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Rightward Cerebral Asymmetry in Subtypes of Schizophrenia

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Rightward Cerebral Asymmetry in Subtypes of Schizophrenia Psychiatry Research: Neuroimaging 123 (2003) 65–79 Rightward cerebral asymmetry in subtypes ofschizophrenia according to Leonhard’s classification and to DSM-IV: a structural MRI study Paulo C. Salletaa , Helio Elkis , Taniaˆ´ M. Alves a , Jose R. Oliveira aa , Erlei Sassi , Claudio Campi de Castrobaa , Geraldo F. Busatto , Wagner F. Gattaz, * aDepartment of Psychiatry, Faculty of Medicine, University of Sao˜ Paulo, Rua Ovidio Pires de Campos syn, Sao˜ Paulo CEP 05403-010, Brazil bDepartment of Radiology, Faculty of Medicine, University of Sao˜ Paulo, Rua Ovidio Pires de Campos syn, Sao˜ Paulo CEP 05403-010, Brazil Received 25 February 2002; received in revised form 16 October 2002; accepted 12 November 2002 Abstract Although well documented, brain structural abnormalities in schizophrenia are non-specific, and morphometric parameters show significant overlap between patients and healthy controls. Such inconsistencies in neuroimaging findings could represent different levels of severity along a single pathogenic process or distinct clinical and etiopathological psychoses within a schizophrenic spectrum. The aim ofthe present study was the investigation of distinct brain abnormalities in different subtypes of schizophrenia. Forty patients were classified according to DSM- IV and Leonhard’s classifications. Psychopathology was assessed by the Positive and Negative Syndrome Scale (PANSS) and the Negative Symptom Rating Scale (NSRS). Patients were compared to 20 healthy volunteers on volumetric measures ofcerebral structures (hemisphere, hippocampus and planum temporale) and ventricular–brain ratio (VBR) obtained by magnetic resonance imaging. Patients showed rightward asymmetry ofcerebral hemispheres and increased VBR. Rightward asymmetry correlated with severity ofnegative symptoms and prevailed in the systematic forms of Leonhard, suggesting a distinct pattern of left hemisphere abnormality in this subgroup of psychoses. Increased VBR values showed a single normal distribution in the subgroups, indicating that ventricular enlargement is not restricted to a subgroup but is present to a certain degree in all cases. ᮊ 2003 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Schizophrenia; Magnetic resonance imaging; Morphometry; Subtyping; Symptoms 1. Introduction is associated with brain structural abnormalities. The most robust findings are enlargement of lateral In the last decades, cumulating evidence from and third ventricles, decreased brain volume, vol- neuroimaging studies has shown that schizophrenia umetric reduction in temporal lobe and limbic structures, and decreased volumes ofsubcortical *Corresponding author. Tel.: q55-11-3062-9029; fax: q55- structures such as the caudate and thalamus in 11-3083-6588. neuroleptic-naive patients (Harrison, 1999; Shen- ( ) E-mail address: [email protected] W.F. Gattaz . ton et al., 2001). 0925-4927/03/$ - see front matter ᮊ 2003 Elsevier Science Ireland Ltd. All rights reserved. PII: S0925-4927Ž03.00020-9 66 P.C. Sallet et al. / Psychiatry Research: Neuroimaging 123 (2003) 65–79 With reference to the timing of brain changes, 1999) or the psychoses ofthe schizophrenia spec- ventricular enlargement and cortical volume reduc- trum constitute distinct clinical and etiopathologi- tion are already present in first-episode patients cal groups (Tsuang and Faraone, 1995; Franzek (Gur et al., 1998; Zipursky et al., 1998), and the and Beckmann, 1998). absence ofgliosis and other neurodegenerative Karl Leonhard (1904–1988) developed his clas- abnormalities (Harrison, 1997) favors the neuro- sification of psychoses based on previous works developmental hypothesis ofschizophrenia. More ofWernicke (1900) and Kleist (1934) that empha- controversial is the question ofwhether such sized the association between particular forms of changes are static (Jaskiw et al., 1994; Vita et al., schizophrenia and abnormalities ofbrain systems, 1997), progressive (Gattaz et al., 1981; DeLisi et in analogy to the anatomofunctional substrate of al., 1997) or a combination ofboth (Gur et al., neurological degenerative disorders (Leonhard, 1998). 1995). In the case ofneurological degenerative Using MRI, standardized measurements have disorders, even when anatomopathological meth- been developed to identify other putative brain ods do not allow the identification of an organic structural abnormalities in schizophrenic patients. substrate, it is possible to identify a regular clinical The planum temporale (PT) is believed to consist syndrome related to the affected neurological sys- ofthe association auditory cortex, which is related tem (e.g. the pyramidal tract syndrome in spastic to the integration and processing oflanguage palsy). In the case ofschizophrenia, the anatomic (Shapleske et al., 1999). The most right-handed substrates are unknown or very imprecise, but we healthy individuals have the left PT larger than can recognize defect state syndromes (‘Defektzu- the right PT, reflecting the physiologic asymmetry stand Syndrome’) composed ofregular and specif- ofregions involved in language processing ic symptomatological complexes (‘Symptom- (Geschwind and Levitsky, 1968). Several MRI verbande’¨ ), which point to differently disturbed studies with schizophrenic patients have demon- ‘psychic systems’. However, in comparison with strated symmetry or reversed asymmetry ofthe PT neurological disorders, these systems are connected (Kwon et al., 1999; Hirayasu et al., 2000). Others with more extended functional areas and, hence, have found associations between reversed asym- structural deficits should be too diffuse in brain metry ofthe PT and severity ofpsychotic symp- areas to be easily detected (Leonhard, 1970). Such toms (Rossi et al., 1994; Flaum et al., 1995; Petty statements are particularly pertinent to the so- et al., 1995), raising the hypothesis that some called systematic schizophrenias (SS), which schizophrenic symptoms could result from dis- according to Leonhard show insidious onset, pro- turbed functional lateralization of brain areas relat- gressive course and well-delimited symptomatolo- ed to language. Nevertheless, several studies gy. On the other hand, non-systematic forms (NSS) reported negative findings, either with reference to show a multiplicity ofsymptoms, frequently the hypothesis ofreversed asymmetry (Kulynych including elements characteristic ofother psycho- et al., 1995; O’Leary et al., 1995; Frangou et al., ses, such as cycloid and manic-depressive psycho- 1997) or to the correlation with symptomatology ses and other non-systematic forms. In contrast to (DeLisi et al., 1994; Kleinschmidt et al., 1994; SS, NSS forms present periods of crisis intermin- Barta et al., 1997). gled with periods ofpartial remission, and bipolar Indeed, those morphometric changes are non- characteristics at the level ofcertain functionssuch specific, showing significant overlap between as affect, formal thought and psychomotor schizophrenia and other neuropsychiatric condi- functions. tions, and even for the most robust findings there A previous MRI study involving endogenous are a number ofstudies reporting negative results. psychoses defined according to Leonhard’s classi- Such inconsistencies raise the question whether fication showed that SS had reduced temporal lobe ‘schizophrenia’ is a single disease with different volumes compared with NSS (Serfling et al., levels ofseverity along a pathogenetic continuum 1995). According to the low genetic risk and high (Goldberg and Weinberger, 1995; Andreasen, incidence ofmaternal infectionsobserved in sys- P.C. Sallet et al. / Psychiatry Research: Neuroimaging 123 (2003) 65–79 67 tematic forms (Franzek and Beckmann, 1996; daily dose of811 mg (S.D. "425)(American Stober¨ et al., 1994, 1997), Serfling and colleagues Psychiatric Association, 1997). Exclusion criteria (1995) interpreted the finding of volumetric reduc- were: (a) age lower than 18 or greater than 60 tion in the temporal lobes as evidence ofexoge- years; (b) history ofsubstance dependence; and nous damage acting on brain development. (c) history ofhead trauma, degenerative neurolog- It is possible that the inconsistencies in neuroim- ical disorders and previous treatment with steroid aging findings reflect the heterogeneity of the medication. A control group of20 healthy volun- studied populations. As far as psychopathology is teers, recruited from the community, was selected concerned in the search for more homogeneous using the same exclusion criteria above (based on subgroups, we predicted that a diagnostic system the SCID-IyP interview). A written informed con- grounded also in the longitudinal course ofsymp- sent was obtained from all subjects before partici- toms (Leonhard’s classification) would provide pation. Local research and ethics committees more validity than the cross-sectional criteria approved the study. adopted in the diagnostic decision ofDSM-IV Current symptom severity was measured using subtypes. Therefore, we performed the present the Positive and Negative Syndrome Scale study to investigate commonly reported brain mor- (PANSS)(Kay et al., 1987) and the Negative phologic abnormalities associated with schizophre- Symptom Rating Scale (NSRS)(Iager et al., nia in discrete subgroups ofschizophrenic patients 1985). Handedness was assessed with the Hand- classified according to Leonhard, compared to the edness Inventory (Briggs and Nebes, 1975). All DSM-IV subgroups. the patients were receiving stable doses ofanti- psychotics at the time ofthe study. Clinical ratings 2. Methods were
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