Increased structural covariance of cortical measures in individuals with an at-risk mental state

Daiki Sasabayashi; Sakiko Tsugawa; Shinichiro Nakajima; Tsutomu Takahashi; Yoichiro Takayanagi; Shinsuke Koike; Naoyuki Katagiri; Masahiro Katsura; Atsushi Furuichi; Yuko Mizukami; Shimako Nishiyama; Haruko Kobayashi; Yusuke Yuasa; Naohisa Tsujino; Atsushi Sakuma; Noriyuki Ohmuro; Yutaro Sato; Kazuho Tomimoto; Naohiro Okada; Mariko Tada; Motomu Suga; Norihide Maikusa; Eric Plitman; Cassandra M J Wannan; Andrew Zalesky; Mallar Chakravarty; Kyo Noguchi; Hidenori Yamasue; Kazunori Matsumoto; Takahiro Nemoto; Hiroaki Tomita; Masafumi Mizuno; Kiyoto Kasai; Michio Suzuki

doi:10.1016/j.pnpbp.2024.111197

Increased structural covariance of cortical measures in individuals with an at-risk mental state

Prog Neuropsychopharmacol Biol Psychiatry. 2024 Nov 22:136:111197. doi: 10.1016/j.pnpbp.2024.111197. Online ahead of print.

Authors

Daiki Sasabayashi¹, Sakiko Tsugawa², Shinichiro Nakajima³, Tsutomu Takahashi⁴, Yoichiro Takayanagi⁵, Shinsuke Koike⁶, Naoyuki Katagiri⁷, Masahiro Katsura⁸, Atsushi Furuichi⁴, Yuko Mizukami⁹, Shimako Nishiyama¹⁰, Haruko Kobayashi⁴, Yusuke Yuasa⁴, Naohisa Tsujino¹¹, Atsushi Sakuma¹², Noriyuki Ohmuro¹³, Yutaro Sato¹², Kazuho Tomimoto¹⁴, Naohiro Okada¹⁵, Mariko Tada¹⁵, Motomu Suga¹⁶, Norihide Maikusa¹⁷, Eric Plitman¹⁸, Cassandra M J Wannan¹⁹, Andrew Zalesky²⁰, Mallar Chakravarty²¹, Kyo Noguchi²², Hidenori Yamasue²³, Kazunori Matsumoto²⁴, Takahiro Nemoto⁷, Hiroaki Tomita²⁵, Masafumi Mizuno²⁶, Kiyoto Kasai¹⁵, Michio Suzuki⁴

Affiliations

¹ Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, 2630 Sugitani, Toyama city, Toyama 930-0194, Japan; Research Center for Idling Brain Science, University of Toyama, 2630 Sugitani, Toyama city, Toyama 930-0194, Japan. Electronic address: [email protected].
² Department of Neuropsychiatry, Keio University School of Medicine, 35 Shinano-machi, Shinjuku-ku, Tokyo 160-8582, Japan.
³ Department of Neuropsychiatry, Keio University School of Medicine, 35 Shinano-machi, Shinjuku-ku, Tokyo 160-8582, Japan; Brain Health Imaging Centre, Centre for Addiction and Mental Health, 250 College Street, Toronto, Ontario M5T 1R8, Canada.
⁴ Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, 2630 Sugitani, Toyama city, Toyama 930-0194, Japan; Research Center for Idling Brain Science, University of Toyama, 2630 Sugitani, Toyama city, Toyama 930-0194, Japan.
⁵ Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, 2630 Sugitani, Toyama city, Toyama 930-0194, Japan; Arisawabashi Hospital, 5-5 Hane-Shin, Toyama city, Toyama 939-2704, Japan.
⁶ The University of Tokyo Institute for Diversity and Adaptation of Human Mind, Komaba 3-8-1, Meguro-ku, Tokyo 153-8902, Japan; Center for Evolutionary Cognitive Sciences, Graduate School of Art and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902, Japan; International Research Center for Neurointelligence, The University of Tokyo Institutes for Advanced Study, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-0033, Japan.
⁷ Department of Neuropsychiatry, Toho University School of Medicine, 6-11-1 Omori-nishi, Ota-ku, Tokyo 143-8541, Japan.
⁸ Department of Psychiatry, Tohoku University Hospital, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan; Canal Kotodai General Mental Clinic, 2-4-8 Honcho, Aoba-ku, Sendai 980-0014, Japan.
⁹ Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, 2630 Sugitani, Toyama city, Toyama 930-0194, Japan.
¹⁰ Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, 2630 Sugitani, Toyama city, Toyama 930-0194, Japan; Center for Health Care and Human Sciences, University of Toyama, 3190 Gofuku, Toyama 930-8555, Japan.
¹¹ Department of Neuropsychiatry, Toho University School of Medicine, 6-11-1 Omori-nishi, Ota-ku, Tokyo 143-8541, Japan; Department of Psychiatry, Saiseikai Yokohamashi Tobu Hospital, 3-6-1 Shimosueyoshi, Tsurumi-ku, Yokohama, Kanagawa 230-8765, Japan.
¹² Department of Psychiatry, Tohoku University Hospital, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan.
¹³ Department of Psychiatry, Tohoku University Hospital, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan; Osaki Citizen Hospital, 3-8-1 Honami, Osaki, Miyagi 989-6183, Japan.
¹⁴ Department of Psychiatry, Tohoku University Graduate School of Medicine, 1-1, Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan.
¹⁵ International Research Center for Neurointelligence, The University of Tokyo Institutes for Advanced Study, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-0033, Japan; Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-8655, Japan.
¹⁶ Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-8655, Japan; Graduate School of Clinical Psychology, Teikyo Heisei University, 2-51-4 Higashi Ikebukuro, Toshima-ku, Tokyo 170-8445, Japan.
¹⁷ Center for Evolutionary Cognitive Sciences, Graduate School of Art and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902, Japan.
¹⁸ Department of Psychiatry, University of Toronto, 250 College Street, Toronto, Ontario M5T 1R8, Canada.
¹⁹ Melbourne Neuropsychiatry Centre, Department of Psychiatry, University of Melbourne, Melbourne, Grattan Street, Parkville, Victoria 3010, Australia; Orygen, Parkville, 35 Poplar Road, Parkville, Victoria 3052, Australia; Centre for Youth Mental Health, The University of Melbourne, 35 Poplar Road, Parkville, Victoria 3052, Australia.
²⁰ Melbourne Neuropsychiatry Centre, Department of Psychiatry, University of Melbourne, Melbourne, Grattan Street, Parkville, Victoria 3010, Australia; Melbourne School of Engineering, University of Melbourne, Melbourne, Grattan Street, Parkville, Victoria 3010, Australia.
²¹ Cerebral Imaging Center, Douglas Mental Health University Institute, McGill University, 6875 LaSalle Boulevard, Montreal, Quebec H4H 1R3, Canada; Department of Psychiatry, McGill University, 1033 Pine Avenue West, Montreal, Quebec H3A 1A1, Canada; Biological and Biomedical Engineering, McGill University, 3655 Promenade Sir-William-Osler, Montreal, Quebec H3G 1Y6, Canada.
²² Department of Radiology, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, 2630 Sugitani, Toyama City, Toyama 930-0194, Japan.
²³ Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-8655, Japan; Department of Psychiatry, Hamamatsu University School of Medicine, 1-20-1 Handayama, Hamamatsu 431-3192, Japan.
²⁴ Department of Psychiatry, Tohoku University Hospital, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan; Kokoro no Clinic OASIS, 17-27 Futsukamachi, Aoba-ku, Sendai 980-0802, Japan.
²⁵ Department of Psychiatry, Tohoku University Hospital, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan; Department of Psychiatry, Tohoku University Graduate School of Medicine, 1-1, Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan; Department of Disaster Psychiatry, International Research Institute of Disaster Science, Tohoku University, 468-1 Aoba, Aramaki, Aoba-ku, Sendai 980-8572, Japan.
²⁶ Department of Neuropsychiatry, Toho University School of Medicine, 6-11-1 Omori-nishi, Ota-ku, Tokyo 143-8541, Japan; Tokyo Metropolitan Matsuzawa Hospital, 2-1-1 Kamikitazawa, Setagaya-ku, Tokyo 156-0057, Japan.

PMID: 39579961
DOI: 10.1016/j.pnpbp.2024.111197

Abstract

An anomalous pattern of structural covariance has been reported in schizophrenia, which has been suggested to represent connectome changes during brain maturation and neuroprogressive processes. It remains unclear whether similar differences exist in a clinical high-risk state for psychosis, and if they are associated with a prodromal phenotype and/or later psychosis onset. This multicenter magnetic resonance imaging study cross-sectionally examined structural covariance in a large at-risk mental state (ARMS) sample with different outcomes. The whole-brain structural covariance of four cortical measures (thickness, area, volume, and gyrification) was assessed in 155 individuals with ARMS, who were subclassified into 26 (16.8 %) with a later psychosis onset (ARMS-P), 44 with persistent subthreshold psychotic symptoms, and 53 with the remission of psychotic symptoms (ARMS-R) during the clinical follow-up, and 191 healthy controls. The relationships of changes in structural covariance with clinical symptoms and cognitive impairments were also investigated in the ARMS subsample. Structural covariance was significantly higher in widespread cortical regions in the ARMS group than in the controls, with each cortical measure having a different pattern in affected cortical regions. The higher structural covariance of the cortical area was partly related to severe suspiciousness-persecutory ideation. Structural covariance was significantly higher, mainly in fronto-parietal gyrification, in the ARMS-P group than in the ARMS-R group. The present results suggest that changes in structural covariance result in psychosis vulnerability and the excessive structural covariance of brain gyrification in ARMS subjects may contribute to their later clinical course.

Keywords: At-risk mental state; Cortical measures; Individual differential structural covariance network; Magnetic resonance imaging; Multicenter; Structural covariance.