An MRI study of the superior temporal subregions in first-episode patients with various psychotic disorders
Introduction
Morphologic abnormalities of the superior temporal gyri (STG), which play a crucial role in auditory processing and language- and sociality-related functions (Gallagher and Frith, 2003, Pearlson, 1997), have been repeatedly described in previous magnetic resonance imaging (MRI) studies of schizophrenia (reviewed by Shenton et al., 2001). Gray matter reductions of the STG (Hirayasu et al., 1998, Kasai et al., 2003b, Keshavan et al., 1998, Kim et al., 2003) and its functionally relevant subregions [e.g., primary auditory cortex (Heschl gyrus, HG) or a neocortical language region (planum temporale, PT)] (Hirayasu et al., 2000, Kasai et al., 2003a) appear to be already present at first-episode of schizophrenia accompanied by further progressive changes during the early stages of illness (Kasai et al., 2003a, Kasai et al., 2003b, Takahashi et al., 2007), and these morphologic changes have been implicated in various psychotic symptoms such as auditory hallucinations or thought disorder (Barta et al., 1990, Rajarethinam et al., 2000, Shenton et al., 1992, Sumich et al., 2005, Takahashi et al., 2006). On the other hand, white matter findings of the STG in schizophrenia have been controversial; some MRI studies reported smaller STG white matter volume (O'Daly et al., 2007, Spalletta et al., 2003), whereas others found no changes (Antonova et al., 2005, Matsumoto et al., 2001, Sanfilipo et al., 2002, Suzuki et al., 2002) or even enlargement (Taylor et al., 2005). In addition, given the recent findings of smaller STG in schizotypal personality disorder (Goldstein, et al., 2009, Takahashi et al., 2006), it remains unclear whether the STG changes reported in schizophrenia are diagnostically specific or common to various psychotic disorders.
Several lines of evidence suggest that affective disorder with psychotic features is similar to schizophrenia genetically and neurobiologically, with more pronounced cognitive and structural brain abnormalities being evident in schizophrenia, although this view remains controversial (Maier et al., 2006, Murray et al., 2004). Although not consistently replicated (e.g., Morgan et al., 2007), previous MRI studies that directly compared brain morphology in these two major psychotic disorders have identified more gray matter deficits in schizophrenia, predominantly in fronto-temporolimbic-paralimbic regions (Hirayasu et al., 1998, Hirayasu et al., 2001, Kasai et al., 2003c, Koo et al., 2008, McDonald et al., 2005). On the other hand, some brain changes, such as ventricular enlargement, might be common to both disorders (Elkis et al., 1995, Nakamura et al., 2007, Strasser et al., 2005). Less is known about the white matter changes in psychotic disorders, but McDonald et al., 2004, McDonald et al., 2005 reported white matter reduction in the frontal and temporo-parietal regions for both disorders. Regarding the STG changes, previous studies suggested that schizophrenia but not affective psychosis exhibited gray matter reduction compared with controls (Hirayasu et al., 1998, Hirayasu et al., 2000, Kasai et al., 2003a, Kasai et al., 2003b), but these studies might be partly limited by lack of white matter investigation and relatively small sample size. Furthermore, to our knowledge, no MRI studies have specifically examined the STG changes in schizophreniform disorder, in which the psychotic episode has a duration of less than 6 months [DSM-III-R and -IV (American Psychiatric Association, 1987, American Psychiatric Association, 1994)].
The present study aimed to address the disease specificity of the STG morphologic changes within various psychotic disorders. We used MRI to measure the volumes of the STG (both gray and white matter) and its gray matter subregions [planum polare (PP), HG, PT, rostral STG, and caudal STG] in patients with first-episode psychoses (i.e., schizophrenia, affective psychosis, schizophreniform disorder, and other psychoses) and healthy controls. Based on previous MRI findings (Goldstein, et al., 2009, Hirayasu et al., 2000, Kasai et al., 2003a, Kasai et al., 2003b) and the potential role of the STG in clinical characteristics associated with schizophrenia spectrum (Rajarethinam et al., 2000), we hypothesized that only schizophrenia and schizophreniform patients would have STG gray matter reduction compared with controls.
Section snippets
Subjects
Patients with first-episode psychosis (FEP) (n = 162) and healthy controls (n = 62) participated in this study (Table 1). All participants in this study were screened for comorbid medical and psychiatric conditions by clinical assessment and physical and neurological examination (excluding a urine toxicology screen), although the healthy controls did not receive a structured diagnostic interview. Exclusion criteria were a lifetime history of serious head trauma, neurological illness, serious
Superior temporal gyrus volumes
MANCOVA of the absolute STG volume showed significant main effects for group [F (4, 212) = 8.43, p < 0.001] and tissue class [F (1, 214) = 4745.14, p < 0.001] and a significant interaction between them [F (4, 214) = 7.45, p < 0.001], with the schizophrenia patients having a smaller gray matter volume compared to all other groups (post hoc test, all p < 0.001), while white matter did not differ between the groups (post hoc test, all p > 0.319). There was also a significant tissue class × hemisphere interaction [F
Discussion
This region of interest (ROI)-based MRI study examined the volumes of the STG and its functionally relevant subregions in first-episode patients with various psychotic disorders. The schizophrenia patients had significantly smaller STG gray matter in bilateral HG, PT, and caudal STG compared with healthy controls, whereas the affective and schizophreniform psychosis patients as well as the ‘other psychoses’ group, which included small numbers of patients with less common diagnoses (e.g.,
Role of Funding Source
This study was supported by project grants from the National Health & Medical Research Council (NHMRC; grant IDs: 145627, 145737, 970598, 981112, 970391), NHMRC Program Grant (ID: 350241), and Colonial Foundation. DV and SJW were supported as Research Officers with funding from the NHMRC. PDM was supported by a NARSAD Distinguished Investigator Award. SJW is currently supported by a Clinical Career Development Award from the NHMRC (ID: 359223). TT was supported to undertake this work by a
Contributors
MS, DV, and CP conceived the idea and methodology of the study. TT conducted the statistical analyses and wrote the manuscript. SJW, PDM, DV, and CP recruited subjects, were involved in clinical and diagnostic assessments and for MRI scanning. TT and YK analyzed magnetic resonance imaging. BS provided technical support (data processing). All authors contributed in writing of the manuscript and have approved the final manuscript.
Conflict of interest
There are no conflicts of interest for any of the authors.
Acknowledgement
The authors are grateful to the clinical staff of the Early Psychosis Prevention and Intervention Centre (EPPIC) for their assistance in diagnostic and psychopathological assessments of the study participants.
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