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

doi:10.1016/j.neuroimage.2020.116965

Neurometabolic underpinning of the intergenerational transmission of prosociality

Neuroimage. 2020 Sep:218:116965. doi: 10.1016/j.neuroimage.2020.116965. Epub 2020 May 24.

Authors

Naohiro Okada¹, Noriaki Yahata², Daisuke Koshiyama³, Kentaro Morita³, Kingo Sawada³, Sho Kanata⁴, Shinya Fujikawa³, Noriko Sugimoto³, Rie Toriyama³, Mio Masaoka³, Shinsuke Koike⁵, Tsuyoshi Araki³, Yukiko Kano⁶, Kaori Endo⁷, Syudo Yamasaki⁷, Shuntaro Ando⁸, Atsushi Nishida⁷, Mariko Hiraiwa-Hasegawa⁹, Richard A E Edden¹⁰, Akira Sawa¹¹, Kiyoto Kasai¹²

Affiliations

¹ 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. Electronic address: nokada-tky@umin.ac.jp.
² 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.
³ Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan.
⁴ Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan; Department of Psychiatry, Teikyo University School of Medicine, Tokyo, Japan.
⁵ 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.
⁶ Department of Child Psychiatry, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan.
⁷ Department of Psychiatry and Behavioral Sciences, Tokyo Metropolitan Institute of Medical Science, Tokyo, Japan.
⁸ 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.
⁹ Department of Evolutionary Studies of Biosystems, School of Advanced Sciences, The Graduate University for Advanced Studies (SOKENDAI), Kanagawa, Japan.
¹⁰ 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.
¹¹ 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.
¹² 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.

PMID: 32461150
DOI: 10.1016/j.neuroimage.2020.116965

Abstract

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.

Keywords: Inhibitory/excitatory balance; Intergenerational transmission; MR spectroscopy; Population neuroscience; Prosociality.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Adolescent
Adult
Brain Chemistry / physiology*
Child
Child, Preschool
Cohort Studies
Female
Glutamine / metabolism
Gyrus Cinguli / diagnostic imaging
Gyrus Cinguli / metabolism
Humans
Intergenerational Relations*
Longitudinal Studies
Magnetic Resonance Imaging
Magnetic Resonance Spectroscopy
Male
Mother-Child Relations
Parent-Child Relations
Personality
Puberty / physiology
Social Behavior*
Social Class
gamma-Aminobutyric Acid / metabolism

Substances

Glutamine
gamma-Aminobutyric Acid