Abstract
Previous magnetic resonance imaging (MRI) studies reported increased brain gyrification in schizophrenia and schizotypal disorder, a prototypic disorder within the schizophrenia spectrum. This may reflect deviations in early neurodevelopment; however, it currently remains unclear whether the gyrification pattern longitudinally changes over the course of the schizophrenia spectrum. The present MRI study using FreeSurfer compared longitudinal changes (mean inter-scan interval of 2.7 years) in the local gyrification index (LGI) in the entire cortex among 23 patients with first-episode schizophrenia, 14 with schizotypal disorder, and 39 healthy controls. Significant differences were observed in longitudinal LGI changes between these groups; the schizophrenia group exhibited a progressive decline in LGI, predominantly in the fronto-temporal regions, whereas LGI increased over time in several brain regions in the schizotypal and control groups. In the schizophrenia group, a greater reduction in LGI over time in the right precentral and post central regions correlated with smaller improvements in negative symptoms during the follow-up period. The cumulative medication dosage during follow-up negatively correlated with a longitudinal LGI increase in the right superior parietal area in the schizotypal group, but did not affect longitudinal LGI changes in the schizophrenia group. Collectively, these results suggest that gyrification patterns in the schizophrenia spectrum reflect both early neurodevelopmental abnormalities as a vulnerability factor and active brain pathology in the early stages of schizophrenia.
Highlights
Brain gyrification is regarded as an early neurodevelopmental marker of cortical complexity because its pattern is genetically mediated (Bartley et al, 1997) and it undergoes the greatest development during pregnancy but remains rather stable after birth (Armstrong et al, 1995; Zilles et al, 2013)
Since the cortical surface may flatten during adolescence as a late neurodevelopmental process (Alemán-Gómez et al, 2013), this longitudinal decline appears to be consistent with the notion that a progressive brain pathology in the early stages of psychosis is associated with the acceleration of normal brain maturational processes (Pantelis et al, 2007)
There were no significant differences in baseline local gyrification index (LGI) between the combined patient group and control group
Summary
Brain gyrification is regarded as an early neurodevelopmental marker of cortical complexity because its pattern is genetically mediated (Bartley et al, 1997) and it undergoes the greatest development during pregnancy but remains rather stable after birth (Armstrong et al, 1995; Zilles et al, 2013). Increased brain gyrification in the frontal and other cortical regions was detected in individuals with genetic (Falkai et al, 2007; Neilson et al, 2018) and clinical risk for the development of psychosis (Tepest et al, 2013; Sasabayashi et al, 2017b) and in patients with schizotypal disorder (Sasabayashi et al, 2020), who share biological commonalities with schizophrenia patients as part of the schizophrenia spectrum in the context of the neurodevelopmental hypothesis but are mostly spared from developing overt psychosis (Siever and Davis, 2004) These findings support brain hypergyrification being an early developmental trait marker associated with vulnerability to psychosis (Sasabayashi et al, 2021). To the best of our knowledge, potential changes in gyrification over time have not yet been investigated in schizotypal patients using MRI
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