Decreased number of orbital sulci in schizophrenia spectrum disorders

https://doi.org/10.1016/j.pscychresns.2016.03.005Get rights and content

Highlights

  • This MRI study examined the number of orbital sulci in the schizophrenia-spectrum.

  • Schizophrenia and schizotypal patients had a decreased number of orbital sulci.

  • Sulcus number was related to the severity of negative symptoms.

Abstract

An altered orbitofrontal sulcogyral pattern has been reported in the schizophrenia-spectrum, but it remains unknown whether they also have differences in the number of intermediate and posterior orbital sulci compared with healthy subjects. This magnetic resonance imaging study investigated the number of these sulci in 102 schizophrenia patients, 47 schizotypal disorder patients, and 84 controls. Both patient groups had a significantly lower number of both sulci bilaterally compared with controls, which was weakly associated with the severity of negative symptoms. Our results may reflect the neurodevelopmental pathology related to vulnerability to psychosis.

Introduction

Schizotypal (personality) disorder, which has attenuated forms of schizophrenic features without the manifestation of overt psychosis, is a prototypic disorder within the schizophrenia-spectrum. They are genetically related to schizophrenia and may share neurodevelopmental abnormalities with schizophrenia as a common neurobiological basis for vulnerability factors (Siever and Davis, 2004).

Altered surface morphology of the orbitofrontal cortex (OFC) has been reported in schizophrenia (Nakamura et al., 2007, Takayanagi et al., 2010, Cropley et al., 2015) and in genetic/clinical high-risk cohorts (Chakirova et al., 2010, Lavoie et al., 2014). These studies have mainly examined the sulcogyral pattern (i.e., variations in the ‘H-shaped’ sulcus defined by Chiavaras and Petrides (2000)), but recent studies have further demonstrated that the number of intermediate orbital sulci (IOS), which has considerable inter-individual variability, is decreased in first-episode (Bartholomeusz et al., 2013) or high-risk (Lavoie et al., 2014) subjects for psychosis. Lavoie et al. (2014) demonstrated that high-risk subjects were also characterized by a lower number of posterior orbital sulci (POS). Because the gross cortical folding patterns are largely established by birth (Chi et al., 1977), these findings may reflect neurodevelopmental anomalies related to a vulnerability to psychosis. Our recent study found no alteration of the H-shaped sulcogyral pattern in schizotypal patients (Nishikawa et al., 2016), but it remains unknown whether they exhibit the IOS/POS anomalies.

This magnetic resonance imaging (MRI) study investigated the number of IOS/POS in schizophrenia patients, schizotypal disorder patients, and healthy controls. Based on the concept of the schizophrenia-spectrum (Siever and Davis, 2004) as well as the findings of fewer IOS/POS in high-risk subjects regardless of future transition into psychosis (Lavoie et al., 2014), we predicted that schizotypal patients would share a lower number of IOS/POS with schizophrenia patients as a vulnerability marker.

Section snippets

Subjects

Forty-seven schizotypal disorder, 102 schizophrenia, and 84 healthy subjects were included (Table 1); their sample characteristics and the OFC H-shaped folding patterns have been described elsewhere (Nishikawa et al., 2016). All subjects were right-handed and physically healthy, and none had a lifetime history of serious head trauma, neurological illness, serious medical or surgical illness, or substance abuse.

The schizotypal patients were recruited from among the patients who visited our

Results

The schizophrenia and schizotypal patients had a significantly lower number of both IOS and POS bilaterally compared with controls, but there was no difference between both patient groups (Table 1). The schizotypal patients with left single-IOS had a trend toward higher total SANS score than those with left double-IOS [F (1,42)=3.70, p=0.061] (eFig. 2). In the schizophrenia and schizotypal patients as a whole, the patients with left absent-POS had significantly higher medication dose compared

Discussion

To our knowledge, this is the first MRI study to report the frequency of IOS/POS in both schizotypal and schizophrenia patients. We demonstrated that both patient groups had a decreased number of these sulci to the same degree as compared with control subjects and that such gross morphologic characteristic was weakly related to the negative symptoms.

Our finding of decreased IOS/POS is thought to reflect orbitofrontal neural underdevelopment, because secondary orbital sulci (IOS, POS, and other

Contributors

In this study, Drs. Suzuki and Takahashi conceived the idea and methodology of the study. Dr. Takahashi conducted the statistical analyses and wrote the manuscript. Drs. Takahashi, Furuichi, Kido, Nishikawa, Nakamura, and Sasabayashi recruited subjects, and were involved in clinical and diagnostic assessments. Drs. Takahashi and Nakamura analyzed the MRI data. Dr. Noguchi provided technical support for MRI scanning and data processing. Drs. Suzuki, Takahashi, and Takayanagi contributed to the

Conflict of interest

No conflicts of interest to declare.

Acknowledgments

This research was supported in part by Grants-in-Aid for Scientific Research (C) (No. 26461739) and Grants-in-Aid for Scientific Research (B) (No. 24390281) from the Japanese Society for the Promotion of Science, and Health and Labour Sciences Research Grants for Comprehensive Research on Persons with Disabilities from Japan Agency for Medical Research and Development (AMED).

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      The surface morphology of the orbitofrontal cortex (OFC) is also a potential neurodevelopmental marker because it is largely established by birth (Armstrong et al., 1995; Chi et al., 1977); schizophrenia patients are generally characterized by a shallower olfactory sulcus (Nishikawa et al., 2016; Takahashi et al., 2013a, 2014), decreased Type I and increased Type III expression in the variation of the OFC ‘H-shaped’ sulcus [Type I, II, and III; defined by Chiavaras and Petrides (2000)] (Chakirova et al., 2010; Nakamura et al., 2007; Takayanagi et al., 2010), as well as a decreased number of intermediate and posterior orbital sulci (IOS/POS) (Bartholomeusz et al., 2013; Takahashi et al., 2016). We have previously demonstrated that AI length and number of POS are related to the severity of negative symptoms in schizophrenia (Takahashi et al., 2008a, 2016). Further, nucleus accumbens atrophy (De Rossi et al., 2016) as well as microstructural disruption of the forceps minor (Spalletta et al., 2015) in deficit schizophrenia may imply significant role of the OFC abnormalities in this clinical subtype, because both of these structures are functionally and structurally connected with the OFC (Catani and Thiebaut de Schotten, 2008; Diekhof et al., 2012).

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