Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-29T10:54:59.912Z Has data issue: false hasContentIssue false

Reduction of cortical volume in schizophrenia on magnetic resonance imaging

Published online by Cambridge University Press:  09 July 2009

I. Harvey
Affiliation:
Institute of Neurology; Institute of Psychiatry; and Charing Cross & Westminster Medical School, London
M. A. Ron*
Affiliation:
Institute of Neurology; Institute of Psychiatry; and Charing Cross & Westminster Medical School, London
G. Du Boulay
Affiliation:
Institute of Neurology; Institute of Psychiatry; and Charing Cross & Westminster Medical School, London
D. Wicks
Affiliation:
Institute of Neurology; Institute of Psychiatry; and Charing Cross & Westminster Medical School, London
S. W. Lewis
Affiliation:
Institute of Neurology; Institute of Psychiatry; and Charing Cross & Westminster Medical School, London
R. M. Murray
Affiliation:
Institute of Neurology; Institute of Psychiatry; and Charing Cross & Westminster Medical School, London
*
1Address for correspondence: Dr M. A. Ron, National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BG.

Synopsis

The MRI scans of 48 schizophrenic patients, fulfilling RDC criteria, were compared to those of 34 healthy controls matched for age, ethnicity and parental social class. The volume of the frontal and anterior parietal lobes was significantly reduced in the schizophrenic group as a result of a selective decrease in cortical volume, with a corresponding increase in the volume of sulcal fluid. Reduction in the volume of the temporal grey matter was more marked on the right, but was not in excess of the loss of volume observed in other areas of the cortex. MRI abnormalities correlated poorly with clinical parameters, although both unemployment and poor pre-morbid adjustment predicted reduced cerebral volume and increased sulcal volume. These results question whether the medial temporal lobes are the only site of structural pathology in schizophrenia.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 1993

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altschuler, L. L., Casanova, M. E., Goldberg, T. E. & Kleinman, J. E. (1990). The hippocampus and parahippocampus in schizophrenic, suicide and control brains. Archives of General Psychiatry 47, 10291034.CrossRefGoogle Scholar
American Psychiatric Association, Committee on Nomenclature and Statistics (1987). Diagnostic and Statistical Manual of Mental Disorders, 3rd edn – Revised. American Psychiatric Association: Washington, DC.Google Scholar
Andreasen, N. C., Endicott, J., Spitzer, R. L. & Winokur, G. (1977). The family history method using diagnostic criteria. Archives of General Psychiatry 34, 12291235.CrossRefGoogle ScholarPubMed
Andreasen, N. C., Nasrallah, H. A., Dunn, V., Olson, S. C., Grove, W. M., Ehrhardt, J. C., Coffman, J. A. & Crossett, J. H. W. (1986). Structural abnormalities in the frontal lobe system in schizophrenia: a magnetic resonance imaging study. Archives of General Psychiatry 43, 136144.CrossRefGoogle ScholarPubMed
Andreasen, N. C., Ehrhardt, J. C., Swayze, V. W., Alliger, R. J., Yuh, W. T., Cohen, G. & Ziebell, S. (1990). Magnetic resonance imaging of the brain in schizophrenia. The pathophysiologic significance of structural abnormalities. Archives of General Psychiatry 47, 3544.CrossRefGoogle ScholarPubMed
Annett, M. (1970). A classification of hand preference by association analysis. British Journal of Psychology 61, 303321.CrossRefGoogle ScholarPubMed
Awad, I. A., Spetzler, R. F., Hodak, J. A., Awad, C. A. & Carey, R. (1986). Incidental subcortical lesions identified on magnetic resonance imaging in the elderly. Stroke 17, 10841097.CrossRefGoogle ScholarPubMed
Barta, P. E., Pearlson, G. D., Powers, R. E., Richards, S. S. & Tune, L. E. (1990). Auditory hallucinations and smaller superior temporal lobe gyms volume in schizophrenia. American Journal of Psychiatry 147, 14571482.Google Scholar
Bartko, J. J. & Carpenter, W. T. Jr. (1976). On the methods and theory of reliability. Journal of Nervous and Mental Disease 163, 307317.CrossRefGoogle ScholarPubMed
Benes, F. M., Davison, J. & Bird, E. D. (1986). Quantitative cytoarchitectural studies of the cerebral cortex of schizophrenics. Archives of General Psychiatry 43, 3135.CrossRefGoogle ScholarPubMed
Bogerts, B., Meertz, E. & Schonfeldt-Bausch, R. (1985). Basal ganglia and limbic system pathology in schizophrenia. A morpho-metric study of brain volume and shrinkage. Archives of General Psychiatry 42, 784791.CrossRefGoogle Scholar
Bogerts, B., Falkai, P., Haupts, M., Greve, B., Ernst, S., Tapernon-Franz, U. & Heinzmann, U. (1990 a). Post-mortem volume measurements of limbic system and basal ganglia structures in chronic schizophrenics: initial results from a new brain collection. Schizophrenic Research 3, 295301.CrossRefGoogle ScholarPubMed
Bogerts, B., Ashtari, M., DeGreef, G., Alvir, J.-M. S., Bilder, R. M. & Lieberman, J. A. (1990 b). Reduced temporal limbic structure volumes on magnetic resonance images in first episode schizophrenia. Psychiatry Research 35, 113.CrossRefGoogle ScholarPubMed
Brown, R., Colter, N., Corsellis, J. A. N., Crow, T. J., Frith, C. D., Jagoe, R., Johnstone, E. C. & Marsh, L. (1986). Postmortem evidence of structural brain changes in schizophrenia. Archives of General Psychiatry 43, 3642.CrossRefGoogle ScholarPubMed
Bruton, C. J., Crow, T. J., Frith, C. D., Johnstone, E. C., Owens, D. G. & Roberts, G. W. (1990). Schizophrenia and the brain: a prospective clinico-neuropathological study. Psychological Medicine 20, 285304.CrossRefGoogle Scholar
Buchsbaum, M. S., Neuchterlein, K. H., Haier, R. J., Wu, J., Sicotte, N., Hazlett, E., Arsanow, R., Potkin, S. & Guich, S. (1990). Glucose metabolic rate in normals and schizophrenics during the continuous performance test assessed by positron emission tomography. British Journal of Psychiatry 156, 216227.CrossRefGoogle ScholarPubMed
Bydder, G. M. & Young, I. R. (1985). MR imaging: clinical use of the inversion recovery sequence. Journal of Computer Assisted Tomography 9, 659674.CrossRefGoogle ScholarPubMed
Coffman, J. A., Schwarzkopf, S. B., Nasrallah, H. A., Bornstein, R. A. & Olson, S. C. (1989). Temporal lobe asymmetry in schizophrenics by coronal MRI. Biological Psychiatry 25, 9798.CrossRefGoogle Scholar
Conlon, E. J. (1972). Quantitative cytoarchitectonics of the human cerebral cortex in schizophrenic dementia. Acta Neuropathologica 20, 110.CrossRefGoogle Scholar
Crow, T. J., Ball, J., Bloom, S. R., Brown, R., Bruton, C. J., Colter, N., Frith, C. D., Johnstone, E. C., Owens, D. G. C. & Roberts, G. W. (1989). Schizophrenia as an anomaly of development of cerebral asymmetry. Archives of General Psychiatry 46, 11451150.CrossRefGoogle ScholarPubMed
Dauphinais, I. D., DeLisi, L. E., Crow, T. J., Alexandropoulos, K., Colter, N., Tuma, I. & Gershon, E. S. (1990). Reduction in temporal lobe size in siblings with schizophrenia: a magnetic resonance imaging study. Psychiatric Research 35, 137138.CrossRefGoogle ScholarPubMed
Davis, J. M. (1976). Comparative doses and costs of anti-psychotic medication. Archives of General Psychiatry 33, 858861.CrossRefGoogle Scholar
Davis, P. J. M. & Wright, E. A. (1977). A new method for measuring cranial cavity volume and its application to the assessment of cerebral atrophy at autopsy. Neuropathology and Applied Neurobiology 3, 341358.CrossRefGoogle Scholar
DeLisi, L. E. & Goldin, L. R. (1987). Hat size in schizophrenia (letter). Archives of General Psychiatry 44, 672673.CrossRefGoogle Scholar
DeLisi, L. E., Alexandropolous, A., Colter, N., Crow, T. J., Dauphinais, D., Frith, C. & Gershon, E. C. (1988). Reduced temporal lobe area: an MRI study of siblings with schizophrenia. Schizophrenia Research 1, 169170.Google Scholar
DeLisi, L. E., Hoff, A. L., Schwartz, J. E., Shields, G. W., Halthore, S. N., Gupta, S. M., Henn, F. A. & Anand, A. K. (1991). Brain morphology in first episode schizophrenic-like psychotic patients: a quantitative MRI study. Biological Psychiatry 29, 159175.CrossRefGoogle Scholar
Dewan, M. J., Pandurangi, A. K., Lee, S. H., Ramachandran, T., Levy, B., Boucher, M., Yozawitz, A. & Major, L. (1986). A comprehensive study of chronic schizophrenic patients: quantitative computed tomography – cerebral density, ventricle and sulcal measures. Acta Psychiatrica Scandinavica 73, 152160.CrossRefGoogle ScholarPubMed
Falkai, P. & Bogerts, B. (1986). Cell loss in the hippocampus of schizophrenics. European Archives of Psychiatry and Neurological Sciences 236, 154161.CrossRefGoogle ScholarPubMed
Falkai, P., Bogerts, B. & Rozumek, M. (1988). Limbic pathology in schizophrenia: the entorhinal region – a morphometric study. Biological Psychiatry 24, 515521.CrossRefGoogle ScholarPubMed
Fazekas, F., Offenbacher, H., Fuchs, S., Schmidt, R., Niederkorn, K., Horner, S. & Lechner, H. (1988). Criteria for an increased specificity of MRI interpretation in elderly subjects with suspected multiple sclerosis. Neurology 38, 18221825.CrossRefGoogle ScholarPubMed
Geraud, G., Arne-Bes, M. C., Guell, A. & Bes, A. (1987). Reversibility of hemodynamic hypofrontality in schizophrenia. Journal of Cerebral Blood Flow and Metabolism 7, 912.CrossRefGoogle ScholarPubMed
Gittelman, R. & Klein, D. F. (1969). Premorbid asocial adjustment and prognosis in schizophrenia. Journal of Psychiatric Research 7, 3553.CrossRefGoogle Scholar
Goldthorpe, J. H. & Hope, K. (1974). The Social Grading of Occupation – A New Approach and Scale. Clarendon Press: Oxford.Google Scholar
Gur, R. E., Mozley, P. D., Resnick, S. M., Shtasel, D., Kohn, M., ZimmermanR., Herman, G. R., Herman, G., Atlas, S., Grossman, R., Erwin, R. & Gur, R. C. (1991). Magnetic resonance imaging in schizophrenia. I. Volumetric analysis of brain and cerebrospinal fluid. Archives of General Psychiatry 48, 407412.CrossRefGoogle ScholarPubMed
Guy, W. (1976). ECDEU Assessment Manual for Psycho-pharmacology, pp. 534537. US Public Health Service: Washington, DC.Google Scholar
Harvey, I., Williams, M., Toone, B. K., Lewis, S. W. & McGuffin, P. (1990). The ventricle–brain ratio (VBR) in functional psychoses: the relationship of lateral ventricular and total ventricular area. Psychological Medicine 20, 5562.CrossRefGoogle Scholar
Harvey, I., Ron, M. A., Murray, R., Lewis, S., Barker, G. & McManus, D. (1991). MRI in schizophrenia: basal ganglia and white matter T1 relaxation times. Psychological Medicine 21, 587598.CrossRefGoogle Scholar
Hauser, P., Dauphinais, I. D., Berrettini, W., DeLisi, L. E., Gelernter, J. & Post, R. M. (1989). Corpus callosum dimensions measured by magnetic resonance imaging in bipolar affective disorder and schizophrenia. Biological Psychiatry 26, 659668.CrossRefGoogle Scholar
Heckers, S., Heinsen, H., Heinsen, Y. C. & Beckmann, H. (1990). Limbic structures and lateral ventricle in schizophrenia: a quantitative postmortem study. Archives of General Psychiatry 47, 10161022.CrossRefGoogle ScholarPubMed
Holzman, P. S., Solomon, C. M., Levin, S. & Waternaux, C. S. (1984). Pursuit eye movement dysfunctions in schizophrenia. Family evidence for specificity. Archives of General Psychiatry 41, 136139.CrossRefGoogle ScholarPubMed
Iager, A.-C., Kirch, D. G. & Wyatt, R. J. (1985). A negative symptom rating scale. Psychiatry Research 16, 2736.CrossRefGoogle ScholarPubMed
Jablensky, A., Cooper, J. E., Tomov, T., Schwarz, R., Biehl, H., Giel, R., Ibrahim, H. H., Isele, R., Krumm, B., Ozturk, O. M., Savasir, I., Schubart, C. & Wiersma, D. (1985). A Procedure and Schedule for the Assessment of Disability in Patients with Severe Psychiatric Disorders. World Health Organization: Geneva.Google Scholar
Jernigan, T. L., Press, A. & Hesselink, J. R. (1990). Methods for measuring brain morphologic features on magnetic resonance images. Archives of Neurology 47, 2732.CrossRefGoogle ScholarPubMed
Jeste, D. V. & Lohr, J. B. (1989). Hippocampal pathological findings in schizophrenia. Archives of General Psychiatry 46, 10191024.CrossRefGoogle ScholarPubMed
Johnson, G., Miller, D. H., MacManus, D., Tofts, P., Barnes, D., du Boulay, E. P. & MacDonald, W. I. (1987). STIR sequences in NMR imaging of the optic nerve. Neuroradiology 29, 238245.CrossRefGoogle ScholarPubMed
Johnstone, E. C., Owens, D. G., Crow, T. J., Frith, C. D., Alexandropolis, K., Bydder, G. & Colter, N. (1989). Temporal lobe structure as determined by nuclear magnetic resonance in schizophrenia and bipolar affective disorder. Journal of Neurology, Neurosurgery, and Psychiatry 52, 736741.CrossRefGoogle ScholarPubMed
Kelsoe, J. R., Cadet, J. L., Pickar, D. & Weinberger, D. R. (1988). Quantitative neuroanatomy in schizophrenia. Archives of General Psychiatry 45, 533541.CrossRefGoogle ScholarPubMed
Kertesz, A., Black, S. E., Tokar, G., Benke, T., Carr, T. & Nicholson, L. (1988). Periventricular and subcortical hyperintensities on magnetic resonance imaging. Archives of Neurology 45, 404408.CrossRefGoogle ScholarPubMed
Khang-cheng, H., Roessman, U., Straumfjord, J. V. & Monroe, G. (1980). Analysis of brain weight. Archives of Pathology and Laboratory Medicine 104, 635645.Google Scholar
Lewis, S. W. (1990). Computerised tomography in schizophrenia 15 years on. British Journal of Psychiatry 157 (supp. 9), 1624.CrossRefGoogle Scholar
Lewis, S. W., Owen, M. J. & Murray, R. M. (1989). Obstetric complications and schizophrenia: methodology and mechanisms. In Schizophrenia – A Scientific Focus (ed. Schulz, S. C. and Tamminga, C. A.), pp. 5668. Oxford University Press: New York.Google Scholar
Lewis, S. W., Ford, R. A., Syed, G. M., Reveley, A. M. & Toone, B. K. (1992). A controlled study of 99mTc-HMPAO single-photon emission imaging in chronic schizophrenia. Psychological Medicine 22, 2735.CrossRefGoogle ScholarPubMed
McCarley, R. W., Faux, S. F., Shenton, M., LeMay, M., Cane, M., Ballinger, R. & Duffy, F. H. (1989). CT abnormalities in schizophrenia – a preliminary study of their correlation with P300/P200 electrophysiological features and positive/negative symptoms. Archives of General Psychiatry 46, 698708.CrossRefGoogle ScholarPubMed
McManus, D. G., Kermode, A. G. & Tofts, P. S. (1989). A repositioning technique for cerebral magnetic resonance imaging of patients with multiple sclerosis. Society of Magnetic Resonance in Medicine, Abstracts (Volume 2) of the 8th Annual Meeting, Amsterdam 1989, p. 617.Google Scholar
Marsh, L., Pearlson, G. D., Richards, S. S. & Barta, P. E. (1991). Structural brain changes in schizophrenia: MRI replication of a post-mortem study. Paper presented at the International Congress of Schizophrenia Research, 1991. Tucson, Arizona, 21–25 04.Google Scholar
Nasrallah, H. A., McCalley-Whitters, M. & Jacoby, C. G. (1982). Cortical atrophy in schizophrenia and mania: a comparative CT study. Journal of Clinical Psychiatry 43, 439441.Google Scholar
Nasrallah, H. A., Coffman, J. A., Schwartzkopf, S. B. & Olson, S. C. (1990). Reduced cerebral volume in schizophrenia. Schizophrenia Research 3, 17.CrossRefGoogle Scholar
Nauta, W. J. H. & Feirtag, M. (1986). Fundamental Neuroanatomy. W. H. Freeman and Co.: New York.Google Scholar
Nelson, H. E. (1982). National Adult Reading Test: Manual. Windsor: NFER-Nelson.Google Scholar
Nelson, H. E. & O'Connell, A. (1978). Dementia: the estimation of premorbid intelligence levels using the new adult reading test. Cortex 14, 234244.CrossRefGoogle ScholarPubMed
Norusis, M. J. (1988). SPSS/PC+ Advanced Statistics V2.0. SPSS Inc.: Chicago.Google Scholar
Pakkenberg, B. (1987). Post-mortem study of chronic schizophrenic brains. British Journal of Psychiatry 151, 744752.CrossRefGoogle ScholarPubMed
Pearlson, G. D., Kim, W. S., Kubos, K. L., Moberg, P. J., Jayaram, G., Bascom, M. J., Chase, G. A., Goldfinger, A. D. & Tune, L. E. (1989). Ventricle–brain ratio, computed tomographic density, and brain area in 50 schizophrenics. Archives of General Psychiatry 46, 690697.CrossRefGoogle ScholarPubMed
Pfefferbaum, A., Zipursky, R. B., Lim, K. O., Zatz, L. M., Stahl, S. M. & Jernigan, T. L. (1988). Computed tomographic evidence for generalized sulcal and ventricular enlargement in schizophrenia. Archives of General Psychiatry 45, 633640.CrossRefGoogle ScholarPubMed
Rieder, R. O., Donnelly, E. F., Herdt, J. R. & Waldman, I. N. (1979). Sulcal prominence in young chronic schizophrenic patients: CT scan findings associated with impairment on neuro-psychological tests. Psychiatry Research 1, 18.CrossRefGoogle Scholar
Rieder, R. O., Mann, L. S., Weinberger, D. R., van Kammen, D. P. & Post, R. M. (1983). Computed tomographic scans in patients with schizophrenia, schizo-affective and bipolar affective disorder. Archives of General Psychiatry 40, 735739.CrossRefGoogle Scholar
Robb, R. A. & Barillot, C. (1989). Interactive display and analysis of 3-D medical images. IEEE Transactions on Medical Imaging 8, 217226.CrossRefGoogle ScholarPubMed
Rossi, A., Stratta, P., de Cataldo, S., di Michele, V., Orfanelli, G., Serio, A., Petruzzi, C. & Casacchia, M. (1988). Cortical and subcortical computed tomographic study in schizophrenia. Journal of Psychiatric Research 22, 99105.CrossRefGoogle ScholarPubMed
Rossi, A., Stratta, P., D'Albenzio, L., Tartaro, A., Schiazza, G., Di Michele, V., Bolino, F. & Casacchia, M. (1990). Reduced temporal lobe areas in schizophrenia: preliminary evidence from a controlled multiplanar magnetic resonance imaging study. Biological Psychiatry 27, 6168.CrossRefGoogle ScholarPubMed
Scottish Schizophrenia Research Group (1989). The Scottish first episode schizophrenia study. VI. Computerised tomography brain scans in patients and controls. British Journal of Psychiatry 154, 492498.CrossRefGoogle Scholar
Seidman, L. J. (1983). Schizophrenia and brain dysfunction: an integration of recent neurodiagnostic findings. Psychological Bulletin 94, 195238.CrossRefGoogle ScholarPubMed
Serban, G., George, A., Siegel, S., DeLeon, M. & Gaffney, M. (1990). Computed tomography scans and negative symptoms in schizophrenia: chronic schizophrenics with negative symptoms and non-enlarged lateral ventricles. Acta Psychiatrica Scandinavica 81, 441447.CrossRefGoogle Scholar
Shelton, R. C., Karson, C. N., Doran, A. R., Pickar, D., Bigelow, L. B. & Weinberger, D. R. (1988). Cerebral structural pathology in schizophrenia: evidence for a selective prefrontal deficit. American Journal of Psychiatry 145, 154163.Google Scholar
Smith, R. C., Chaing, S. & Meyendorff, E. (1987). Magnetic resonance and computed tomographic studies of frontal lobe size and brain size in schizophrenia.Society of Magnetic Resonance in Medicine, Abstracts of the 6th Annual Meeting,New York1987, p. 286.Google Scholar
Spitzer, R. L., Endicott, J. & Robins, E. (1978). Research Diagnostic Criteria (RDC) for a Selected Group of Functional Psychoses. 3rd edn.Biometrics Research Division, New York State Psychiatric Institute: New York.Google Scholar
Stahl, S. M., Jernigan, T. L., Pfefferbaum, A. & Zatz, L. (1988). Brain computerized tomography in subtypes of severe chronic schizophrenia. Psychological Medicine 18, 7377.CrossRefGoogle ScholarPubMed
Stratta, P., Rossi, A., Galluci, M., Amicarelli, I., Passariello, R. & Casacchia, M. (1989). Hemispheric asymmetries and schizophrenia: a preliminary magnetic resonance imaging study. Biological Psychiatry 25, 275284.CrossRefGoogle ScholarPubMed
Suddath, R. L., Casanova, M. F., Goldberg, T. E., Daniel, D. G., Kelsoe, J. R. & Weinberger, D. R. (1989). Temporal lobe pathology in schizophrenia: a quantitative magnetic resonance imaging study. American Journal of Psychiatry 146, 464472.Google ScholarPubMed
Suddath, R. L., Christison, G. W., Fuller Torrey, E., Casanova, M. F. & Weinberger, D. R. (1990). Anatomical abnormalities in the brains of monozygotic twins discordant for schizophrenia. New England Journal of Medicine 322, 789794.CrossRefGoogle ScholarPubMed
Synek, V. & Reuben, J. R. (1976). The ventricular–brain ratio using planimetric measurement of EMI scans. British Journal of Radiology 49, 233237.CrossRefGoogle ScholarPubMed
Takahashi, R., Inabi, Y., Inanaga, K., Kato, N., Kumashiro, H., Nishimura, T., Okuma, T., Otsuki, S., Sakai, T., Sato, T. & Shimazono, Y. (1981). CT scanning and the investigation of schizophrenia. In Developments in Psychiatry, Volume 5 (ed. Perris, C., Struwe, G. and Jansson, B.), pp. 259268. Elsevier/North Holland Biomedical Press: Amsterdam.Google Scholar
Vita, A., Sacchetti, E., Calzeroni, A. & Cazullo, C. L. (1988). Cortical atrophy in schizophrenia: prevalence and associated features. Schizophrenia Research 1, 329337.CrossRefGoogle ScholarPubMed
Volkow, N. D., Wolf, A. P., Van Gelder, P., Brodie, J. D., Overall, J. E., Cancro, R. & Gomez-Mont, F. (1987). Phenomenological correlates of metabolic activity in 18 patients with chronic schizophrenia. American Journal of Psychiatry 144, 151158.Google ScholarPubMed
Waddington, J. L., O'Callaghan, E., Larkin, C., Redmond, O., Stack, J. & Ennis, J. T. (1990). Magnetic resonance imaging and spectroscopy in schizophrenia. British Journal of Psychiatry (supplement 9) 157, 5665.CrossRefGoogle Scholar
Weinberger, D. R., Fuller Torrey, E., Neophytides, A. N. & Wyatt, R. J. (1979). Structural abnormalities in the cerebral cortex of chronic schizophrenic patients. Archives of General Psychiatry 36, 935939.CrossRefGoogle ScholarPubMed
Weinberger, D. R., Cannon-Spoor, E., Potkin, S. G. & Wyatt, R. J. (1980). Poor premorbid adjustment and CT scan abnormalities in chronic schizophrenia. American Journal of Psychiatry 137, 14101413.Google ScholarPubMed
Weinberger, D. R., Berman, K. F. & Zec, R. F. (1986). Physiological dysfunction of dorsolateral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow evidence. Archives of General Psychiatry 43, 114124.CrossRefGoogle ScholarPubMed
Williams, A. O., Reveley, M. A., Kolakowska, T., Ardern, M. & Mandelbrote, B. M. (1985). Schizophrenia with good and poor outcome: cerebral ventricular size and its clinical significance. British Journal of Psychiatry 146, 239246.CrossRefGoogle ScholarPubMed
Wing, J. K., Cooper, J. E. & Sartorius, N. (1974). The Measurement and Classification of Psychiatric Symptoms. Cambridge University Press: Cambridge.Google Scholar
Wolkin, A., Angrist, B., Wolf, A. P., Brodie, J. D., Wolkin, B., Jaeger, J., Cancro, R. & Rotrosen, J. (1988). Low frontal glucose utilization in chronic schizophrenia: a replication study. American Journal of Psychiatry 145, 251253.Google ScholarPubMed
Zipursky, R. B., Lim, K. O., Sullivan, E. V., Brown, B. W. & Pfefferbaum, A. (1992). Widespread cerebral grey matter volume deficits in schizophrenia. Archives of General Psychiatry 49, 195205.CrossRefGoogle ScholarPubMed