Temporal lobe gray matter in schizophrenia spectrum: A volumetric MRI study of the fusiform gyrus, parahippocampal gyrus, and middle and inferior temporal gyri

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Abstract

Although several brain morphologic studies have suggested abnormalities in the temporal regions to be a common indicator of vulnerability for the schizophrenia spectrum, less attention has been paid to temporal lobe structures other than the superior temporal gyrus or the medial temporal region. In this study, we investigated the volume of gray matter in the fusiform gyrus, the parahippocampal gyrus, the middle temporal gyrus, and the inferior temporal gyrus using magnetic resonance imaging in 39 schizotypal disorder patients, 65 schizophrenia patients, and 72 age and gender matched healthy control subjects. The anterior fusiform gyrus was significantly smaller in the schizophrenia patients than the control subjects but not in the schizotypal disorder patients, while the volume reduction of the posterior fusiform gyrus was common to both disorders. Volumes for the middle and inferior temporal gyri or the parahippocampal gyrus did not differ between groups. These findings suggest that abnormalities in the posterior region of the fusiform gyrus are, as have been suggested for the superior temporal gyrus or the amygdala/hippocampus, prominent among the temporal lobe structures as a common morphologic substrate for the schizophrenia spectrum, whereas more widespread alterations involving the anterior region might be associated with the development of full-blown schizophrenia.

Introduction

Subjects with schizotypal features diagnosed as schizotypal disorder in ICD-10 (World Health Organization, 1992) or schizotypal personality disorder (SPD) in DSM-IV (American Psychiatric Association, 1994) share genetic, biological, and psychological commonalities with schizophrenia and are suggested to constitute a prototypic disorder for the schizophrenia spectrum (Siever et al., 1993, Siever and Davis, 2004). Previous studies concerning brain morphologic changes and cognitive characteristics in schizotypal subjects (reviewed by Dickey et al., 2002, Siever and Davis, 2004) and schizophrenia provided a theoretical model that the abnormalities in temporal regions are common to both groups as a neurobiological basis for vulnerability factors as part of the schizophrenia spectrum (Kurachi, 2003a, Kurachi, 2003b, Siever and Davis, 2004). More specifically, recent volumetric (Suzuki et al., 2005b, Takahashi et al., 2006) and voxel-based morphometric (VBM) (Kawasaki et al., 2004) magnetic resonance imaging (MRI) studies by our group have demonstrated the regional gray matter reductions for the superior temporal gyrus (STG) and the medial temporal lobe structures such as the amygdala and the hippocampus in schizotypal disorder patients to the same degree as those seen in schizophrenia patients. However, whether schizotypal subjects exhibit abnormalities in other temporal regions has yet to be elucidated.

The fusiform gyrus, or the occipitotemporal gyrus, is a spindle-shaped structure located on the ventral occipitotemporal surface and is selectively engaged in face recognition (George et al., 1999, Grill-Spector et al., 2004, Haxby et al., 2000, Haxby et al., 2002, Kanwisher et al., 1997) which has been reported to be disturbed in schizophrenia (Martin et al., 2003, Sachs et al., 2003). Although there have been relatively few morphologic studies of this region in schizophrenia, postmortem (McDonald et al., 2000) and MRI (Lee et al., 2002, Onitsuka et al., 2003) studies have reported volume reduction and its correlation with poor facial recognition. For schizotypal subjects, who exhibit face recognition deficits similar to schizophrenia patients (Conklin et al., 2002, Mikhailova et al., 1996, Poreh et al., 1994), only a single volumetric MRI study has examined the fusiform gyrus, and it found no significant volume changes in male SPD subjects (Dickey et al., 2003b). However, they have not taken into account the presumable differences in the connectivities and functions of the anterior versus posterior portions of the fusiform gyrus (George et al., 1999, Haxby et al., 2002, Kanwisher et al., 1997). Thus, more data on the volumetric changes of the fusiform gyrus in both schizophrenia and schizotypal patients are needed to evaluate the potential role of the fusiform gyrus in the neurobiology of the schizophrenia spectrum.

The middle and inferior temporal gyri, which contribute to visual recognition and are also related to speech perception (Hickok and Poeppel, 2004), have received less attention in the search for the neural substrate of schizophrenia. The only volumetric MRI study on these regions in schizophrenia revealed gray matter reductions in the left middle temporal gyrus and bilateral inferior temporal gyrus (Onitsuka et al., 2004), but most VBM studies found no significant gray matter changes (reviewed by Honea et al., 2005). For patients with SPD, Downhill et al. (2001) found a more marked reduction in temporal gray matter in the non-STG region, which includes the middle and inferior temporal gyri, than in the STG. To our knowledge, however, no volumetric MRI studies have specifically delineated the middle and inferior temporal gyri in schizotypal subjects.

The present study aimed to extend volumetric analyses of the temporal lobe in schizophrenia spectrum disorders to structures other than the STG and the medial temporal region. We used MRI to measure the volume of gray matter in the anterior and poster portions of the fusiform gyrus, the parahippocampal gyrus, the middle temporal gyrus, and the inferior temporal gyrus in schizophrenia patients, schizotypal disorder patients, and healthy controls. Based on previous VBM (Kawasaki et al., 2004) and volumetric (Dickey et al., 2003b) MRI studies, we predicted that volumetric changes in the temporal lobe in schizotypal disorder patients would be localized to the STG and the amygdala/hippocampus but would not be marked for the other temporal structures. We also examined whether these volumetric measures were related to clinical symptoms in schizophrenia and schizotypal disorder patients.

Section snippets

Subjects

Thirty-nine schizotypal disorder patients (24 males and 15 females), 65 schizophrenia patients (35 males and 30 females), and 72 control subjects (38 males and 34 females) were included in this study. The subjects were right-handed except for one female patient with schizotypal disorder of unknown handedness. Table 1 shows the demographic and clinical data of the subjects. MRI findings of the superior temporal sub-regions in the same group of subjects have been reported previously (Takahashi et

Volumes of ROIs

Table 2 shows the gray matter volumes for measured ROIs and results of MANCOVAs for the main effect of diagnosis. The effect involving gender was not significant for any region measured in this study. To demonstrate the regional volume changes within the temporal lobe in schizophrenia spectrum disorders, the previously published data of the hippocampus (Suzuki et al., 2005a, Suzuki et al., 2005b), the amygdala (Niu et al., 2004, Suzuki et al., 2005a, Suzuki et al., 2005b), the temporal pole (

Discussion

In this study, we demonstrated that the volume of gray matter in the posterior fusiform gyrus was reduced in both schizophrenia and schizotypal disorder patients compared with healthy controls, whereas a reduction in the volume of gray matter in the anterior fusiform was found only for schizophrenia patients. For the parahippocampal gyrus and the middle and inferior temporal gyri, as predicted, we found no significant reductions in gray matter in either disorder.

This study generally supports

Acknowledgements

This study was supported in part by a Grant-in-aid for Young Scientists 16790678 from the Ministry of Education, Culture, Sports, Science and Technology, Japan, and a Research Grant (11-3) for Nervous and Mental Disorders from the Ministry of Health and Welfare, Japan.

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