Smaller anterior subgenual cingulate volume mediates the effect of girls’ early sexual maturation on negative psychobehavioral outcome
Naohiro Okada,
Noriaki Yahata,
Daisuke Koshiyama,
Kentaro Morita,
Kingo Sawada,
Sho Kanata,
Shinya Fujikawa,
Noriko Sugimoto,
Rie Toriyama,
Mio Masaoka,
Shinsuke Koike,
Tsuyoshi Araki,
Yukiko Kano,
Kaori Endo,
Syudo Yamasaki,
Shuntaro Ando,
Atsushi Nishida,
Mariko Hiraiwa-Hasegawa,
Kiyoto Kasai
Affiliations
Naohiro Okada
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan; International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo Institutes for Advanced Study (UTIAS), The University of Tokyo, Tokyo, Japan; Corresponding author. International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo Institutes for Advanced Study (UTIAS), The University of Tokyo, Tokyo, Japan.
Noriaki Yahata
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan; Institute for Quantum Life Science, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan; Department of Molecular Imaging and Theranostics, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan
Daisuke Koshiyama
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Kentaro Morita
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Kingo Sawada
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan; Office for Mental Health Support, Division for Counseling and Support, The University of Tokyo, Tokyo, Japan
Sho Kanata
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan; Department of Psychiatry, Teikyo University School of Medicine, Tokyo, Japan
Shinya Fujikawa
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Noriko Sugimoto
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Rie Toriyama
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Mio Masaoka
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Shinsuke Koike
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan; International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo Institutes for Advanced Study (UTIAS), The University of Tokyo, Tokyo, Japan; UTokyo Institute for Diversity and Adaptation of Human Mind (UTIDAHM), The University of Tokyo, Tokyo, Japan; UTokyo Center for Integrative Science of Human Behavior (CiSHuB), The University of Tokyo, Tokyo, Japan
Tsuyoshi Araki
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Yukiko Kano
UTokyo Institute for Diversity and Adaptation of Human Mind (UTIDAHM), The University of Tokyo, Tokyo, Japan; Department of Child Psychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Kaori Endo
Department of Psychiatry and Behavioral Sciences, Tokyo Metropolitan Institute of Medical Science, Tokyo, Japan
Syudo Yamasaki
Department of Psychiatry and Behavioral Sciences, Tokyo Metropolitan Institute of Medical Science, Tokyo, Japan
Shuntaro Ando
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan; Department of Psychiatry and Behavioral Sciences, Tokyo Metropolitan Institute of Medical Science, Tokyo, Japan
Atsushi Nishida
Department of Psychiatry and Behavioral Sciences, Tokyo Metropolitan Institute of Medical Science, Tokyo, Japan
Mariko Hiraiwa-Hasegawa
Department of Evolutionary Studies of Biosystems, School of Advanced Sciences, The Graduate University for Advanced Studies (SOKENDAI), Kanagawa, Japan
Kiyoto Kasai
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan; International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo Institutes for Advanced Study (UTIAS), The University of Tokyo, Tokyo, Japan; UTokyo Institute for Diversity and Adaptation of Human Mind (UTIDAHM), The University of Tokyo, Tokyo, Japan; UTokyo Center for Integrative Science of Human Behavior (CiSHuB), The University of Tokyo, Tokyo, Japan
Early-maturing girls are relatively likely to experience compromised psychobehavioral outcomes. Some studies have explored the association between puberty and brain morphology in adolescents, while the results were non-specific for females or the method was a region-of-interest analysis. To our knowledge, no large-scale study has comprehensively explored the effects of pubertal timing on whole-brain volumetric development or the neuroanatomical substrates of the association in girls between pubertal timing and psychobehavioral outcomes. We collected structural magnetic resonance imaging (MRI) data of a subsample (N = 203, mean age 11.6 years) from a large-scale population-based birth cohort. Tanner stage, a scale of physical maturation in adolescents, was rated almost simultaneously with MRI scan. The Strengths and Difficulties Questionnaire total difficulties (SDQ-TD) scores were rated by primary parents some duration after MRI scan (mean age 12.1 years). In each sex group, we examined brain regions associated with Tanner stage using whole-brain analysis controlling for chronological age, followed by an exploration of brain regions also associated with the SDQ-TD scores. We also performed mediation analyses. In girls, Tanner stage was significantly negatively correlated with gray matter volumes (GMVs) in the anterior/middle cingulate cortex (ACC/MCC), of which the subgenual ACC (sgACC) showed a negative correlation between GMVs and SDQ-TD scores. Smaller GMVs in the sgACC mediated the association between higher Tanner stages and higher SDQ-TD scores. We found no significant results in boys. Our results from a minimally biased, large-scale sample provide new insights into neuroanatomical correlates of the effect of pubertal timing on developmental psychological difficulties emerging in adolescence.
