C, Genz K et al (2000). Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 287: 1056-1060.
46. Ikonomidou C, Bosch F, Miksa M, Bittigau P, Vockler J, Dikranian K et al (1999). Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283: 70-74.
47. Jakob H, Beckmann H (1986). Prenatal developmental disturbances in the limbic allocortex in schizophrenics. J Neural Transm 65: 303-326.
48. Javitt DC, Zukin SR (1991). Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 148: 1301-1308.
49. Keilhoff G, Becker A, Grecksch G, Wolf G, Bernstein HG (2004). Repeated application of ketamine to rats induces changes in the hippocampal expression of parvalbumin, neuronal nitric oxide synthase and cFOS similar to those found in human schizophrenia. Neuroscience 126: 591-598.
50. Komitova M, Perfilieva E, Mattsson B, Eriksson PS, Johansson BB (2002). Effects of cortical ischemia and postischemic environmental enrichment on hippocampal cell genesis and differentiation in the adult rat. J Cereb Blood Flow Metab 22: 852-860.
51. Konick LC, Friedman L (2001). Meta-analysis of thalamic size in schizophrenia. Biol Psychiatry 49: 28-38.
52. Kovalenko S, Bergmann A, Schneider-Axmann T, Ovary I, Majtenyi K, Havas L et al (2004). Regio entorhinalis in schizophrenia: more evidence for migrational disturbances and suggestions for a new biological hypothesis. Pharmacopsychiatry 36(Suppl 3): S158-S161.
53. Kriss JP, Maruyama Y, Tung LA, Bond SB, Revesz L (1963). The fate of 5-bromodeoxyuridine, 5-bromodeoxycytidine, and 5-iododeoxycytidine in man. Cancer Res 23: 260-268.
54. Lawrie SM, Abukmeil SS (1998). Brain abnormality in schizophrenia - a systematic and quantitative review of volumetric magnetic resonance imaging studies. Br J Psychiatry 172: 110-120.
55. Lewis DA (2000). GABAergic local circuit neurons and prefrontal dysfunction in schizophrenia. Brain Res Rev 31: 270-276.
56. Lewis DA, Cruz DA, Melchitzky DS, Pierri JN (2001). Lamina-specific deficits in parvalbuminimmunoreactive varicosities in the prefrontal cortex of subjects with schizophrenia: evidence for fewer projections from the thalamus. Am J Psychiatry 158: 1411-1422.
57. Lewis DA, Gonzalez-Burgos G (2006). Pathophysiologically based treatment interventions in schizophrenia. Nat Med 12: 1016-1022.
58. Lewis DA, Hashimoto T, Volk DW (2005). Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6: 312-324.
59. Lovinger DM, White G, Weight FF (1989). Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 243: 1721-1724.
60. 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.
61. Lynch TP, Cass CE, Paterson AR (1977). Defective transport of thymidine by cultured cells resistant to 5-bromodeoxyuridine. J Supramol Struct 6: 363-374.
62. Miller MW, Nowakowski RS (1988). Use of bromodeoxyuridine- immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res 457: 44-52.
63. Nelson MD, Saykin AJ, Flashman LA, Riordan HJ (1998). Hippocampal volume reduction in schizophrenia as assessed by magnetic resonance imaging: a meta-analytic study. Arch Gen Psychiatry 55: 433-440.
64. Olney JW, Tenkova T, Dikranian K, Muglia LJ, Jermakowicz WJ, D'Sa C et al (2002). Ethanol-induced caspase-3 activation in the in vivo developing mouse brain. Neurobiol Dis 9: 205-219.
65. Packard Jr DS, Menzies RA, Skalko RG (1973). Incorporation of thymidine and its analogue, bromodeoxyuridine, into embryos and maternal tissues of the mouse. Differentiation 1: 397-404.
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 (1993). Total nerve cell number in neocortex in chronic schizophrenics and controls estimated using optical disectors. Biol Psychiatry 34: 768-772.
68. Palmer TD, Willhoite AR, Gage FH (2000). Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425: 479-494.
69. Pantelis C, Velakoulis D, McGorry PD, Wood SJ, Suckling J, Phillips LJ et al (2003). Neuroanatomical abnormalities before and after onset of psychosis: a cross-sectional and longitudinal MRI comparison. Lancet 361: 281-288.
70. Paxinos G, Tork I, Tecott LH, Valentino KL (1994). Atlas of the Developing Rat Brain, 2nd edn. Academic Press: New York, USA.
71. Paxinos G, Watson C (2007). The Rat Brain in Stereotaxic Coordinates, 6th edn. Academic Press, Inc.: San Diego, California, USA.
72. Pearlson GD, Marsh L (1999). Structural brain imaging in schizophrenia: a selective review. Biol Psychiatry 46: 627-649.
73. Popken GJ, Bunney Jr WE, Potkin SG, Jones EG (2000). Subnucleusspecific loss of neurons in medial thalamus of schizophrenics. Proc Natl Acad Sci USA 97: 9276-9280.
74. Powell CM, Miyakawa T (2006). Schizophrenia-relevant behavioral testing in rodent models: a uniquely human disorder? Biol Psychiatry 59: 1198-1207.
75. Reynolds GP, Abdul-Monim Z, Neill JC, Zhang ZJ (2004). Calcium binding protein markers of GABA deficits in schizophrenia - postmortem studies and animal models. Neurotox Res 6: 57-61.
76. Reynolds GP, Beasley CL (2001). GABAergic neuronal subtypes in the human frontal cortex - development and deficits in schizophrenia. J Chem Neuroanat 22: 95-100.
77. Reynolds GP, Beasley CL, Zhang ZJ (2002). Understanding the neurotransmitter pathology of schizophrenia: selective deficits of subtypes of cortical GABAergic neurons. J Neural Transm 109: 881-889.
78. Reynolds GP, Zhang ZJ, Beasley CL (2001). Neurochemical correlates of cortical GABAergic deficits in schizophrenia: selective losses of calcium binding protein immunoreactivity. Brain Res Bull 55: 579-584.
79. D-aspartate receptor hypofunction: molecular, cellular, functional and behavioral abnormalities. Biol Psychiatry 59: 721-729.
80. Sadikot AF, Burhan AM, Bélanger MC, Sasseville R (1998). NMDA receptor antagonists influence early development of GABAergic interneurons in the mammalian striatum. Brain Res Dev Brain Res 105: 35-42.
81. Sánchez MP, Frassoni C, Alvarez-Bolado G, Spreafico R, Fairén A (1992). Distribution of calbindin and parvalbumin in the developing somatosensory cortex and its primordium in the rat: an immunocytochemical study. J Neurocytol 21: 717-736.
82. Scallet AC, Schmued LC, Slikker W, Grunberg N, Faustino PJ, Davis H et al (2004). Developmental neurotoxicity of ketamine: morphometric confirmation, exposure parameters, and multiple fluorescent labeling of apoptotic neurons. Toxicol Sci 81: 364-370.
83. Selemon LD, Goldman-Rakic PS (1999). The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biol Psychiatry 45: 17-25.
84. Shenton ME, Dickey CC, Frumin M, McCarley RW (2001). A review of MRI findings in schizophrenia. Schizophr Res 49: 1-52.
85. Sherwood NM, Timiras PS (1970). A Stereotaxic Atlas of the Developing Rat Brain. University of California Press: Berkeley, CA, USA.
86. Solbach S, Celio MR (1991). Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anat Embryol (Berl) 184: 103-124.
87. Spector R, Berlinger WG (1982). Localization and mechanism of thymidine transport in the central nervous system. J Neurochem 39: 837-841.
88. Steen RG, Mull C, McClure R, Hamer RM, Lieberman JA (2006). Brain volume in first-episode schizophrenia: systematic review and meta-analysis of magnetic resonance imaging studies. Br J Psychiatry 188: 510-518.
89. D-aspartate receptor antagonists and their prevention by insulin-like growth factor I. J Neurochem 73: 548-556.
90. Takahashi T, Nowakowski RS, Caviness Jr VS (1992). BUdR as an S-phase marker for quantitative studies of cytokinetic behaviour in the murine cerebral ventricular zone. J Neurocytol 21: 185-197.
91. Takahashi T, Nowakowski RS, Caviness Jr VS (1995). The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15: 6046-6057.
92. Taupin P (2007). BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res Rev 53: 198-214.
93. Thomas née Williams SA, Segal MB (1996). Identification of a saturable uptake system for deoxyribonucleosides at the blood-brain and blood-cerebrospinal fluid barriers. Brain Res 741: 230-239.
94. Thomas SA, Davson H, Segal MB (1997). Quantification of efflux into the blood and brain of intraventricularly perfused [3H]-thymidine in the anaesthetized rabbit. Exp Physiol 82: 139-148.
95. Thompson PM, Vidal C, Giedd JN, Gochman P, Blumenthal J, Nicolson R et al (2001). Mapping adolescent brain change reveals dynamic wave of accelerated gray matter loss in very early-onset schizophrenia. Proc Natl Acad Sci USA 98: 11650-11655.
96. Turner CP, Miller R, Smith C, Brown L, Blackstone K, Dunham SR et al (2007). Widespread neonatal brain damage following calcium channel blockade. Dev Neurosci 29: 213-231.
97. Turner CP, Pulciani D, Rivkees SA (2002). Reduction in intracellular calcium levels induces injury in developing neurons. Exp Neurol 178: 21-32.
98. Walker MA, Highley JR, Esiri MM, McDonald B, Roberts HC, Evans SP et al (2002). Estimated neuronal populations and volumes of the hippocampus and its subfields in schizophrenia. Am J Psychiatry 159: 821-828.
99. Wang CZ, Johnson KM (2005). Differential effects of acute and subchronic administration on phencyclidine-induced neurodegeneration in the postnatal rat. J Neurosci Res 81: 284-292.
100. Wang CZ, Johnson KM (2007). The role of caspase-3 activation in phencyclidine-induced neuronal death in postnatal rats. Neuropsychopharmacology 32: 1178-1194.
101. West MJ (1993). New stereological methods for counting neurons. Neurobiol Aging 14: 275-285.
102. Wheeler DG, Dixon G, Harper CG (2006). No differences in calcium-binding protein immunoreactivity in the posterior cingulate and visual cortex: schizophrenia and controls. Prog Neuropsychopharmacol Biol Psychiatry 30: 630-639.
103. Woo TU, Miller JL, Lewis DA (1997). Schizophrenia and the parvalbumin-containing class of cortical local circuit neurons. Am J Psychiatry 154: 1013-1015.
104. Woo TU, Whitehead RE, Melchitzky DS, Lewis DA (1998). A subclass of prefrontal gamma-aminobutyric acid axon terminals are selectively altered in schizophrenia. Proc Natl Acad Sci USA 95: 5341-5346.
105. Wozniak DF, Hartman RE, Boyle MP, Vogt SK, Brooks AR, Tenkova T et al (2004). Apoptotic neurodegeneration induced by ethanol in neonatal mice is associated with profound learning/memory deficits in juveniles followed by progressive functional recovery in adults. Neurobiol Dis 17: 403-414.
106. Wright IC, Rabe-Hesketh S, Woodruff PWR, David AS, Murray RM, Bullmore ET (2000). Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 157: 16-25.
107. Yoon WJ, Won SJ, Ryu BR, Gwag BJ (2003). Blockade of ionotropic glutamate receptors produces neuronal apoptosis through the Bax-cytochrome C-caspase pathway: the causative role of Ca2+ deficiency. J Neurochem 85: 525-533.
108. Young C, Jevtovic-Todorovic V, Qin YQ, Tenkova T, Wang H, Labruyere J et al (2005). Potential of ketamine and midazolam, individually or in combination, to induce apoptotic neurodegeneration in the infant mouse brain. Br J Pharmacol 146: 189-197.
109. Young KA, Manaye KF, Liang CL, Hicks PB, German DC (2000). Reduced number of mediodorsal and anterior thalamic neurons in schizophrenia. Biol Psychiatry 47: 944-953.
110. Zhang ZJ, Reynolds GP (2002). A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schiz Res 55: 1-10.