TY - JOUR
T1 - Neurometabolic underpinning of the intergenerational transmission of prosociality
AU - Okada, Naohiro
AU - Yahata, Noriaki
AU - Koshiyama, Daisuke
AU - Morita, Kentaro
AU - Sawada, Kingo
AU - Kanata, Sho
AU - Fujikawa, Shinya
AU - Sugimoto, Noriko
AU - Toriyama, Rie
AU - Masaoka, Mio
AU - Koike, Shinsuke
AU - Araki, Tsuyoshi
AU - Kano, Yukiko
AU - Endo, Kaori
AU - Yamasaki, Syudo
AU - Ando, Shuntaro
AU - Nishida, Atsushi
AU - Hiraiwa-Hasegawa, Mariko
AU - Edden, Richard A.E.
AU - Sawa, Akira
AU - Kasai, Kiyoto
N1 - Funding Information:
The pn-TTC project is currently working on making its MRI data available openly under the grant [Brain Mapping by Integrated Neurotechnologies for Disease Studies (Brain/MINDS) and Beyond] supported by Japan Agency for Medical Research and Development (AMED). The data supporting the findings of the current study can be requested by contacting the last author at kasaik-tky@umin.net. Applicants will be asked to fill out the data request form, which will be examined by the pn-TTC Data Resource Committee.The current work is a part of the Tokyo Teen Cohort Study. The authors would like to thank all researchers, investigators, and participants for their substantial support. The current work was supported by JSPS KAKENHI grant numbers JP16H06395 (K.K.), JP16H06398 (A.N.), JP16H06399 (K.K.), JP16K21720 (K.K.), JP16H06280 (K.K.), and JP17H04244 (K.K.); AMED, grant numbers JP19dm0307001 (K.K.), JP19dm0307004 (K.K.), and JP19dm0207069 (K.K.), MHLW Grant-in-Aid for Scientific Research, grant numbers JPMH19DA3001 (N.O.) and JPMH20DA1001 (N.O.); National Institutes of Health, grant numbers MH-094268 Silvio O. Conte Center (A.S.), MH-092443 (A.S.) and MH-105660 (A.S.). The current work was also partially supported by UTokyo Center for Integrative Science of Human Behavior (CiSHuB), and the International Research Center for Neurointelligence (WPI-IRCN) at the University of Tokyo Institutes for Advanced Study (UTIAS).
Funding Information:
The current work is a part of the Tokyo Teen Cohort Study. The authors would like to thank all researchers, investigators, and participants for their substantial support. The current work was supported by JSPS KAKENHI grant numbers JP16H06395 (K.K.), JP16H06398 (A.N.), JP16H06399 (K.K.), JP16K21720 (K.K.), JP16H06280 (K.K.), and JP17H04244 (K.K.); AMED , grant numbers JP19dm0307001 (K.K.), JP19dm0307004 (K.K.), and JP19dm0207069 (K.K.), MHLW Grant-in-Aid for Scientific Research, grant numbers JPMH 19DA3001 (N.O.) and JPMH20DA1001 (N.O.); National Institutes of Health , grant numbers MH-094268 Silvio O. Conte Center (A.S.), MH-092443 (A.S.) and MH-105660 (A.S.). The current work was also partially supported by UTokyo Center for Integrative Science of Human Behavior (CiSHuB), and the International Research Center for Neurointelligence (WPI-IRCN) at the University of Tokyo Institutes for Advanced Study (UTIAS).
Publisher Copyright:
© 2020 The Authors
PY - 2020/9
Y1 - 2020/9
N2 - 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.
AB - 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.
KW - Inhibitory/excitatory balance
KW - Intergenerational transmission
KW - MR spectroscopy
KW - Population neuroscience
KW - Prosociality
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UR - http://www.scopus.com/inward/citedby.url?scp=85085766474&partnerID=8YFLogxK
U2 - 10.1016/j.neuroimage.2020.116965
DO - 10.1016/j.neuroimage.2020.116965
M3 - Article
C2 - 32461150
AN - SCOPUS:85085766474
SN - 1053-8119
VL - 218
JO - NeuroImage
JF - NeuroImage
M1 - 116965
ER -