Magnetic resonance texture analysis reveals stagewise nonlinear alterations of the frontal gray matter in patients with early psychosis

Molecular Psychiatry (2023)Cite this article

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Although gray matter (GM) abnormalities are present from the early stages of psychosis, subtle/miniscule changes may not be detected by conventional volumetry. Texture analysis (TA), which permits quantification of the complex interrelationship between contrasts at the individual voxel level, may capture subtle GM changes with more sensitivity than does volume or cortical thickness (CTh). We performed three-dimensional TA in nine GM regions of interest (ROIs) using T1 magnetic resonance images from 101 patients with first-episode psychosis (FEP), 85 patients at clinical high risk (CHR) for psychosis, and 147 controls. Via principal component analysis, three features of gray-level cooccurrence matrix – informational measure of correlation 1 (IMC1), autocorrelation (AC), and inverse difference (ID) – were selected to analyze cortical texture in the ROIs that showed a significant change in volume or CTh in the study groups. Significant reductions in GM volume and CTh of various frontotemporal regions were found in the FEP compared with the controls. Increased frontal AC was found in the FEP group compared to the controls after adjusting for volume and CTh changes. While volume and CTh were preserved in the CHR group, a stagewise nonlinear increase in frontal IMC1 was found, which exceeded both the controls and FEP group. Increased frontal IMC1 was also associated with a lesser severity of attenuated positive symptoms in the CHR group, while neither volume nor CTh was. The results of the current study suggest that frontal IMC1 may reflect subtle, dynamic GM changes and the symptomatology of the CHR stage with greater sensitivity, even in the absence of gross GM abnormalities. Some structural mechanisms that may contribute to texture changes (e.g., macrostructural cortical lamina, neuropil/myelination, cortical reorganization) and their possible implications are explored and discussed. Texture may be a useful tool to investigate subtle and dynamic GM abnormalities, especially during the CHR period.

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This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) and the KBRI basic research program through Korea Brain Research Institute, funded by the Ministry of Science & ICT (grant nos. 2019R1C1C1002457, 2020M3E5D9079910, and 21-BR-03-01).

Department of Public Health Service, Seoul National University Bundang Hospital, Seongnam, Republic of Korea

Sun Young Moon

Institute of Human Behavioral Medicine, Seoul National University Medical Research Center, Seoul, Republic of Korea

Sun Young Moon, Ki Woong Kim & Jun Soo Kwon

Department of Brain and Cognitive Science, Seoul National University College of Natural Science, Seoul, Republic of Korea

Hyungyou Park, Won Lee, Subin Lee, Ki Woong Kim & Jun Soo Kwon

Research and Development Division, 40FY Inc., Seongnam, Republic of Korea

Silvia Kyungjin Lho

Department of Neuropsychiatry, Seoul National University Hospital, Seoul, Republic of Korea

Minah Kim & Jun Soo Kwon

Department of Psychiatry, Seoul National University College of Medicine, Seoul, Republic of Korea

Minah Kim, Ki Woong Kim & Jun Soo Kwon

Department of Neuropsychiatry, Seoul National University Bundang Hospital, Seongnam, Republic of Korea

Ki Woong Kim

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JSK, KWK, and SYM conceived the project. SYM designed the study methodology and wrote the first manuscript with the help of all other authors. HP and WL performed MRI and texture analysis with the help of SL, KWK, and SYM. MK and JSK provided the resources and supervised the project. Review and editing of the first manuscript were performed by MK, JSK, and SYM.

Correspondence to Jun Soo Kwon.

The authors declare no competing interests.

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Moon, S.Y., Park, H., Lee, W. et al. Magnetic resonance texture analysis reveals stagewise nonlinear alterations of the frontal gray matter in patients with early psychosis. Mol Psychiatry (2023). https://doi.org/10.1038/s41380-023-02163-3

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Received: 15 December 2022

Revised: 13 June 2023

Accepted: 23 June 2023

Published: 27 July 2023

DOI: https://doi.org/10.1038/s41380-023-02163-3

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