The neurodevelopmental hypothesis of schizophrenia: A review of recent developments

Annals of Medicine

Volumn 35, Issue 2, 2003, Pages 86-93

  McGrath, John J ^a   Féron, François P ^a,b   Burne, Thomas H J ^a,b   Mackay Sim, Alan ^b   Eyles, Darryl W ^a  

^a The Park Centre for Mental Health   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

Author keywords

Brain growth and development; Prenatal exposures; Schizophrenia

Indexed keywords

ANIMAL MODEL; BRAIN DEVELOPMENT; BRAIN DISEASE; BRAIN GROWTH; BRAIN SIZE; CLINICAL TRIAL; DIAGNOSTIC IMAGING; HUMAN; HYPOTHESIS; LIFE EVENT; LIFESPAN; META ANALYSIS; NERVE DEGENERATION; NEUROIMAGING; NEUROPATHOLOGY; ONSET AGE; PRENATAL EXPOSURE; PRIORITY JOURNAL; PSYCHOSIS; REVIEW; SCHIZOPHRENIA;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; HUMANS; SCHIZOPHRENIA; TREATMENT OUTCOME;

EID: 0038779583     PISSN: 07853890     EISSN: None     Source Type: Journal    
DOI: 10.1080/07853890310010005     Document Type: Review

References (71)

1. Evans K, McGrath J, Milns R. Searching for schizophrenia in ancient Greek and Roman literature: a systematic review. Acta Psychiatr Scand (in press).
2. Lewis SW. Congenital risk factors for schizophrenia. Psychol Med 1989; 19: 5-13.
3. Clouston TS. The neuroses of development; being the Morison Lectures for 1890. Edinburgh: Oliver and Boyd; 1891.
4. Southard EE. On the topographical distribution of cortex lesions and anomalies in dementia praecox, with some account of their functional significance. American Journal of Insanity 1915; 71: 603-71.
5. Kraepelin E. Dementia praecox and paraphrenia (Translated by R. M. Barclay). Edinburgh: Livingstone; 1919.
6. Bleuler E. Dementia praecox: or the group of schizophrenias (Translated by J. Zinkin). New York: International Universities Press; 1911.
7. Feinberg I. Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence? J Psychiatr Res 1982; 17: 319-34.
8. Weinberger DR. Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen Psychiatry 1987; 44: 660-9.
9. Murray RM, Lewis SW. Is schizophrenia a neurodevelopmental disorder? BMJ (Clin Res Ed) 1987; 295: 681-2.
10. Marenco S, Weinberger DR. The neurodevelopmental hypothesis of schizophrenia: following a trail of evidence from cradle to grave. Dev Psychopathol 2000; 12: 501-27.
11. Parnas J, Schulsinger F, Teasdale TW, Schulsinger H, Feldman PM, Mednick SA. Perinatal complications and clinical outcome within the schizophrenia spectrum. Br J Psychiatry 1982; 140: 416-20.
12. Murray RM, Lewis SW, Owen MJ, Foerster A. The neurodevelopmental origins of dementia praecox. In: Bebbington P, McGuffin P, eds. Schizophrenia: The major issues. London: Heinemann; 1988: 90-106.
13. McGrath JJ, Murray RM. Risk factors for schizophrenia: from conception to birth. In: Weinberger DR, Hirsch SR, eds. Schizophrenia. Oxford: Blackwells; 1994.
14. Bradbury TN, Miller GA. Season of birth in schizophrenia: A review of evidence, methodology, and etiology. Psychol Bull 1985; 98: 569-94.
15. Mortensen PB, Pedersen CB, Westergaard T, Wohlfahrt J, Ewald H, Mors O, et al. Effects of family history and place and season of birth on the risk of schizophrenia. N Engl J Med 1999; 340: 603-8.
16. McGrath J, Castle D. Does influenza cause schizophrenia? A five year review. Aust N Z J Psychiatry 1995; 29: 23-31.
17. McGrath J. Hypothesis: is low prenatal vitamin D a risk-modifying factor for schizophrenia? Schizophr Res 1999; 40: 173-7.
18. Cannon M, Jones PB, Murray RM. Obstetric complications and schizophrenia: historical and meta-analytic review. Am J Psychiatry 2002; 159: 1080-92.
19. Brown AS, Susser ES. In utero infection and adult schizophrenia. Ment Retard Dev Disabil Res Rev 2002; 8: 51-7.
20. Palmer CG, Turunen JA, Sinsheimer JS, Minassian S, Paunio T, Lonnqvist J, et al. RHD Maternal-Fetal Genotype Incompatibility Increases Schizophrenia Susceptibility. Am J Hum Genet 2002; 71: 1312-9.
21. Susser E, Neugebauer R, Hoek H, Brown AS, Lin S, Labovitz D, et al. Schizophrenia after prenatal famine: further evidence. Arch Gen Psychiatry 1996; 53: 25-31.
22. McDonald C, Murray RM. Early and late environmental risk factors for schizophrenia. Brain Res Brain Res Rev 2000; 31: 130-7.
23. Jones PB. Schizophrenia: social and environmental factors: implications for aetiology. Curr Opin Psychiatry 2001; 14: 39-43.
24. Tarrant CJ, Jones PB. Precursors to schizophrenia: do biological markers have specificity? Can J Psychiatry 1999; 44: 335-49.
25. Davies N, Russell A, Jones P, Murray RM. Which characteristics of schizophrenia predate psychosis? J Psychiatr Res 1998; 32: 121-31.
26. McCarley RW, Wible CG, Frumin M, Hirayasu Y, Levitt JJ, Fischer IA, et al. MRI anatomy of schizophrenia. Biol Psychiatry 1999; 45: 1099-119.
27. Wright IC, Rabe-Hesketh S, Woodruff PW, David AS, Murray RM, Bullmore ET. Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 2000; 157: 16-25.
28. Bloom FE. Advancing a neurodevelopmental origin for schizophrenia. Arch Gen Psychiatry 1993; 50: 224-7.
29. Harrison PJ. The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 1999; 122: 593-624.
30. Stefansson H, Sarginson J, Kong A, Yates P, Steinthorsdottir V, Gudfinnsson E, et al. Association of neuregulin 1 with schizophrenia confirmed in a Scottish population. Am J Hum Genet 2003; 72: 83-7.
31. Stefansson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Ghosh S, et al. Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 2002; 71: 877-92.
32. Straub RE, Jiang Y, MacLean CJ, Ma Y, Webb BT, Myakishev MV, et al. Genetic variation in the 6p22.3 gene DTNBP1, the human ortholog of the mouse dybindin gene, is associated with schizophrenia. Am J Hum Genet 2002; 71: 337-48.
33. Schwab SG, Knapp M, Mondabon S, Hallmayer J, Borrman-Hassenbach M, Albus M, et al. Support for associatior of schizophrenia with genetic variation in the 6p22.3 gene, dysbindin, in sib-pair families with linkage and in an additional sample of triad families. Am J Hum Genet 2003; 72:185-90.
34. Jones P, Murray RM. The genetics of schizophrenia is the genetics of neurodevelopment. Br J Psychiatry 1991; 158: 615-23.
35. Razi K, Greene KP, Sakuma M, Ge S, Kushner M, DeLisi LE. Reduction of the parahippocampal gyrus and the hippocampus in patients with chronic schizophrenia [see comments]. Br J Psychiatry 1999; 174: 512-9.
36. DeLisi LE. Regional brain volume change over the life-time course of schizophrenia. J Psychiatr Res 1999; 33: 535-41.
37. DeLisi LE. Is schizophrenia a lifetime disorder of brain plasticity, growth and aging? Schizophr Res 1997; 23: 119-29.
38. Velakoulis D, Pantelis C, McGorry PD, Dudgeon P, Brewer W, Cook M, et al. Hippocampal volume in first-episode psychoses and chronic schizophrenia: a high-resolution magnetic resonance imaging study [see comments]. Arch Gen Psychiatry 1999; 56: 133-41.
39. Keller A, Castellanos FX, Vaituzis AC, Jeffries NO, Giedd JN, Rapoport JL. Progressive loss of cerebellar volume in childhood-onset schizophrenia. Am J Psychiatry 2003; 160: 128-33.
40. Kasai K, Shenton ME, Salisbury DF, Hirayasu Y, Lee CU, Ciszewski AA, et al. Progressive decrease of left superior temporal gyrus gray matter volume in patients with first-episode schizophrenia. Am J Psychiatry 2003; 160: 156-64.
41. Harvey PD, Lombardi J, Kincaid MM, Parrella M, White L, Powchik P, et al. Cognitive functioning in chronically hospitalized schizophrenic patients: age-related changes and age disorientation as a predictor of impairment. Schizophr Res 1995; 17: 15-24.
42. McGorry PD, Jackson HJ. The recognition and management of early psychosis: a preventive approach. Cambridge: Cambridge University Press; 1999.
43. McGrath J, McGlashan TH. Improving outcomes for recent-onset psychoses: disentangling hope, speculation and evidence. Acta Psychiatr Scand 1999; 100: 83-4.
44. Lieberma JA. Is schizophrenia a neurodegenerative disorder? A clinical and neurobiological perspective. Biol Psychiatry 1999; 46: 729-39.
45. Lieberman JA, Perkins D, Belger A, Chakos M, Jarskog F, Boteva K, et al. The early stages of schizophrenia: speculations on pathogenesis, pathophysiology, and therapeutic approaches. Biol Psychiatry 2001; 50: 884-97.
46. Weinberger DR, McClure RK. Neurotoxicity, neuroplasticity, and magnetic resonance imaging morphometry: what is happening in the schizophrenic brain? Arch Gen Psychiatry 2002; 59: 553-8.
47. Woods BT. Is schizophrenia a progressive neurodevelopmental disorder? Toward a unitary pathogenetic mechanism. Am J Psychiatry 1998; 155: 1661-70.
48. Williams NM, O' Donovan MC, Owen MJ. Genome scans and microarrays: converging on genes for schizophrenia? Genome Biol 2002; 3: Reviews 1011.
49. Thompson PM, Vidal C, Giedd JN, Gochman P, Blumenthal J, Nicolson R, et al. Mapping adolescent brain change reveals dynamic wave of accelerated gray matter loss in very early-onset schizophrenia. Proc Natl Acad Sci U S A 2001; 98: 11650-5.
50. Moises HW, Zoega T, Gottesman II. The glial growth factors deficiency and synaptic destabilization hypothesis of schizophrenia. BMC Psychiatry 2002; 2: 8 http://www. biomedcentral.com/1471-244X/2/8.
51. Lawrie SM, Whalley HC, Abukmeil SS, Kestelman JN, Miller P, Best JJ, et al. Temporal lobe volume changes in people at high risk of schizophrenia with psychotic symptoms. Br J Psychiatry 2002; 181: 138-43.
52. Pearce BD. Schizophrenia and viral infection during neurodevelopment: a focus on mechanisms. Mol Psychiatry 2001; 6: 634-46.
53. Torrey EF, Peterson MR. Slow and latent viruses in schizophrenia. Lancet 1973; 2: 22-4.
54. Feinberg I. Cortical pruning and the development of schizophrenia. Schizophr Bull 1990; 16: 567-70.
55. Zammit S, Allebeck P, Andreasson S, Lundberg I, Lewis G. Self reported cannabis use as a risk factor for schizophrenia in Swedish conscripts of 1969: historical cohort study. BMJ 2002; 325: 1199.
56. Keshavan MS. Development, disease and degeneration in schizophrenia: a unitary pathophysiological model. J Psychiatr Res 1999; 33: 513-21.
57. Feinberg I. Neurodevelopmental models of mental illness. Clin Genet 1990; 37: 491-2.
58. Keshavan MS, Anderson S, Pettegrew JW. Is schizophrenia due to excessive synaptic pruning in the prefrontal cortex? The Feinberg hypothesis revisited. J Psychiatr Res 1994; 28: 239-65.
59. Selemon LD, Goldman-Rakic PS. The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biol Psychiatry 1999; 45: 17-25.
60. Rajkowska G, Selemon LD, Goldman-Rakic PS. Neuronal and glial somal size in the prefrontal cortex: a postmortem morphometric study of schizophrenia and Huntington disease. Arch Gen Psychiatry 1998; 55: 215-24.
61. Selemon LD, Rajkowska G, Goldman-Rakic PS. Abnormally high neuronal density in the schizophrenic cortex. A morphometric analysis of prefrontal area 9 and occipital area 17. Arch Gen Psychiatry 1995; 52:805-18 [see discussion 819-20].
62. Mirnics K, Middleton FA, Lewis DA, Levitt P. Analysis of complex brain disorders with gene expression microarrays: schizophrenia as a disease of the synapse. Trends Neurosci 2001; 24:479-86.
63. Hogarty GE, Flesher S. Developmental theory for a cognitive enhancement therapy of schizophrenia. Schizophr Bull 1999; 25: 677-92.
64. Keshavan MS, Hogarty GE. Brain maturational processes and delayed onset in schizophrenia. Dev Psychopathol 1999; 11: 525-43.
65. McDonald C, Fearon P, Murray RM. Neurodevelopmental hypothesis of schizophrenia 12 years on: data and doubts. In: Rapopart J, ed. Childhood onset of adult psychopathology. Washington (DC): American Psychiatric Press; 1999.
66. Lipska BK, Swerdlow NR, Geyer MA, Jaskiw GE, Braff DL, Weinberger DR. Neonatal excitotoxic hippocampal damage in rats causes post-pubertal changes in prepulse inhibition of startle and its disruption by apomorphine. Psychopharmacology (Berl) 1995; 122: 35-43.
67. Lipska BK, Jaskiw GE, Chrapusta S, Karoum F, Weinberger DR. Ibotenic acid lesion of the ventral hippocampus differentially affects dopamine and its metabolites in the nucleus accumbens and prefrontal cortex in the rat. Brain Res 1992; 585: 1-6.
68. Fatemi SH, Cuadra AE, El Fakahany EE, Sidwell RW, Thuras P. Prenatal viral infection causes alterations in nNOS expression in developing mouse brains. Neuroreport 2000; 11: 1493-6.
69. Fatemi SH, Emamian ES, Kist D, Sidwell RW, Nakajima K, Akhter P, et al. Defective corticogenesis and reduction in Reelin immunoreactivity in cortex and hippocampus of prenatally infected neonatal mice. Mol Psychiatry 1999; 4: 145-54.
70. Hornig M, Weissenbock H, Horscroft N, Lipkin WI. An infection-based model of neurodevelopmental damage. Proc Natl Acad Sci USA 1999; 96: 12102-7.
71. Mallard EC, Rehn A, Rees S, Tolcos M, Copolov D. Ventriculomegaly and reduced hippocampal volume following intrauterine growth-restriction: implications for the aetiology of schizophrenia. Schizophr Res 1999; 40: 11-21.