Brain, Vol. 122, No. 4, 593-624,
April 1999
© 1999 Oxford University Press
Invited Review |
The neuropathology of schizophrenia
A critical review of the data and their interpretation
University Department of Psychiatry, Warneford Hospital, Oxford, UK
Correspondence to:
Dr P. J. Harrison, Neurosciences Building, University Department of Psychiatry, Warneford Hospital, Oxford OX3 7JX, UK E-mail: paul.harrison{at}psychiatry.ox.ac.uk
Despite a hundred years' research, the neuropathology of schizophrenia remains obscure. However, neither can the null hypothesis be sustained—that it is a `functional' psychosis, a disorder with no structural basis. A number of abnormalities have been identified and confirmed by meta-analysis, including ventricular enlargement and decreased cerebral (cortical and hippocampal) volume. These are characteristic of schizophrenia as a whole, rather than being restricted to a subtype, and are present in first-episode, unmedicated patients. There is considerable evidence for preferential involvement of the temporal lobe and moderate evidence for an alteration in normal cerebral asymmetries. There are several candidates for the histological and molecular correlates of the macroscopic features. The probable proximal explanation for decreased cortical volume is reduced neuropil and neuronal size, rather than a loss of neurons. These morphometric changes are in turn suggestive of alterations in synaptic, dendritic and axonal organization, a view supported by immunocytochemical and ultrastructural findings. Pathology in subcortical structures is not well established, apart from dorsal thalamic nuclei, which are smaller and contain fewer neurons. Other cytoarchitectural features of schizophrenia which are often discussed, notably entorhinal cortex heterotopias and hippocampal neuronal disarray, remain to be confirmed. The phenotype of the affected neuronal and synaptic populations is uncertain. A case can be made for impairment of hippocampal and corticocortical excitatory pathways, but in general the relationship between neurochemical findings (which centre upon dopamine, 5-hydroxytryptamine, glutamate and GABA systems) and the neuropathology of schizophrenia is unclear. Gliosis is not an intrinsic feature; its absence supports, but does not prove, the prevailing hypothesis that schizophrenia is a disorder of prenatal neurodevelopment. The cognitive impairment which frequently accompanies schizophrenia is not due to Alzheimer's disease or any other recognized neurodegenerative disorder. Its basis is unknown. Functional imaging data indicate that the pathophysiology of schizophrenia reflects aberrant activity in, and integration of, the components of distributed circuits involving the prefrontal cortex, hippocampus and certain subcortical structures. It is hypothesized that the neuropathological features represent the anatomical substrate of these functional abnormalities in neural connectivity. Investigation of this proposal is a goal of current neuropathological studies, which must also seek (i) to establish which of the recent histological findings are robust and cardinal, and (ii) to define the relationship of the pathological phenotype with the clinical syndrome, its neurochemistry and its pathogenesis.
Alzheimer's disease; cytoarchitecture; morphometry; synapse; psychosis
DLPFC = dorsolateral prefrontal cortex; 5-HT = 5-hydroxytryptamine; VBR = ventricle : brain ratio
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A. Sawa and A. Kamiya Elucidating the pathogenesis of schizophrenia BMJ, September 20, 2003; 327(7416): 632 - 633. [Full Text] [PDF]
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P. C. Sallet, H. Elkis, T. M. Alves, J. R. Oliveira, E. Sassi, C. C. de Castro, G. F. Busatto, and W. F. Gattaz Reduced Cortical Folding in Schizophrenia: An MRI Morphometric Study Am J Psychiatry, September 1, 2003; 160(9): 1606 - 1613. [Abstract] [Full Text] [PDF]
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M. Kromkamp, H. B. M. Uylings, M. P. Smidt, A. J. C. G. M. Hellemons, J. P. H. Burbach, and R. S. Kahn Decreased Thalamic Expression of the Homeobox Gene DLX1 in Psychosis Arch Gen Psychiatry, September 1, 2003; 60(9): 869 - 874. [Abstract] [Full Text] [PDF]
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G. R. Kuperberg, M. R. Broome, P. K. McGuire, A. S. David, M. Eddy, F. Ozawa, D. Goff, W. C. West, S. C. R. Williams, A. J. W. van der Kouwe, et al. Regionally Localized Thinning of the Cerebral Cortex in Schizophrenia Arch Gen Psychiatry, September 1, 2003; 60(9): 878 - 888. [Abstract] [Full Text] [PDF]
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M. S. Bagary, M. R. Symms, G. J. Barker, S. H. Mutsatsa, E. M. Joyce, and M. A. Ron Gray and White Matter Brain Abnormalities in First-Episode Schizophrenia Inferred From Magnetization Transfer Imaging Arch Gen Psychiatry, August 1, 2003; 60(8): 779 - 788. [Abstract] [Full Text] [PDF]
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S. L. COLLINSON, C. E. MACKAY, A. C. JAMES, D. J. QUESTED, T. PHILLIPS, N. ROBERTS, and T. J. CROW Brain volume, asymmetry and intellectual impairment in relation to sex in early-onset schizophrenia The British Journal of Psychiatry, August 1, 2003; 183(2): 114 - 120. [Abstract] [Full Text] [PDF]
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J. R. Highley, M. A. Walker, T. J. Crow, M. M. Esiri, and P. J. Harrison Low Medial and Lateral Right Pulvinar Volumes in Schizophrenia: A Postmortem Study Am J Psychiatry, June 1, 2003; 160(6): 1177 - 1179. [Abstract] [Full Text] [PDF]
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J. BURNS, D. JOB, M. E. BASTIN, H. WHALLEY, T. MACGILLIVRAY, E. C. JOHNSTONE, and S M. LAWRIE Structural disconnectivity in schizophrenia: a diffusion tensor magnetic resonance imaging study The British Journal of Psychiatry, May 1, 2003; 182(5): 439 - 443. [Abstract] [Full Text] [PDF]
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K. C. Luk, T. E. Kennedy, and A. F. Sadikot Glutamate Promotes Proliferation of Striatal Neuronal Progenitors by an NMDA Receptor-Mediated Mechanism J. Neurosci., March 15, 2003; 23(6): 2239 - 2250. [Abstract] [Full Text] [PDF]
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P. O. Koh, C. Bergson, A. S. Undie, P. S. Goldman-Rakic, and M. S. Lidow Up-regulation of the D1 Dopamine Receptor-Interacting Protein, Calcyon, in Patients With Schizophrenia Arch Gen Psychiatry, March 1, 2003; 60(3): 311 - 319. [Abstract] [Full Text] [PDF]
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P. O. Koh, C. Bergson, A. S. Undie, P. S. Goldman-Rakic, and M. S. Lidow Up-regulation of the D1 Dopamine Receptor-Interacting Protein, Calcyon, in Patients With Schizophrenia Arch Gen Psychiatry, March 1, 2003; 60(3): 311 - 319. [Abstract] [Full Text]
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Y. Ozeki, T. Tomoda, J. Kleiderlein, A. Kamiya, L. Bord, K. Fujii, M. Okawa, N. Yamada, M. E. Hatten, S. H. Snyder, et al. From the Cover: Disrupted-in-Schizophrenia-1 (DISC-1): Mutant truncation prevents binding to NudE-like (NUDEL) and inhibits neurite outgrowth PNAS, January 7, 2003; 100(1): 289 - 294. [Abstract] [Full Text] [PDF]
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J. R. Highley, M. A. Walker, M. M. Esiri, T. J. Crow, and P. J. Harrison Asymmetry of the Uncinate Fasciculus: A Post-mortem Study of Normal Subjects and Patients with Schizophrenia Cereb Cortex, November 1, 2002; 12(11): 1218 - 1224. [Abstract] [Full Text] [PDF]
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D. COTTER and C. M. PARIANTE Stress and the progression of the developmental hypothesis of schizophrenia The British Journal of Psychiatry, November 1, 2002; 181(5): 363 - 365. [Full Text] [PDF]
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P. O'Donnell, B. L. Lewis, D. R. Weinberger, and B. K. Lipska Neonatal Hippocampal Damage Alters Electrophysiological Properties of Prefrontal Cortical Neurons in Adult Rats Cereb Cortex, September 1, 2002; 12(9): 975 - 982. [Abstract] [Full Text] [PDF]
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L. J. Seidman, S. V. Faraone, J. M. Goldstein, W. S. Kremen, N. J. Horton, N. Makris, R. Toomey, D. Kennedy, V. S. Caviness, and M. T. Tsuang Left Hippocampal Volume as a Vulnerability Indicator for Schizophrenia: A Magnetic Resonance Imaging Morphometric Study of Nonpsychotic First-Degree Relatives Arch Gen Psychiatry, September 1, 2002; 59(9): 839 - 849. [Abstract] [Full Text] [PDF]
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S. M. LAWRIE, H. C. WHALLEY, S. S. ABUKMEIL, J. N. KESTELMAN, P. MILLER, J. J. K. BEST, D. G. C. OWENS, and E. C. JOHNSTONE Temporal lobe volume changes in people at high risk of schizophrenia with psychotic symptoms The British Journal of Psychiatry, August 1, 2002; 181(2): 138 - 143. [Abstract] [Full Text] [PDF]
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M. R. Gluck, R. G. Thomas, K. L. Davis, and V. Haroutunian Implications for Altered Glutamate and GABA Metabolism in the Dorsolateral Prefrontal Cortex of Aged Schizophrenic Patients Am J Psychiatry, July 1, 2002; 159(7): 1165 - 1173. [Abstract] [Full Text] [PDF]
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M. Ilia, C. Beasley, D. Meijer, R. Kerwin, D. Cotter, I. Everall, and J. Price Expression of Oct-6, a POU III Domain Transcription Factor, in Schizophrenia Am J Psychiatry, July 1, 2002; 159(7): 1174 - 1182. [Abstract] [Full Text] [PDF]
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P. J. Harrison The neuropathology of primary mood disorder Brain, July 1, 2002; 125(7): 1428 - 1449. [Abstract] [Full Text] [PDF]
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D. R. Weinberger and R. K. McClure Neurotoxicity, Neuroplasticity, and Magnetic Resonance Imaging Morphometry: What Is Happening in the Schizophrenic Brain? Arch Gen Psychiatry, June 1, 2002; 59(6): 553 - 558. [Full Text] [PDF]
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