The neuropathology of schizophrenia: Central role for the hippocampus?

Advances in Schizophrenia Research 2009

Volumn , Issue , 2010, Pages 149-165

  Falkai, Peter ^a   Parlapani, Eleni ^a   Gruber, Oliver ^a   Schmitt, Andrea ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84874515653     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4419-0913-8_7     Document Type: Chapter

References (118)

1. Adams, W., Kendell, R.E., Hare, E.H., & Munk-Jorgensen, P. (1993) Epidemiological evidence that maternal influenza contributes to the aetiology of schizophrenia. An analysis of Scottish, English, and Danish data. Br J Psychiatry 163: 522-534 (Pubitemid 23297472)
2. Akbarian, S., Bunney, W.E. JR., Potkin, S.G., Wigal, S.B., Hagman, J.O., Sandman, C.A., & Jones, E.G. (1993a) Altered distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase cells in frontal lobe of schizophrenics implies disturbances of cortical development. Arch Gen Psychiatry 50: 169-177 (Pubitemid 23077471)
3. Akbarian, S., Vinuela, A., Kim, J.J., Potkin, S.G., Bunney, W.E. Jr., & Jones, E.G. (1993b) Distorted distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase neurons in temporal lobe of schizophrenics implies anomalous cortical development. Arch Gen Psychiatry 50: 178-187 (Pubitemid 23077472)
4. Andreasen, N.C. (1999) A unitary model of schizophrenia: Bleuler's "fragmented phrene" as schizencephaly. Arch Gen Psychiatry 56: 781-78
5. Arnold, S.E. (1997) The medial temporal lobe in schizophrenia. J Neuropsychiatry Clin Neurosci 9: 460-470 (Pubitemid 27363949)
6. Arnold, S.E., Franz, B.R., Gur, R.C., Gur, R.E., Shapiro, R.M., Moberg, P.J., & Trojanowski, J.Q. (1995) Smaller neuron size in schizophrenia in hippocampal subfields that mediate cortical-hippocampal interactions. Am J Psychiatry 152: 738-748
7. Arnold, S.E., Lee, V.M., Gur, R.E., & Trojanowski, J.Q. (1991) Abnormal expression of two microtubule-associated proteins (MAP2 and MAP5) in specific subfields of the hippocampal formation in schizophrenia. Proc Natl Acad Sci USA 88: 10850-10854 (Pubitemid 21915936)
8. Aston, C., Jiang, L., & Sokolov, B.P. (2004) Microarray analysis of postmortem temporal cortex from patients with schizophrenia. J Neurosci Res 77: 858-866 (Pubitemid 39187068)
9. Aylward, E., Walker, E., & Bettes, B. (1984) Intelligence in schizophrenia: meta-analysis of the research. Schizophr Bull 10: 430-459
10. Baldessarini, R.J., Hegarty, J.D., Bird, E.D., & Benes, F.M. (1997) Meta-analysis of postmortem studies of Alzheimer's disease-like neuropathology in schizophrenia. Am J Psychiatry 154: 861-863 (Pubitemid 27230114)
11. Becker, A., Grecksch, G., Bernstein, H.G., Hollt, V., & Bogerts, B. (1999) Social behaviour in rats lesioned with ibotenic acid in the hippocampus: quantitative and qualitative analysis. Psychopharmacology (Berl) 144: 333-338 (Pubitemid 29307257)
12. Benes, F.M. (1989) Myelination of cortical-hippocampal relays during late adolescence. Schizophr Bull 15: 585-593 (Pubitemid 20066726)
13. Benes, F.M., Kwok, E.W., Vincent, S.L., & Todtenkopf, M.S. (1998) A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives. Biol Psychiatry 44: 88-97 (Pubitemid 28305527)
14. Benes, F.M., Mcsparren, J., Bird, E.D., Sangiovanni, J.P., & Vincent, S.L. (1991a) Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 48: 996-1001
15. Benes, F.M., Sorensen, I., & Bird, E.D. (1991b) Reduced neuronal size in posterior hippocampus of schizophrenic patients. Schizophr Bull 17: 597-608
16. Benes, F.M., Turtle, M., Khan, Y., & Farol, P. (1994) Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Arch Gen Psychiatry 51: 477-484 (Pubitemid 24180494)
17. Bernstein, H.G., Krell, D., Baumann, B., Danos, P., Falkai, P., Diekmann, S., Henning, H., & Bogerts, B. (1998) Morphometric studies of the entorhinal cortex in neuropsychiatric patients and controls: clusters of heterotopically displaced lamina II neurons are not indicative of schizophrenia. Schizophr Res 33: 125-132 (Pubitemid 28446536)
18. Bertolino, A., Saunders, R.C., Mattay, V.S., Bachevalier, J., Frank, J.A., & Weinberger, D.R. (1997) Altered development of prefrontal neurons in rhesus monkeys with neonatal mesial temporolimbic lesions: a proton magnetic resonance spectroscopic imaging study. Cereb Cortex 7: 740-748 (Pubitemid 27505810)
19. Bogerts, B., Ashtari, M., Degreef, G., Alvir, J.M., Bilder, R.M., & Lieberman, J.A. (1990) Reduced temporal limbic structure volumes on magnetic resonance images in first episode schizophrenia. Psychiatry Res 35: 1-13 (Pubitemid 20203211)
20. Bogerts, B., Meertz, E., & Schonfeldt-Bausch, R. (1985) Basal ganglia and limbic system pathology in schizophrenia. A morphometric study of brain volume and shrinkage. Arch Gen Psychiatry 42: 784-791 (Pubitemid 15244829)
21. Brown, A.S., Begg, M.D., Gravenstein, S., Schaefer, C.A., Wyatt, R.J., Bresnahan, M., Babulas, V.P., & Susser, E.S. (2004) Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch Gen Psychiatry 61: 774-780 (Pubitemid 39031117)
22. Brown, A.S., Susser, E.S., Butler, P.D., Richardson Andrews, R., Kaufmann, C.A., & Gorman, J.M. (1996) Neurobiological plausibility of prenatal nutritional deprivation as a risk factor for schizophrenia. J Nerv Ment Dis 184: 71-85 (Pubitemid 26092339)
23. Byne, W., Kidkardnee, S., Tatusov, A., Yiannoulos, G., Buchsbaum, M.S. & Haroutunian, V. (2006) Schizophrenia-associated reduction of neuronal and oligodendrocyte numbers in the anterior principal thalamic nucleus. Schizophr Res 85: 245-253 (Pubitemid 43947537)
24. Callicott, J.H., Egan, M.F., Bertolino, A., Mattay, V.S., Langheim, F.J., Frank, J.A., & Weinberger, D.R. (1998) Hippocampal N-acetyl aspartate in unaffected siblings of patients with schizophrenia: a possible intermediate neurobiological phenotype. Biol Psychiatry 44: 941-950 (Pubitemid 28545222)
25. Cannon, T.D., Kaprio, J., Lonnqvist, J., Huttunen, M., & Koskenvuo, M. (1998) The genetic epidemiology of schizophrenia in a Finnish twin cohort. A population-based modeling study. Arch Gen Psychiatry 55: 67-74 (Pubitemid 28069041)
26. Casanova, M.F., & Rothberg B. (2002) Shape distortion of the hippocampus: a possible explanation of the pyramidal cell disarray reported in schizophrenia. Schizophr Res 55: 19-24 (Pubitemid 34310533)
27. Chambers, R.A., Moore, J., Mcevoy, J.P., & Levin, E.D. (1996) Cognitive effects of neonatal hippocampal lesions in a rat model of schizophrenia. Neuropsychopharmacology 15: 587-594 (Pubitemid 26400763)
28. Chaudhury, A.R., Gerecke, K.M., Wyss, J.M., Morgan, D.G., Gordon, M.N., & Carroll, S.L. (2003) Neuregulin-1 and erbB4 immunoreactivity is associated with neuritic plaques in Alzheimer disease brain and in a transgenic model of Alzheimer disease. J Neuropathol Exp Neurol 62: 42-54 (Pubitemid 36068892)
29. Christison, G.W., Casanova, M.F., Weinberger, D.R., Rawlings, R., & Kleinman, J.E. (1989) A quantitative investigation of hippocampal pyramidal cell size, shape, and variability of orientation in schizophrenia. Arch Gen Psychiatry 46: 1027-1032 (Pubitemid 19278232)
30. Colter, N., Battal, S., Crow, T.J., Johnstone, E.C., Brown, R., & Bruton, C. (1987) White matter reduction in the parahippocampal gyrus of patients with schizophrenia. Arch Gen Psychiatry 44: 1023
31. Conrad, A.J., Abebe, T., Austin, R., Forsythe, S., & Scheibel, A.B. (1991) Hippocampal pyramidal cell disarray in schizophrenia as a bilateral phenomenon. Arch Gen Psychiatry 48: 413-417
32. Cotter, D., Kerwin, R., Doshi, B., Martin, C.S., & Everall, I.P. (1997) Alterations in hippocampal non-phosphorylated MAP2 protein expression in schizophrenia. Brain Res 765: 238-46 (Pubitemid 27397619)
33. Crow, T.J. (2007) How and why genetic linkage has not solved the problem of psychosis: review and hypothesis. Am J Psychiatry 164: 13-21 (Pubitemid 46154775)
34. Crow, T.J., Ball, J., Bloom, S. R., Brown, R., Bruton, C.J., Colter, N., Frith, C.D., Johnstone, E.C., Owens, D.G., & Roberts, G.W. (1989) Schizophrenia as an anomaly of development of cerebral asymmetry. A postmortem study and a proposal concerning the genetic basis of the disease. Arch Gen Psychiatry 46: 1145-1150 (Pubitemid 20016453)
35. Davis, K.L., Stewart, D.G., Friedman, J.I., Buchsbaum, M., Harvey, P.D., Hof, P.R., Buxbaum, J., & Haroutunian, V. (2003) White matter changes in schizophrenia: evidence for myelin-related dysfunction. Arch Gen Psychiatry 60: 443-456 (Pubitemid 36539053)
36. Dracheva, S., Davis, K.L., Chin, B., Woo, D.A., Schmeidler, J., & Haroutunian, V. (2006) Myelinassociated mRNA and protein expression deficits in the anterior cingulate cortex and hippocampus in elderly schizophrenia patients. Neurobiol Dis 21: 531-540 (Pubitemid 43277536)
37. Eyler, L.T., Jeste, D.V., & Brown, G.G. (2008) Brain response abnormalities during verbal learning among patients with schizophrenia. Psychiatry Res 162: 11-25 (Pubitemid 350299857)
38. Falkai, P., & Bogerts B. (1986) Cell loss in the hippocampus of schizophrenics. Eur Arch Psychiatry Neurol Sci 236: 154-161 (Pubitemid 17050518)
39. Falkai, P., Bogerts, B., Greve, B., Pfeiffer, U., Machus, B., Folsch-Reetz, B., Majtenyi, C., & Ovary, I. (1992) Loss of sylvian fissure asymmetry in schizophrenia. A quantitative post mortem study. Schizophr Res 7: 23-32
40. Falkai, P., Bogerts, B., & Rozumek, M. (1988) Limbic pathology in schizophrenia: the entorhinal region-a morphometric study. Biol Psychiatry 24: 515-521
41. Falkai, P., Honer, W.G., David, S., Bogerts, B., Majtenyi, C., & Bayer, T.A. (1999) No evidence for astrogliosis in brains of schizophrenic patients. A post-mortem study. Neuropathol Appl Neurobiol 25: 48-53 (Pubitemid 29121694)
42. Falkai, P., Schneider-Axmann, T., & Honer, W.G. (2000) Entorhinal cortex pre-alpha cell clusters in schizophrenia: quantitative evidence of a developmental abnormality. Biol Psychiatry 47: 937-943 (Pubitemid 30320738)
43. Falls, D.L. (2003) Neuregulins: functions, forms, and signaling strategies. Exp Cell Res 284: 14-30 (Pubitemid 36335807)
44. Friston, K.J., & Frith C.D. (1995) Schizophrenia: a disconnection syndrome? Clin Neurosci 3: 89-97
45. Gerecke, K.M., Wyss, J.M., & Carroll, S.L. (2004) Neuregulin-1beta induces neurite extension and arborization in cultured hippocampal neurons. Mol Cell Neurosci 27: 379-393 (Pubitemid 39539993)
46. Goldman-Rakic, P.S., Selemon, L.D., & Schwartz, M.L. (1984) Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience 12: 719-743 (Pubitemid 14092488)
47. Grecksch, G., Bernstein, H.G., Becker, A., Hollt, V., & Bogerts, B. (1999) Disruption of latent inhibition in rats with postnatal hippocampal lesions. Neuropsychopharmacology 20: 525-532 (Pubitemid 29189257)
48. Green, M.F., Satz, P., Gaier, D.J., Ganzell, S., & Kharabi, F. (1989) Minor physical anomalies in schizophrenia. Schizophr Bull 15: 91-99 (Pubitemid 19096075)
49. Gruber, O., Falkai, P., Schneider-Axmann, T., Schwab, S.G., Wagner, M., & Maier, W. (2008) Neuregulin-1 haplotype HAP(ICE) is associated with lower hippocampal volumes in schizophrenic patients and in non-affected family members. J Psychiatr Res 19: 19
50. Hakak, Y., Walker, J.R., Li, C., Wong, W.H., Davis, K.L., Buxbaum, J.D., Haroutunian, V., & Fienberg, A.A. (2001) Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc Natl Acad Sci USA 98: 4746-4751 (Pubitemid 32295047)
51. Hall, J., Whalley, H.C., Job, D.E., Baig, B.J., Mcintosh, A.M., Evans, K.L., Thomson, P.A., Porteous, D.J., Cunningham-Owens, D.G., Johnstone, E.C., & Lawrie, S.M. (2006) A neuregulin 1 variant associated with abnormal cortical function and psychotic symptoms. Nat Neurosci 9: 1477-1478 (Pubitemid 44862654)
52. Harrison, P.J., & Eastwood S.L. (2001) Neuropathological studies of synaptic connectivity in the hippocampal formation in schizophrenia. Hippocampus 11: 508-519 (Pubitemid 33100372)
53. Harrison, P.J., & Weinberger D.R. (2005) Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 10: 40-68 (Pubitemid 40139588)
54. Heckers, S., Heinsen, H., Geiger, B., & Beckmann, H. (1991) Hippocampal neuron number in schizophrenia. A stereological study. Arch Gen Psychiatry 48: 1002-1008
55. Highley, J.R., Walker, M.A., McDonald, B., Crow, T.J., & Esiri, M.M. (2003) Size of hippocampal pyramidal neurons in schizophrenia. Br J Psychiatry 183: 414-417 (Pubitemid 37357573)
56. Hirayasu, Y., Shenton, M.E., Salisbury, D.F., Dickey, C.C., Fischer, I.A., Mazzoni, P., Kisler, T., Arakaki, H., Kwon, J.S., Anderson, J.E., Yurgelun-Todd, D., Tohen, M., & Mccarley, R.W. (1998) Lower left temporal lobe MRI volumes in patients with first-episode schizophrenia compared with psychotic patients with first-episode affective disorder and normal subjects. Am J Psychiatry 155: 1384-1391 (Pubitemid 28471195)
57. Hof, P.R., Haroutunian, V., Copland, C., Davis, K.L., & Buxbaum, J.D. (2002) Molecular and cellular evidence for an oligodendrocyte abnormality in schizophrenia. Neurochem Res 27: 1193-1200 (Pubitemid 35316115)
58. Hong, L.E., Wonodi, I., Stine, O.C., Mitchell, B.D., Thaker, G.K. (2008) Evidence of missense mutations on the neuregulin 1 gene affecting function of prepulse inhibition. Biol Psychiatry 63: 17-23 (Pubitemid 350234892)
59. Jakob, H., & Beckmann H. (1986) Prenatal developmental disturbances in the limbic allocortex in schizophrenics. J Neural Transm 65: 303-326 (Pubitemid 16073151)
60. Jaskiw, G.E., Juliano, D. M., Goldberg, T.E., Hertzman, M., Urow-Hamell, E., & Weinberger, D.R. (1994) Cerebral ventricular enlargement in schizophreniform disorder does not progress. A seven year follow-up study. Schizophr Res 14: 23-28 (Pubitemid 24372780)
61. Jeste, D.V., & Lohr J.B. (1989) Hippocampal pathologic findings in schizophrenia. A morphometric study. Arch Gen Psychiatry 46: 1019-1024 (Pubitemid 19278231)
62. Jones, P., Rodgers, B., Murray, R., & Marmot, M. (1994) Child development risk factors for adult schizophrenia in the British 1946 birth cohort. Lancet 344: 1398-1402 (Pubitemid 24365314)
63. Kaplan, M.J., Lazoff, M., Kelly, K., Lukin, R., & Garver, D.L. (1990) Enlargement of cerebral third ventricle in psychotic patients with delayed response to neuroleptics. Biol Psychiatry 27: 205-214 (Pubitemid 20033768)
64. Katsel, P., Davis, K.L., & Haroutunian, V. (2005) Variations in myelin and oligodendrocyte-related gene expression across multiple brain regions in schizophrenia: a gene ontology study. Schizophr Res 79: 157-173 (Pubitemid 41457256)
65. Kovalenko, S., Bergmann, A., Schneider-Axmann, T., Ovary, I., Majtenyi, K., Havas, L., Honer, W.G., Bogerts, B., & Falkai, P. (2003) Regio entorhinalis in schizophrenia: more evidence for migrational disturbances and suggestions for a new biological hypothesis. Pharmacopsychiatry 36: S158-161 (Pubitemid 38088028)
66. Kovelman, J.A., & Scheibel A.B. (1984) A neurohistological correlate of schizophrenia. Biol Psychiatry 19: 1601-1621 (Pubitemid 15196107)
67. Kwon, O.B., Longart, M., Vullhorst, D., Hoffman, D.A., & Buonanno, A. (2005) Neuregulin-1 reverses long-term potentiation at CA1 hippocampal synapses. J Neurosci 25: 9378-9383 (Pubitemid 41464750)
68. Lane, A., Kinsella, A., Murphy, P., Byrne, M., Keenan, J., Colgan, K., Cassidy, B., Sheppard, N., Horgan, R., Waddington, J.L., Larkin, C., & O'callaghan, E. (1997) The anthropometric assessment of dysmorphic features in schizophrenia as an index of its developmental origins. Psychol Med 27: 1155-1164 (Pubitemid 27401837)
69. Law, A.J., Lipska, B.K., Weickert, C.S., Hyde, T.M., Straub, R.E., Hashimoto, R., Harrison, P.J., Kleinman, J.E., & Weinberger, D.R. (2006) Neuregulin 1 transcripts are differentially expressed in schizophrenia and regulated by 5' SNPs associated with the disease. Proc Natl Acad Sci USA 103: 6747-6752
70. Law, A.J., Shannon Weickert, C., Hyde, T.M., Kleinman, J.E., & Harrison, P.J. (2004a) Neuregulin-1 (NRG-1) mRNA and protein in the adult human brain. Neuroscience 127: 125-136 (Pubitemid 38829158)
71. Law, A.J., Weickert, C.S., Hyde, T.M., Kleinman, J.E., & Harrison, P.J. (2004b) Reduced spinophilin but not microtubule-associated protein 2 expression in the hippocampal formation in schizophrenia and mood disorders: molecular evidence for a pathology of dendritic spines. Am J Psychiatry 161: 1848-1855 (Pubitemid 39314679)
72. Le Pen, G., Gaudet, L., Mortas, P., Mory, R., & Moreau, J.L. (2002) Deficits in reward sensitivity in a neurodevelopmental rat model of schizophrenia. Psychopharmacology (Berl) 161: 434-441 (Pubitemid 34595796)
73. Li, D., Collier, D.A., & He, L. (2006) Meta-analysis shows strong positive association of the neuregulin 1 (NRG1) gene with schizophrenia. Hum Mol Genet 15: 1995-2002 (Pubitemid 43983273)
74. Lim, K.O., Ardekani, B.A., Nierenberg, J., Butler, P.D., Javitt, D.C., & Hoptman, M.J. (2006) Voxelwise correlational analyses of white matter integrity in multiple cognitive domains in schizophrenia. Am J Psychiatry 163: 2008-2010 (Pubitemid 44807796)
75. Lipska, B.K. (2004) Using animal models to test a neurodevelopmental hypothesis of schizophrenia. J Psychiatry Neurosci 29: 282-286 (Pubitemid 39179574)
76. Lipska, B.K., Aultman, J.M., Verma, A., Weinberger, D.R., & Moghaddam, B. (2002a) Neonatal damage of the ventral hippocampus impairs working memory in the rat. Neuropsychopharma-cology 27: 47-54 (Pubitemid 34626742)
77. Lipska, B.K., Halim, N.D., Segal, P.N., & Weinberger, D.R. (2002b) Effects of reversible inactivation of the neonatal ventral hippocampus on behavior in the adult rat. J Neurosci 22: 2835-2842 (Pubitemid 37465832)
78. Lipska, B.K., Jaskiw, G.E., & Weinberger, D.R. (1993) Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: a potential animal model of schizophrenia. Neuropsychopharmacology 9: 67-75 (Pubitemid 23242602)
79. Lipska, B.K., Swerdlow, N.R., Geyer, M.A., Jaskiw, G.E., Braff, D.L., & Weinberger, D.R. (1995) Neonatal excitotoxic hippocampal damage in rats causes post-pubertal changes in prepulse inhibition of startle and its disruption by apomorphine. Psychopharmacology (Berl) 122: 35-43
80. Lipska, B.K., & Weinberger D.R. (2000) To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology 23: 223-239 (Pubitemid 30609657)
81. Maier, W., Zobel, A., & Rietschel, M. (2003) Genetics of schizophrenia and affective disorders. Pharmacopsychiatry 36: S195-202 (Pubitemid 38085137)
82. McNeil, T.F., Cantor-Graae, E., Nordstrom, L.G., & Rosenlund, T. (1993) Head circumference in "preschizophrenic" and control neonates. Br J Psychiatry 162: 517-523 (Pubitemid 23105925)
83. McNeil, T.F., Cantor-Graae, E., & Weinberger, D.R. (2000) Relationship of obstetric complications and differences in size of brain structures in monozygotic twin pairs discordant for schizophrenia. Am J Psychiatry 157: 203-212 (Pubitemid 30080899)
84. Munafo, M.R., Attwood, A.S., & Flint, J. (2008) Neuregulin 1 genotype and schizophrenia. Schizophr Bull 34: 9-12 (Pubitemid 350262294)
85. Munafo, M.R., Thiselton, D.L., Clark, T.G., & Flint, J. (2006) Association of the NRG1 gene and schizophrenia: a meta-analysis. Mol Psychiatry 11: 539-546
86. Nasrallah, H.A., Skinner, T.E., Schmalbrock, P., & Robitaille, P.M. (1994) Proton magnetic resonance spectroscopy (1H MRS) of the hippocampal formation in schizophrenia: a pilot study. Br J Psychiatry 165: 481-485 (Pubitemid 24305956)
87. Nordahl, T.E., Kusubov, N., Carter, C., Salamat, S., Cummings, A.M., O'SHORA-Celaya, L., Eberling, J., Robertson, L., Huesman, R.H., Jagust, W., & Budinger, T.F. (1996) Temporal lobe metabolic differences in medication-free outpatients with schizophrenia via the PET-600. Neuropsychopharmacology 15: 541-554 (Pubitemid 26412555)
88. Parlapani, E., Schmitt, A., Wirths, O., Bauer, M., Sommer, C., Rueb, U., Skowronek, M.H., Treutlein, J., Petroianu, G.A., Rietschel, M., & Falkai, P. (2008) Gene expression of neuregulin-1 isoforms in different brain regions of elderly schizophrenia patients. World J Biol Psychiatry 7: 1-8
89. Pegues, M.P., Rogers, L.J., Amend, D., Vinogradov, S., & Deicken, R.F. (2003) Anterior hippocampal volume reduction in male patients with schizophrenia. Schizophr Res 60: 105-115 (Pubitemid 36184704)
90. Rametti, G., Segarra, N., Junque, C., Bargallo, N., Caldu, X., Ibarretxe, N., & Bernardo, M. (2007) Left posterior hippocampal density reduction using VBM and stereological MRI procedures in schizophrenia. Schizophr Res 961-3: 62-71 (Pubitemid 47494623)
91. Rosoklija, G., Toomayan, G., Ellis, S.P., Keilp, J., Mann, J.J., Latov, N., Hays, A.P., & Dwork, A.J. (2000) Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch Gen Psychiatry 57: 349-356 (Pubitemid 30202325)
92. Sams-Dodd, F., Lipska, B.K., & Weinberger, D.R. (1997) Neonatal lesions of the rat ventral hippocampus result in hyperlocomotion and deficits in social behaviour in adulthood Psychopharmacology (Berl) 132: 303-310 (Pubitemid 27351432)
93. Saykin, A.J., Shtasel, D.L., Gur, R.E., Kester, D.B., Mozley, L.H., Stafiniak, P., & Gur, R.C. (1994) Neuropsychological deficits in neuroleptic naive patients with first-episode schizophrenia. Arch Gen Psychiatry 51: 124-131
94. Schmitt, A., Parlapani, E., Gruber, O., Wobrock, T., & Falkai, P. (2008a) Impact of neuregulin-1 on the pathophysiology of schizophrenia in human post-mortem studies. Eur Arch Psychiatry Clin Neurosci 258: 35-39
95. Schmitt, A., Steyskal, C., Bernstein, H.G., Schneider-Axmann, T., Parlapani, E., Schaeffer, E.L., Gattaz, W.F., Bogerts, B., Schmitz, C., & Falkai, P. (2008b) Stereologic investigation of the posterior part of the hippocampus in schizophrenia. Acta Neuropathol 6: 6
96. Seidman, L.J., Faraone, S.V., Goldstein, J.M., Kremen, W.S., Horton, N.J., Makris, N., Toomey, R., Kennedy, D., Caviness, V.S., & Tsuang, M.T. (2002) Left hippocampal volume as a vulnerability indicator for schizophrenia: a magnetic resonance imaging morphometric study of nonpsychotic first-degree relatives. Arch Gen Psychiatry 59: 839-849 (Pubitemid 35001150)
97. Shenton, M.E., Dickey, C.C., Frumin, M., & Mccarley, R.W. (2001) A review of MRI findings in schizophrenia. Schizophr Res 49: 1-52 (Pubitemid 32451739)
98. Stark, A.K., Uylings, H.B., Sanz-Arigita, E., & Pakkenberg, B. (2004) Glial cell loss in the anterior cingulate cortex, a subregion of the prefrontal cortex, in subjects with schizophrenia. Am J Psychiatry 161: 882-888 (Pubitemid 38625342)
99. Stefansson, H., Sigurdsson, E., Steinthorsdottir, V., Bjornsdottir, S., Sigmundsson, T., Ghosh, S., Brynjolfsson, J., Gunnarsdottir, S., Ivarsson, O., Chou, T.T., Hjaltason, O., et al. (2002) Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 71: 877-892 (Pubitemid 135750519)
100. Stevens, J.R. (1982) Neuropathology of schizophrenia. Arch Gen Psychiatry 39: 1131-1139 (Pubitemid 12034167)
101. Szeszko, P.R., Goldberg, E., Gunduz-Bruce, H., Ashtari, M., Robinson, D., Malhotra, A.K., Lencz, T., Bates, J., Crandall, D.T., Kane, J.M., & Bilder, R.M. (2003) Smaller anterior hippocampal formation volume in antipsychotic-naive patients with first-episode schizophrenia. Am J Psychiatry 160: 2190-2197 (Pubitemid 39619612)
102. Talamini, L.M., Meeter, M., Elvevag, B., Murre, J.M., & Goldberg, T.E. (2005) Reduced parahippocampal connectivity produces schizophrenia-like memory deficits in simulated neural circuits with reduced parahippocampal connectivity. Arch Gen Psychiatry 62: 485-493 (Pubitemid 40637223)
103. Tregellas, J.R., Tanabe, J.L., Miller, D.E., Ross, R.G., Olincy, A., & Freedman, R. (2004) Neurobiology of smooth pursuit eye movement deficits in schizophrenia: an fMRI study. Am J Psychiatry 161: 315-321 (Pubitemid 38419283)
104. Uranova, N.A., Vostrikov, V.M., Vikhreva, O.V., Zimina, I.S., Kolomeets, N.S., & Orlovskaya, D.D. (2007) The role of oligodendrocyte pathology in schizophrenia. Int J Neuropsychopharmacol 10: 537-545 (Pubitemid 46985262)
105. Van Erp, T.G., Saleh, P.A., Rosso, I.M., Huttunen, M., Lonnqvist, J., Pirkola, T., Salonen, O., Valanne, L., Poutanen, V.P., Standertskjold- Nordenstam, C.G., & Cannon, T.D. (2002) Contributions of genetic risk and fetal hypoxia to hippocampal volume in patients with schizophrenia or schizoaffective disorder, their unaffected siblings, and healthy unrelated volunteers. Am J Psychiatry 159: 1514-1520 (Pubitemid 35006731)
106. Velakoulis, D., Pantelis, C., Mcgorry, P.D., Dudgeon, P., Brewer, W., Cook, M., Desmond, P., Bridle, N., Tierney, P., Murrie, V., Singh, B., & Copolov, D. (1999) Hippocampal volume in firstepisode psychoses and chronic schizophrenia: a high-resolution magnetic resonance imaging study. Arch Gen Psychiatry 56: 133-141
107. Velakoulis, D., Stuart, G.W., Wood, S.J., Smith, D.J., Brewer, W.J., Desmond, P., Singh, B., Copolov, D., & Pantelis, C. (2001) Selective bilateral hippocampal volume loss in chronic schizophrenia. Biol Psychiatry 50: 531-539 (Pubitemid 32971884)
108. Walker, M.A., Highley, J.R., Esiri, M.M., Mcdonald, B., Roberts, H.C., Evans, S.P., & Crow, T.J. (2002) Estimated neuronal populations and volumes of the hippocampus and its subfields in schizophrenia. Am J Psychiatry 159: 821-828 (Pubitemid 34465057)
109. Wan, R.Q., Giovanni, A., Kafka, S.H., & Corbett, R. (1996) Neonatal hippocampal lesions induced hyperresponsiveness to amphetamine: behavioral and in vivo microdialysis studies. Behav Brain Res 78: 211-223 (Pubitemid 26252891)
110. Weinberger, D.R. (1996) On the plausibility of "the neurodevelopmental hypothesis" of schizophrenia. Neuropsychopharmacology 14: 1S-11S
111. Weinberger, D.R. (1999) Cell biology of the hippocampal formation in schizophrenia. Biol Psychiatry 45: 395-402 (Pubitemid 29130435)
112. Winterer, G., Konrad, A., Vucurevic, G., Musso, F., Stoeter, P., & Dahmen, N. (2008) Association of 5' end neuregulin-1 (NRG1) gene variation with subcortical medial frontal microstructure in humans. Neuroimage 40: 712-718
113. Wright, I.C., Rabe-Hesketh, S., Woodruff, P.W., David, A.S., Murray, R.M., & Bullmore, E.T. (2000) Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 157: 16-25 (Pubitemid 30027416)
114. Yamasue, H., Iwanami, A., Hirayasu, Y., Yamada, H., Abe, O., Kuroki, N., Fukuda, R., Tsujii, K., Aoki, S., Ohtomo, K., Kato, N., & Kasai, K. (2004) Localized volume reduction in prefrontal, temporolimbic, and paralimbic regions in schizophrenia: an MRI parcellation study. Psychiatry Res 131: 195-207 (Pubitemid 39311727)
115. Zaidel, D.W., Esiri, M.M., & Harrison, P.J. (1997a) The hippocampus in schizophrenia: lateralized increase in neuronal density and altered cytoarchitectural asymmetry. Psychol Med 27: 703-713 (Pubitemid 27216195)
116. Zaidel, D.W., Esiri, M.M., & Harrison, P.J. (1997b) Size, shape, and orientation of neurons in the left and right hippocampus: investigation of normal asymmetries and alterations in schizophrenia. Am J Psychiatry 154: 812-818 (Pubitemid 27230104)
117. Zhang, Z., Sun, J., & Reynolds, G.P. (2002) A selective reduction in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia patients. Chin Med J (Engl) 115: 819-823 (Pubitemid 34716389)
118. Zhou, Y., Shu, N., Liu, Y., Song, M., Hao, Y., Liu, H., Yu, C., Liu, Z., & Jiang, T. (2008) Altered resting-state functional connectivity and anatomical connectivity of hippocampus in schizophrenia. Schizophr Res 100: 120-132