Neurometabolic underpinning of the intergenerational transmission of prosociality
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,
Richard A.E. Edden,
Akira Sawa,
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
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; The University of Tokyo Institute for Diversity and Adaptation of Human Mind (UTIDAHM), The University of Tokyo, Tokyo, Japan
Tsuyoshi Araki
Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Yukiko Kano
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
Richard A.E. Edden
Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins University School of Medicine, Baltimore, MD, USA; F. M. Kirby Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, USA
Akira Sawa
Departments of Psychiatry, Neuroscience, Biomedical Engineering, and Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Department of Mental Health, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, USA
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
Parent-child personality transmission can occur via biological gene-driven processes as well as through environmental factors such as shared environment and parenting style. We recently revealed a negative association between prosociality, a highly valued personality attribute in human society, and anterior cingulate cortex (ACC) γ-aminobutyric acid (GABA) levels in children at the age of 10 years. We thus hypothesized that prosociality would be intergenerationally transmitted, and that transmission would be underwritten by neurometabolic heritability. Here, we collected prosociality data from children aged 10 years and their parents in a large-scale population-based birth cohort study. We also measured ACC GABA+ and glutamate plus glutamine (Glx) levels in a follow-up assessment with a subsample of the participants (aged 11 years) using magnetic resonance spectroscopy. We analyzed the associations among children’s and parents’ prosociality and GABA+/Glx ratios. We also examined the effect of socioeconomic status (SES) and verbalized parental affection (VPA) on these associations. We found a significant positive parent-child association for prosociality (N = 3026; children’s mean age 10.2 years) and GABA+/Glx ratio (N = 99; children’s mean age 11.4 years). There was a significant negative association between GABA+/Glx ratio and prosociality in both children (N = 208) and parents (N = 128). Our model accounting for the effects of neurometabolic heritability on prosociality transmission fitted well. Moreover, in this model, a significant positive effect of VPA but not SES on children’s prosociality was observed independently of the effect of neurometabolic transmission, while SES but not VPA was significantly associated with parental prosociality. Our results provide novel insights into the neurometabolic substrates of parent-child transmission of social behavior.
