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December 1989, Vol 46, No. 12 >
Article | December 1989

Schizophrenia as an Anomaly of Development of Cerebral Asymmetry: Title and subTitle BreakA Postmortem Study and a Proposal Concerning the Genetic Basis of the Disease

Timothy J. Crow, PhD, FRCP, FRCPsych; Joanna Ball, MD, MRCP; Steven R. Bloom, MD, FRCP; Rosemary Brown; Clive J. Bruton, MD; Nigel Colter; Christopher D. Frith, PhD; Eve C. Johnstone, MD, FRCP, FRCPsych; David G. C. Owens, MD, FRCP, FRCPych; Gareth W. Roberts, PhD
[+] Author Affiliations

Accepted for publication September 22, 1989.

Presented as a poster exhibit at the Fourth European Winter Workshop on Schizophrenia, Badgastein, Austria, January, 1988.

Reprint requests to Division of Psychiatry, Clinical Research Centre, Northwick Park Hospital, Harrow, United Kingdom HAI 3UJ (Dr Crow).


Arch Gen Psychiatry. 1989;46(12):1145-1150. doi:10.1001/archpsyc.1989.01810120087013
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References
Comments

• Schizophrenia is associated with structural changes (eg, a mild degree of ventricular enlargement) in the brain, although whether these precede onset of illness or progress with episodes is not established. In a postmortem study, we find that ventricular enlargement affects the posterior and particularly the temporal horn of the lateral cerebral ventricle. By comparison with controls and with patients suffering from Alzheimer-type dementia (in which there is also temporal horn enlargement), the change is highly significantly selective to the left hemisphere. This deviation was not accompanied by an increase in glial cell number (examined chemically by assay of diazepam-binding inhibitor immunoreactivity and microscopically by density of staining with the Holzer' technique). The findings are consistent with the view that schizophrenia is a disorder of the genetic mechanisms that control the development of cerebral asymmetry.

REFERENCES

1 +
Eaton WW.  Epidemiology of schizophrenia . Epidemiol Rev . 1985;;7:105-126.
2 +
Hare EH.  Epidemiology of schizophrenia and affective psychoses . Br Med Bull . 1987;;43:514-530.
3 +
Lewine RRJ.  Gender and schizophrenia . In: Tsuang MT, Simpson JC, eds. Handbook of Schizophrenia: Nosology, Epidemiology and Genetics of Schizophrenia . Amsterdam, the Netherlands: Elsevier Science Publishers; 1988;;3:379-397.
4 +
Kety SS.  Mental illness in the biological and adoptive relatives of schizophrenic adoptees: findings relevant to genetic and environmental factors in etiology . Am J Psychiatry . 1983;;140:720-727.
5 +
Gottesman II, Shields J. Schizophrenia: The Epigenetic Puzzle . New York, NY: Cambridge University Press; 1982;.
6 +
Kendler KS.  The genetics of schizophrenia: an overview . In: Tsuang MT, Simpson JC, eds. Handbook of Schizophrenia: Nosology, Epidemiology and Genetics of Schizophrenia . Amsterdam, the Netherlands: Elsevier Science Publishers; 1988;;3:437-462.
7 +
Haug JO.  Pneumoencephalographic evidence of brain atrophy in acute and chronic schizophrenic patients . Acta Psychiatr Scand . 1982;;66:374-383.
8 +
Johnstone EC, Crow TJ, Frith CD, Husband J, Kreel L.  Cerebral ventricular size and cognitive impairment in chronic schizophrenia . Lancet . 1976;;2:924-926.
9 +
Weinberger DR, Torrey EF, Neophytides AN, Wyatt RJ.  Lateral cerebral ventricular enlargement in chronic schizophrenia . Arch Gen Psychiatry . 1979;;36:735-739.
10 +
Bogerts B, Meertz E, Schonfeld-Bausch R.  Basal ganglia and limbic system pathology in schizophrenia . Arch Gen Psychiatry . 1985;;42:784-791.
11 +
Brown R, Colter N, Corsellis JAN, Crow TJ, Frith CD, Jagoe R, Johnstone EC, Marsh L.  Postmortem evidence of structural brain changes in schizophrenia . Arch Gen Psychiatry . 1986;;43:36-42.
12 +
Feighner JP, Robins E, Guze SB, Woodruff RA, Winokur G, Munoz R.  Diagnostic criteria for use in psychiatric research . Arch Gen Psychiatry . 1972;;26:57-63.
13 +
Bruton CJ, Crow TJ, Frith CD, Johnstone EC, Owens DGC, Roberts GW.  Schizophrenia and the brain: a prospective clinico-neuropathological study . Psychol Med . In press.
14 +
Ball JA, Burnet PWJ, Bretherton-Watt D, Bloom SR.  Increase in diazepam binding inhibitor-like immunoreactivity (51-70) in Huntingtons disease . J Neurol Sci . 1988;;88:177-184.
15 +
Slater ETO, Beard AW, Glithero E.  The schizophrenia-like psychoses of epilepsy . Br J Psychiatry . 1963;;109:95-150.
16 +
Geschwind N, Levitsky W.  Left-right asymmetry in temporal speech region . Science . 1968;;161:186-187.
17 +
Roberts GW, Colter N, Crow TJ, Lofthouse R.  Gliosis in schizophrenia . Biol Psychiatry . 1987;;22:1173-1174.
18 +
Roberts GW, Colter N, Lofthouse R, Johnstone EC, Crow TJ.  Is there gliosis in schizophrenia? investigation of the temporal lobe . Biol Psychiatry . 1987;;22:1459-1468.
19 +
Falkai P, Bogerts B, Rozumek M.  Limbic pathology in schizophrenia: the entorhinal region-a morphometric study . Biol Psychiatry . 1988;;24:515-521.
20 +
Stevens CD, Altshuler LL, Bogerts B, Falkai P.  Quantitative study of gliosis in schizophrenia and Huntingtons chorea . Biol Psychiatry . 1988;;24:697-700.
21 +
Weinberger DR.  The pathogenesis of schizophrenia: a neurodevelopmental theory . In: Nasrallah HA, Weinberger DR, eds. Handbook of Schizophrenia: The Neurology of Schizophrenia . Amsterdam, the Netherlands: Elsevier Science Publishers; 1986;;1:397-406.
22 +
Reynolds GP.  Increased concentration and lateral asymmetry of amygdala dopamine in schizophrenia . Nature . 1983;;305:527-529.
23 +
Reveley MA, Reveley AM, Baldy R.  Left hemisphere hypodensity in discordant schizophrenic twins: a controlled study . Arch Gen Psychiatry . 1987;;44:625-632.
24 +
Jacobi W, Winkler H.  Encephalographische Studien an chronisch Schizophrenen . Arch Psychiatr Nervenkr . 1927;;81:299-332.
25 +
Hunter R, Jones M, Cooper F.  Modified lumbar air encephalography in the investigation of long stay psychiatric patients . J Neurol Sci . 1968;;6:593-596.
26 +
Keefe RSE, Mohs RC, Losonczy MF, Davidson M, Silverman JM, Kendler KS, Horvath HB, Nora R, Davis KL.  Characteristics of very poor outcome schizophrenia . Am J Psychiatry . 1987;;144:889-895.
27 +
Kelsoe JR, Cadet JL, Pickar D, Weinberger DR.  Quantitative neuroanatomy in schizophrenia: a controlled magnetic resonance imaging study . Arch Gen Psychiatry . 1988;;45:533-541.
28 +
Kurihara M, Yamashita S, Miyake S, Yamada M, Iwamoto H.  Computed tomography of epileptic children: an investigation on the temporal horn . No To Hattatsu . 1986;;18:452-458.
29 +
Crow TJ, Colter N, Frith CD, Johnstone EC, Owens DGC.  Developmental arrest of cerebral asymmetries in early onset schizophrenia . Psychiatr Res . 1989;;29:247-253.
30 +
Johnstone EC, Owens DGC, Crow TJ, Frith CD, Alexandropolous K, Bydder GM, Colter N.  Temporal lobe structure as determined by nuclear magnetic resonance in schizophrenia and bipolar affective disorder . J Neurol Neurosurg Psychiatry . 1989;;52:736-741.
31 +
Suddath RL, Casanova MF, Goldberg TE, Daniel DG, Kelsoe JR, Weinberger DR.  Temporal lobe pathology in schizophrenia: a quantitative magnetic resonance imaging study . Arch Gen Psychiatry . 1989;;146:464-472.
32 +
Chi JG, Dooling EC, Gilles FH.  Gyral development of the human brain . Ann Neurol . 1977;;1:86-93.
33 +
Weinberger DR, Luchins DJ, Morihisa J, Wyatt RJ.  Asymmetrical volumes of the right and left frontal and occipital regions of the human brain . Ann Neurol . 1982;;11:97-100.
34 +
Jakob H, Beckmann H.  Prenatal developmental disturbances in the limbic allocortex of schizophrenics . J Neural Transm . 1986;;65:303-326.
35 +
Falkai P, Bogerts B, Roberts GW, Crow TJ.  Measurement of the alpha-cell-migration in the entorhinal region: a marker for developmental disturbances in schizophrenia? Schizophr Res . 1988;;1:157-158.
36 +
Larroche J-C.  Perinatal brain damage . In: Hume Adams J, Corsellis JAN, Duchen LW, eds. Greenfield's Neuropathology . Baltimore, Md: Edward Arnold Publishers Ltd; 1984;:451-489.
37 +
Guzzetta F, Shackleford GD, Volpe S, Perlman JM, Volpe JJ.  Periventricular intraparenchymal echodensities in the premature newborn: critical determinant of neurologic outcome . Pediatrics . 1986;;78:995-1006.
38 +
Goodman R.  Are complications of pregnancy and birth causes of schizophrenia? Dev Med Child Neurol . 1988;;30:391-406.
39 +
Flor-Henry P.  Psychosis and temporal lobe epilepsy: a controlled investigation . Epilepsia . 1969;;10:363-395.
40 +
Broca P.  Perte de la parole: ramollisement chronique et destruction partielle du lobe antérieur gauche du cerveau . Bull Soc Anthropol . 1861;;2:219-235.
41 +
Dax M.  Lesions de la moitié gauche de l'éncéphale coincident avec l'oublie des signes de la pensée. Lu à congres meridionel tenu a Montpellier en 1836 . Gaz Hebd Med Chir . 1865;;11:259-260.
42 +
Crichton-Browne J.  On the weight of the brain and its component parts in the insane . Brain . 1879;;2:42-67.
43 +
Southard EE.  On the topographic distribution of cortex lesions and anomalies in dementia praecox with some account of their functional significance . Am J Insanity . 1915;;71:603-671.
44 +
Yeni-Komshian G, Benson D.  Anatomical study of cerebral asymmetry in the temporal lobe of humans, chimpanzees, and rhesus monkeys . Science . 1976;;192:387-389.
45 +
de Lacoste MC, Horvath DS, Woodward DJ.  Prosencephalic asymmetries in lemuridae . Brain Behav Evol . 1988;;31:296-311.
46 +
Annett M. Left, Right, Hand and Brain: The Right Shift Theory . Hillsdale, NJ: Lawrence Erlbaum Associates Inc Publishers; 1985;.
47 +
McManus IC.  Handedness, language dominance and aphasia: a genetic model . Psychol Med . 1985;;8( (suppl) ):1-40.
48 +
Crow TJ.  A re-evaluation of the viral hypothesis: is psychosis the result of retroviral integration at a site close to the cerebral dominance gene? Br J Psychiatry . 1984;;145:243-253.
49 +
Crow TJ.  Left brain, retrotransposons and schizophrenia . Br Med J . 1986;;293:3-4.
50 +
Crow TJ.  Sex chromosomes and psychosis: the case for a pseudo-autosomal locus . Br J Psychiatry . 1988;;153:675-683.
51 +
Crow TJ, DeLisi LE, Johnstone EC.  Concordance by sex in sibling pairs with schizophrenia is paternally inherited: evidence for a pseudo-autosomal locus . Br J Psychiatry . 1989;;155:92-97.
52 +
Collinge J, Boccio A, DeLisi LE, Johnstone EC, Owen F, Poulter M, Risby D, Shah T, Crow TJ. A pseudo-autosomal locus for schizophrenia? a sibling pair analysis using a telomeric probe. In: Abstracts of the First World Congress of Psychiatric Genetics; August, 1989; Cambridge, England.
53 +
Crow TJ.  A pseudo-autosomal locus for the cerebral dominance gene . Lancet . 1989;;2:339-340.
54 +
O'Rourke DH, Gottesman II, Suarez BK, Rice J, Reich T.  Refutation of the general single-locus model for the etiology of schizophrenia . Am J Hum Genet . 1982;;34:630-649.

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1 +
Eaton WW.  Epidemiology of schizophrenia . Epidemiol Rev . 1985;;7:105-126.
2 +
Hare EH.  Epidemiology of schizophrenia and affective psychoses . Br Med Bull . 1987;;43:514-530.
3 +
Lewine RRJ.  Gender and schizophrenia . In: Tsuang MT, Simpson JC, eds. Handbook of Schizophrenia: Nosology, Epidemiology and Genetics of Schizophrenia . Amsterdam, the Netherlands: Elsevier Science Publishers; 1988;;3:379-397.
4 +
Kety SS.  Mental illness in the biological and adoptive relatives of schizophrenic adoptees: findings relevant to genetic and environmental factors in etiology . Am J Psychiatry . 1983;;140:720-727.
5 +
Gottesman II, Shields J. Schizophrenia: The Epigenetic Puzzle . New York, NY: Cambridge University Press; 1982;.
6 +
Kendler KS.  The genetics of schizophrenia: an overview . In: Tsuang MT, Simpson JC, eds. Handbook of Schizophrenia: Nosology, Epidemiology and Genetics of Schizophrenia . Amsterdam, the Netherlands: Elsevier Science Publishers; 1988;;3:437-462.
7 +
Haug JO.  Pneumoencephalographic evidence of brain atrophy in acute and chronic schizophrenic patients . Acta Psychiatr Scand . 1982;;66:374-383.
8 +
Johnstone EC, Crow TJ, Frith CD, Husband J, Kreel L.  Cerebral ventricular size and cognitive impairment in chronic schizophrenia . Lancet . 1976;;2:924-926.
9 +
Weinberger DR, Torrey EF, Neophytides AN, Wyatt RJ.  Lateral cerebral ventricular enlargement in chronic schizophrenia . Arch Gen Psychiatry . 1979;;36:735-739.
10 +
Bogerts B, Meertz E, Schonfeld-Bausch R.  Basal ganglia and limbic system pathology in schizophrenia . Arch Gen Psychiatry . 1985;;42:784-791.
11 +
Brown R, Colter N, Corsellis JAN, Crow TJ, Frith CD, Jagoe R, Johnstone EC, Marsh L.  Postmortem evidence of structural brain changes in schizophrenia . Arch Gen Psychiatry . 1986;;43:36-42.
12 +
Feighner JP, Robins E, Guze SB, Woodruff RA, Winokur G, Munoz R.  Diagnostic criteria for use in psychiatric research . Arch Gen Psychiatry . 1972;;26:57-63.
13 +
Bruton CJ, Crow TJ, Frith CD, Johnstone EC, Owens DGC, Roberts GW.  Schizophrenia and the brain: a prospective clinico-neuropathological study . Psychol Med . In press.
14 +
Ball JA, Burnet PWJ, Bretherton-Watt D, Bloom SR.  Increase in diazepam binding inhibitor-like immunoreactivity (51-70) in Huntingtons disease . J Neurol Sci . 1988;;88:177-184.
15 +
Slater ETO, Beard AW, Glithero E.  The schizophrenia-like psychoses of epilepsy . Br J Psychiatry . 1963;;109:95-150.
16 +
Geschwind N, Levitsky W.  Left-right asymmetry in temporal speech region . Science . 1968;;161:186-187.
17 +
Roberts GW, Colter N, Crow TJ, Lofthouse R.  Gliosis in schizophrenia . Biol Psychiatry . 1987;;22:1173-1174.
18 +
Roberts GW, Colter N, Lofthouse R, Johnstone EC, Crow TJ.  Is there gliosis in schizophrenia? investigation of the temporal lobe . Biol Psychiatry . 1987;;22:1459-1468.
19 +
Falkai P, Bogerts B, Rozumek M.  Limbic pathology in schizophrenia: the entorhinal region-a morphometric study . Biol Psychiatry . 1988;;24:515-521.
20 +
Stevens CD, Altshuler LL, Bogerts B, Falkai P.  Quantitative study of gliosis in schizophrenia and Huntingtons chorea . Biol Psychiatry . 1988;;24:697-700.
21 +
Weinberger DR.  The pathogenesis of schizophrenia: a neurodevelopmental theory . In: Nasrallah HA, Weinberger DR, eds. Handbook of Schizophrenia: The Neurology of Schizophrenia . Amsterdam, the Netherlands: Elsevier Science Publishers; 1986;;1:397-406.
22 +
Reynolds GP.  Increased concentration and lateral asymmetry of amygdala dopamine in schizophrenia . Nature . 1983;;305:527-529.
23 +
Reveley MA, Reveley AM, Baldy R.  Left hemisphere hypodensity in discordant schizophrenic twins: a controlled study . Arch Gen Psychiatry . 1987;;44:625-632.
24 +
Jacobi W, Winkler H.  Encephalographische Studien an chronisch Schizophrenen . Arch Psychiatr Nervenkr . 1927;;81:299-332.
25 +
Hunter R, Jones M, Cooper F.  Modified lumbar air encephalography in the investigation of long stay psychiatric patients . J Neurol Sci . 1968;;6:593-596.
26 +
Keefe RSE, Mohs RC, Losonczy MF, Davidson M, Silverman JM, Kendler KS, Horvath HB, Nora R, Davis KL.  Characteristics of very poor outcome schizophrenia . Am J Psychiatry . 1987;;144:889-895.
27 +
Kelsoe JR, Cadet JL, Pickar D, Weinberger DR.  Quantitative neuroanatomy in schizophrenia: a controlled magnetic resonance imaging study . Arch Gen Psychiatry . 1988;;45:533-541.
28 +
Kurihara M, Yamashita S, Miyake S, Yamada M, Iwamoto H.  Computed tomography of epileptic children: an investigation on the temporal horn . No To Hattatsu . 1986;;18:452-458.
29 +
Crow TJ, Colter N, Frith CD, Johnstone EC, Owens DGC.  Developmental arrest of cerebral asymmetries in early onset schizophrenia . Psychiatr Res . 1989;;29:247-253.
30 +
Johnstone EC, Owens DGC, Crow TJ, Frith CD, Alexandropolous K, Bydder GM, Colter N.  Temporal lobe structure as determined by nuclear magnetic resonance in schizophrenia and bipolar affective disorder . J Neurol Neurosurg Psychiatry . 1989;;52:736-741.
31 +
Suddath RL, Casanova MF, Goldberg TE, Daniel DG, Kelsoe JR, Weinberger DR.  Temporal lobe pathology in schizophrenia: a quantitative magnetic resonance imaging study . Arch Gen Psychiatry . 1989;;146:464-472.
32 +
Chi JG, Dooling EC, Gilles FH.  Gyral development of the human brain . Ann Neurol . 1977;;1:86-93.
33 +
Weinberger DR, Luchins DJ, Morihisa J, Wyatt RJ.  Asymmetrical volumes of the right and left frontal and occipital regions of the human brain . Ann Neurol . 1982;;11:97-100.
34 +
Jakob H, Beckmann H.  Prenatal developmental disturbances in the limbic allocortex of schizophrenics . J Neural Transm . 1986;;65:303-326.
35 +
Falkai P, Bogerts B, Roberts GW, Crow TJ.  Measurement of the alpha-cell-migration in the entorhinal region: a marker for developmental disturbances in schizophrenia? Schizophr Res . 1988;;1:157-158.
36 +
Larroche J-C.  Perinatal brain damage . In: Hume Adams J, Corsellis JAN, Duchen LW, eds. Greenfield's Neuropathology . Baltimore, Md: Edward Arnold Publishers Ltd; 1984;:451-489.
37 +
Guzzetta F, Shackleford GD, Volpe S, Perlman JM, Volpe JJ.  Periventricular intraparenchymal echodensities in the premature newborn: critical determinant of neurologic outcome . Pediatrics . 1986;;78:995-1006.
38 +
Goodman R.  Are complications of pregnancy and birth causes of schizophrenia? Dev Med Child Neurol . 1988;;30:391-406.
39 +
Flor-Henry P.  Psychosis and temporal lobe epilepsy: a controlled investigation . Epilepsia . 1969;;10:363-395.
40 +
Broca P.  Perte de la parole: ramollisement chronique et destruction partielle du lobe antérieur gauche du cerveau . Bull Soc Anthropol . 1861;;2:219-235.
41 +
Dax M.  Lesions de la moitié gauche de l'éncéphale coincident avec l'oublie des signes de la pensée. Lu à congres meridionel tenu a Montpellier en 1836 . Gaz Hebd Med Chir . 1865;;11:259-260.
42 +
Crichton-Browne J.  On the weight of the brain and its component parts in the insane . Brain . 1879;;2:42-67.
43 +
Southard EE.  On the topographic distribution of cortex lesions and anomalies in dementia praecox with some account of their functional significance . Am J Insanity . 1915;;71:603-671.
44 +
Yeni-Komshian G, Benson D.  Anatomical study of cerebral asymmetry in the temporal lobe of humans, chimpanzees, and rhesus monkeys . Science . 1976;;192:387-389.
45 +
de Lacoste MC, Horvath DS, Woodward DJ.  Prosencephalic asymmetries in lemuridae . Brain Behav Evol . 1988;;31:296-311.
46 +
Annett M. Left, Right, Hand and Brain: The Right Shift Theory . Hillsdale, NJ: Lawrence Erlbaum Associates Inc Publishers; 1985;.
47 +
McManus IC.  Handedness, language dominance and aphasia: a genetic model . Psychol Med . 1985;;8( (suppl) ):1-40.
48 +
Crow TJ.  A re-evaluation of the viral hypothesis: is psychosis the result of retroviral integration at a site close to the cerebral dominance gene? Br J Psychiatry . 1984;;145:243-253.
49 +
Crow TJ.  Left brain, retrotransposons and schizophrenia . Br Med J . 1986;;293:3-4.
50 +
Crow TJ.  Sex chromosomes and psychosis: the case for a pseudo-autosomal locus . Br J Psychiatry . 1988;;153:675-683.
51 +
Crow TJ, DeLisi LE, Johnstone EC.  Concordance by sex in sibling pairs with schizophrenia is paternally inherited: evidence for a pseudo-autosomal locus . Br J Psychiatry . 1989;;155:92-97.
52 +
Collinge J, Boccio A, DeLisi LE, Johnstone EC, Owen F, Poulter M, Risby D, Shah T, Crow TJ. A pseudo-autosomal locus for schizophrenia? a sibling pair analysis using a telomeric probe. In: Abstracts of the First World Congress of Psychiatric Genetics; August, 1989; Cambridge, England.
53 +
Crow TJ.  A pseudo-autosomal locus for the cerebral dominance gene . Lancet . 1989;;2:339-340.
54 +
O'Rourke DH, Gottesman II, Suarez BK, Rice J, Reich T.  Refutation of the general single-locus model for the etiology of schizophrenia . Am J Hum Genet . 1982;;34:630-649.

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