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 SawaKiyoto Kasai

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish (US)
Article number116965
JournalNeuroImage
Volume218
DOIs
StatePublished - Sep 2020

Keywords

  • Inhibitory/excitatory balance
  • Intergenerational transmission
  • MR spectroscopy
  • Population neuroscience
  • Prosociality

ASJC Scopus subject areas

  • Neurology
  • Cognitive Neuroscience

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