The neurodevelopmental basis of schizophrenia: Clinical clues from cerebro-craniofacial dysmorphogenesis, and the roots of a lifetime trajectory of disease

Biological Psychiatry

Volumn 46, Issue 1, 1999, Pages 31-39

  Waddington, John L ^a,b   Lane, Abbie ^c,d   Larkin, Conall ^c,d   O'Callaghan, Eadbhard ^c  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b St Davnet's Hospital   (Ireland)

^c Cluain Mhuire Family Centre   (Ireland)

^d St John of God Hospitaller Services Ireland   (Ireland)

Author keywords

Course of illness; Dysmorphogenesis; Homogeneity; Neurodevelopment; Schizophrenia

Indexed keywords

HEAD INJURY; HUMAN; NERVE CELL DIFFERENTIATION; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; TERATOLOGY;

BRAIN; CHILD, PRESCHOOL; CRANIOSYNOSTOSES; DISEASE PROGRESSION; FETAL DISEASES; HUMANS; INFANT; INFANT, NEWBORN; MATERNAL WELFARE; SCHIZOPHRENIA;

EID: 0033029827     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3223(99)00055-4     Document Type: Review

References (82)

1. Akil M., Lewis D.A. Cytoarchitecture of the entorhinal cortex in schizophrenia. Am J Psychiatry. 154:1997;1010-1012.
2. Alexander R.C., Mukherjee S., Richter J., Kaufmann C.A. Minor physical anomalies in schizophrenia. J Nerv Ment Dis. 182:1994;639-644.
3. Andreasen N.C., O'Leary D.S., Cizadlo T., Arndt S., Rezai K., Boles Ponto L.L., et al. Schizophrenia and cognitive dysmetria a positron-emission tomography study of dysfunctional prefrontal-thalamic-cerebellar circuitry . Proc Natl Acad Sci USA. 93:1996;9985-9990.
4. Andreasen N.C., O'Leary D.S., Flaum M., Nopoulos P., Watkins G.L., Boles Ponto L.L., et al. Hypofrontality in schizophrenia distributed dysfunctional circuits in neuroleptic-naïve patients . Lancet. 349:1997;1730-1734.
5. Arnold S.E., Ruscheinsky D.D., Han L.Y. Further evidence of abnormal cytoarchitecture of the entorhinal cortex in schizophrenia using spatial point pattern analyses. Biol Psychiatry. 42:1997;639-647.
6. Arnold S.E., Trojanowski J.Q. Human fetal hippocampal development I. Cytoarchitecture, myeloarchitecture, and neuronal morphologic features . J Comp Neurol. 367:1996;274-292.
7. Arnold S.E., Trojanowski J.Q., Gur R.E., Blackwell P., Han L.Y., Choi C. Absence of neurodegeneration and neural injury in the cerebral cortex in a sample of elderly patients with schizophrenia. Arch Gen Psychiatry. 55:1998;225-232.
8. Benes F.M. Model generation and testing to probe neural circuitry in the cingulate cortex of postmortem schizophrenic brain. Schizophr Bull. 24:1998;219-230.
9. Bernstein H.G., Krell D., Baumann B., Danos P., Falkai P., Diekmann S., et al. 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. 33:1998;125-132.
10. Bilder R.M., Bogerts B., Ashtari M., Wu H., Alvir J.M., Jody D., et al. Anterior hippocampal volume reductions predict frontal lobe dysfunction in first episode schizophrenia. Schizophr Res. 17:1995;47-58.
11. Brown A.S., Susser E.S., Cohen P., Greenwald S. Schizophrenia following prenatal rubella exposure gestational timing and diagnostic specificity . Schizophr Res. 29:1998;17-18.
12. Buchanan R.W., Carpenter W.T. The neuroanatomies of schizophrenia. Schizophr Bull. 23:1997;367-372.
13. 1H-magnetic resonance spectroscopy of the left temporal and frontal lobes in schizophrenia clinical, neurodevelopmental, and cognitive correlates . Biol Psychiatry. 36:1994;792-800.
14. Cannon M., Jones P. Schizophrenia. J Neurol Neurosurg Psychiatry. 61:1996;604-613.
15. Clouston T.S. The Neuroses of Development. 1891;Oliver and Boyd, Edinburgh, UK.
16. Cohen S.R., Chen L., Trotman C.A., Burdi A.R. Soft-palate myogenesis a developmental field paradigm . Cleft Palate-Craniofac J. 30:1993;441-446.
17. Cotter D., Kerwin R., Al-Sarraji S., Brion J.P., Chadwich A., Lovestone S., et al. Abnormalities of Wnt signalling in schizophrenia - evidence for neurodevelopmental abnormality. NeuroReport. 9:1998;1379-1383.
18. Daniel D.G., Goldberg T.E., Gibbons R.D., Weinberger D.R. Lack of a bimodal distribution of ventricular size in schizophrenia a gaussian mixture analysis of 1056 cases and controls . Biol Psychiatry. 30:1991;887-903.
19. David A.S., Malmberg A., Brandt L., Allebeck P., Lewis G. IQ and schizophrenia a population-based cohort study . Psychol Med. 27:1997;1311-1323.
20. Degreef G., Ashtari M., Bogerts B., Bilder R.M., Jody D.N., Alvir J.M., et al. Volumes of ventricular system subdivisions measured from magnetic resonance images in first-episode schizophrenic patients. Arch Gen Psychiatry. 49:1992;531-537.
21. Deutsch C.K., Price S.F., Wussler J., D'Agostino R. Craniofacial dysmorphology in schizophrenia. Schizophr Res. 24:1997;53-54.
22. Diewert V.M., Lozanoff S. A morphometric analysis of human embryonic craniofacial growth in the median plane during primary palate formation. J Craniofac Genet Dev Biol. 13:1993;147-161.
23. Diewert V.M., Lozanoff S. Growth and morphogenesis of the human embryonic midface during primary palate formation analyzed in frontal sections. J Craniofac Genet Dev Biol. 13:1993;162-183.
24. Diewert V.M., Lozanoff S., Choy V. Computer reconstructions of human embryonic craniofacial morphology showing changes in relations between the face and brain during primary palate formation. J Craniofac Genet Dev Biol. 13:1993;193-201.
25. Done D.J., Crow T.J., Johnstone E.C., Sacker A. Childhood antecedents of schizophrenia and affective illness social adjustment at ages 7 and 11 . Br Med J. 309:1994;699-703.
26. Fatemi S.H., Sidwell R., Akhter P., Sedgewick J., Thuras P., Bailey K., et al. Human influenza viral infection in utero increases nNOS expression in hippocampi of neonatal mice. Synapse. 29:1998;84-88.
27. Geddes J.R., Lawrie S.M. Obstetric complications and schizophrenia a meta-analysis . Br J Psychiatry. 167:1995;786-793.
28. Glantz L.A., Lewis D.A. Reduction of synaptophysin immunoreactivity in the prefrontal cortex of subjects with schizophrenia. Arch Gen Psychiatry. 54:1997;943-952.
29. Green M.F., Satz P., Gaier D.J., Ganzell S., Kharabi F. Minor physical anomalies in schizophrenia. Schizophr Bull. 15:1989;91-99.
30. Haznedar M.M., Buchsbaum M.S., Luu C., Hazlett E.A., Siegel B.V., Lohr J., et al. Decreased anterior cingulate gyrus metabolic rate in schizophrenia. Am J Psychiatry. 154:1997;682-684.
31. Impagnatiello F., Pisu M.G., Pesold C., Uzunov D.P., Dwivedi Y., Pandev G., et al. Reelin expression is decreased in several areas of schizophrenic brain. Soc Neurosci Abstr. 24:1998;1275.
32. Jones E.G. Cortical development and thalamic pathology in schizophrenia. Schizophr Bull. 23:1997;483-501.
33. Jones P., Rodgers B., Murray R., Marmot M. Child developmental risk factors for adult schizophrenia in the British 1946 birth cohort. Lancet. 344:1994;1398-1402.
34. Kier E.L., Kim J.H., Fulbright R.K., Bronen R.A. Embryology of the human fetal hippocampus MR imaging, anatomy and histology . Am J Neuroradiology. 18:1997;525-532.
35. Kostovic I., Krmpotic J. Early prenatal ontogenesis of the neuronal connections in the interhemispheric cortex of the human gyrus cinguli. Verh Anat Ges. 70:1976;305-316.
36. Kostovic I., Petanjek Z., Judas M. Early areal differentiation of the human cerebral cortex entorhinal area . Hippocampus. 3:1993;447-458.
37. Krimer L.S., Herman M.M., Saunders R.C., Boyd J.C., Hyde T.M., Carter J.M., et al. A qualitative and quantitative analysis of the entorhinal cortex in schizophrenia. Cereb Cortex. 7:1997;732-739.
38. Kurnit D.R., Layton W.M., Matthysse S. Genetics, chance, and morphogenesis. Am J Hum Genet. 41:1987;979-995.
39. Lane A., Kinsella A., Murphy P., Byrne M., Keenan J., Colgan K., et al. The anthropometric assessment of dysmorphic features in schizophrenia as an index of its developmental origins. Psychol Med. 27:1997;1155-1164.
40. Lane A., Larkin C., Waddington J.L., O'Callaghan C. Dysmorphic features and schizophrenia. Waddington J.L., Buckley P.F. The Neurodevelopmental Basis of Schizophrenia. 1996;79-93 Landes, Georgetown, Texas.
41. Lewis D.A. Schizophrenia and disordered neural circuitry. Schizophr Bull. 23:1997;529-531.
42. Lewis G., David A., Andreasson S., Allebeck P. Schizophrenia and city life. Lancet. 340:1992;137-140.
43. Lim K.O., Sullivan E.V., Zipursky R.B., Pfefferbaum A. Cortical gray matter volume deficits in schizophrenia a replication . Schizophr Res. 20:1996;157-164.
44. Lim K.O., Tew W., Kushner M., Chow K., Matsumoto B., DeLisi L.E. Cortical gray matter volume deficit in patients with first-episode schizophrenia. Am J Psychiatry. 153:1996;1548-1553.
45. Lohr J.B., Alder M., Flynn K., Harris J., McAdams L.A. Minor physical anomalies in older patients with late-onset schizophrenia, early onset schizophrenia, depression, and Alzheimer's disease. Am J Geriatr Psychiatry. 5:1997;318-323.
46. Lubinsky M.S. Midline developmental "weakness" as a consequence of determinative field properties. Am J Med Genet Suppl. 3:1987;23-28.
47. McGrath J., Murray R.M. Risk factors for schizophrenia from conception to birth . Hirsch S.R., Weinberger D.R. Schizophrenia. 1995;187-205 Blackwell, Oxford, UK.
48. McGuffin P., Asherson P., Owen M., Farmer A. The strength of the genetic effect is there room for an environmental influence in the aetiology of schizophrenia? Br J Psychiatry. 164:1994;593-599.
49. McNeil T.F. Obstetric complications. Waddington J.L., Buckley P.F. The Neurodevelopmental Basis of Schizophrenia. 1996;61-78 Landes, Georgetown, Texas.
50. McNeil T.F., Cantor-Graae E., Blennow G. Do "clumsy" fetuses cause labor and delivery complications? A study of offspring at risk for psychosis . Schizophr Res. 22:1996;85-88.
51. Mojsilovic J., Zecevic N. Early development of the human thalamus Golgi and Nissl study . Early Hum Dev. 27:1991;119-144.
52. Morgan V., Castle D., Page A., Fazio S., Gurrin L., Burton P., et al. Influenza epidemics and incidence of schizophrenia, affective disorders and mental retardation in Western Australia no evidence of a major effect . Schizophr Res. 26:1997;25-39.
53. Murray R.M., Lewis S.W. Is schizophrenia a neurodevelopmental disorder? Br Med J. 296:1987;681-682.
54. Myhrman A., Rantakallio P., Isohanni M., Jones P., Partanen U. Unwantedness of a pregnancy and schizophrenia in the child. Br J Psychiatry. 169:1996;637-640.
55. Nopoulos P., Torres I., Flaum M., Andreasen N.C., Ehrhardt J.C., Yuh W.T.C. Brain morphology in first-episode schizophrenia. Am J Psychiatry. 152:1995;1721-1723.
56. O'Callaghan E., Buckley P., Madigan C., Redmond O., Stack J.P., Kinsella A., et al. The relationship of minor physical anomalies and other putative indices of developmental disturbance in schizophrenia to abnormalities of cerebral structure on magnetic resonance imaging. Biol Psychiatry. 38:1995;516-524.
57. O'Callaghan E., Cotter D., Colgan K., Larkin C., Walsh D., Waddington J.L. Confinement of winter birth excess in schizophrenia to the urban-born and its gender specificity. Br J Psychiatry. 166:1995;51-54.
58. O'Callaghan E., Gibson T., Colohan H.A., Buckley P., Walshe D.G., Larkin C., et al. Risk of schizophrenia in adults born after obstetric complications and their association with early onset of illness a controlled study . Br Med J. 305:1992;1256-1259.
59. O'Connell P., Woodruff P.W.R., Wright I., Jones P., Murray R.M. Developmental insanity or dementia praecox was the wrong concept adopted? Schizophr Res. 23:1997;97-106.
60. Pearlson G.D., Petty R.G., Ross C.A., Tien A.Y. Schizophrenia a disease of heteromodal association cortex? Neuropsychopharmacology. 14:1996;1-17.
61. Pine D.S., Shaffer D., Schonfeld I.S., Davies M. Minor physical anomalies modifiers of environmental risks for psychiatric impairment? J Am Acad Child Adolesc Psychiatry. 36:1997;395-403.
62. Purohit D.P., Perl D.P., Haroutunian V., Powchik P., Davidson M., Davis K.L., et al. Alzheimer disease and related neurodegenerative diseases in elderly patients with schizophrenia. Arch Gen Psychiatry. 55:1998;205-211.
63. Rajkowska G., Selemon L.D., Goldman-Rakic P.S. Neuronal size and glial size in the prefrontal cortex. Arch Gen Psychiatry. 55:1998;215-224.
64. Selten J.P., Slaets J., Kahn R. Prenatal exposure to influenza and schizophrenia in Surinamese and Dutch Antillean immigrants to the Netherlands. Schizophr Res. 30:1998;101-103.
65. Susser E., Neugebaver R., Hoek H.W., Brown A.S., Liu S., Labovitz D., et al. Schizophrenia after prenatal famine. Arch Gen Psychiatry. 53:1996;25-31.
66. Takei N., Mortensen P.B., Klaening U., Murray R.M., Sham P.C., O'Callaghan E., et al. Relationship between in utero exposure to influenza epidemics and risk of schizophrenia in Denmark. Biol Psychiatry. 40:1996;817-824.
67. Torrey E.F., Bowler A.E., Clark K. Urban birth and residence as risk factors for psychoses an analysis of 1880 data . Schizophr Res. 25:1997;169-176.
68. Torrey E.F., Miller J., Rawlings R., Yolken R.H. Seasonality of births in schizophrenia and bipolar disorder a review of the literature . Schizophr Res. 28:1997;1-38.
69. Tsuang M.T., Faraone S.V. The case for heterogeneity in the etiology of schizophrenia. Schizophr Res. 17:1995;161-175.
70. Van Os J., Selten J.P. Prenatal exposure to maternal stress and subsequent schizophrenia. Br J Psychiatry. 172:1998;324-326.
71. Verdoux H., Takei N., de Saint-Mathurin R.C., Murray R.M., Bourgeois M.L. Seasonality of birth in schizophrenia the effect of regional population density . Schizophr Res. 23:1997;175-180.
72. Vesce F., Farina A., Giorgetti M., Jorizzo G., Bianciotto A., Calabrese O., et al. Increased incidence of preeclampsia in pregnancies complicated by fetal malformation. Gynecol Obstet Invest. 44:1997;107-111.
73. Vollmer J.Y., Clerc R.G. Homebox genes in the developing mouse brain. J Neurochem. 71:1998;1-19.
74. Waddington J.L. Schizophrenia developmental neuroscience and pathobiology . Lancet. 341:1993;531-536.
75. Waddington J.L. Genetics, chance and dysmorphogenesis in schizophrenia. Br J Psychiatry. 165:1994;693-694.
76. Waddington J.L., Buckley P.F., Scully P.J., Lane A., O'Callaghan E., Larkin C. Course of psychopathology, cognition and neurobiological abnormality in schizophrenia developmental origins and amelioration by antipsychotics? J Psychiatry Res. 32:1998;179-189.
77. Waddington J.L., Lane A., Scully P.J., Larkin C., O'Callaghan E. Neurodevelopmental and neuroprogressive processes in schizophrenia. Psychiatry Clin North Am. 21:1998;123-149.
78. Waddington J.L., O'Callaghan E., Buckley P.F., Larkin C. Structural brain imaging in schizophrenia in a neurodevelopmental context. Waddington J.L., Buckley P.F. The Neurodevelopmental Basis of Schizophrenia. 1996;95-106 Landes, Georgetown, Texas.
79. Walker E.F. Developmentally moderated expressions of the neuropathhology underlying schizophrenia. Schizophr Bull. 20:1994;453-480.
80. Walker E.F., Savoie T., Davis D. Neuromotor precursors of schizophrenia. Schizophr Bull. 20:1994;441-451.
81. Weinberger D.R. Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen Psychiatry. 44:1987;660-669.
82. Weinberger D.R. Schizophrenia from neuropathology to neurodevelopment . Lancet. 346:1995;552-557.