Neurometabolic and functional connectivity basis of prosocial behavior in early adolescence

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; Peter B. Barker; Akira Sawa; Kiyoto Kasai

doi:10.1038/s41598-018-38355-z

Neurometabolic and functional connectivity basis of prosocial behavior in early adolescence

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, Peter B. BarkerAkira Sawa, Kiyoto Kasai

School of Medicine

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Abstract

Human prosocial behavior (PB) emerges in childhood and matures during adolescence. Previous task-related functional magnetic resonance imaging (fMRI) studies have reported involvement of the medial prefrontal cortex including the anterior cingulate cortex (ACC) in social cognition in adolescence. However, neurometabolic and functional connectivity (FC) basis of PB in early adolescence remains unclear. Here, we measured GABA levels in the ACC and FC in a subsample (aged 10.5–13.4 years) of a large-scale population-based cohort with MR spectroscopy (MEGA-PRESS) and resting-state fMRI. PB was negatively correlated with GABA levels in the ACC (N = 221), and positively correlated with right ACC-seeded FC with the right precentral gyrus and the bilateral middle and posterior cingulate gyrus (N = 187). Furthermore, GABA concentrations and this FC were negatively correlated, and the FC mediated the association between GABA levels and PB (N = 171). Our results from a minimally biased, large-scale sample provide new insights into the neurometabolic and neurofunctional correlates of prosocial development during early adolescence.

Original language	English (US)
Article number	732
Journal	Scientific reports
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41598-018-38355-z
State	Published - Dec 1 2019

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Okada, N., Yahata, N., Koshiyama, D., Morita, K., Sawada, K., Kanata, S., Fujikawa, S., Sugimoto, N., Toriyama, R., Masaoka, M., Koike, S., Araki, T., Kano, Y., Endo, K., Yamasaki, S., Ando, S., Nishida, A., Hiraiwa-Hasegawa, M., Edden, R. A. E., ... Kasai, K. (2019). Neurometabolic and functional connectivity basis of prosocial behavior in early adolescence. Scientific reports, 9(1), Article 732. https://doi.org/10.1038/s41598-018-38355-z

Okada, N, Yahata, N, Koshiyama, D, Morita, K, Sawada, K, Kanata, S, Fujikawa, S, Sugimoto, N, Toriyama, R, Masaoka, M, Koike, S, Araki, T, Kano, Y, Endo, K, Yamasaki, S, Ando, S, Nishida, A, Hiraiwa-Hasegawa, M, Edden, RAE , Barker, PB , Sawa, A & Kasai, K 2019, 'Neurometabolic and functional connectivity basis of prosocial behavior in early adolescence', Scientific reports, vol. 9, no. 1, 732. https://doi.org/10.1038/s41598-018-38355-z

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abstract = "Human prosocial behavior (PB) emerges in childhood and matures during adolescence. Previous task-related functional magnetic resonance imaging (fMRI) studies have reported involvement of the medial prefrontal cortex including the anterior cingulate cortex (ACC) in social cognition in adolescence. However, neurometabolic and functional connectivity (FC) basis of PB in early adolescence remains unclear. Here, we measured GABA levels in the ACC and FC in a subsample (aged 10.5–13.4 years) of a large-scale population-based cohort with MR spectroscopy (MEGA-PRESS) and resting-state fMRI. PB was negatively correlated with GABA levels in the ACC (N = 221), and positively correlated with right ACC-seeded FC with the right precentral gyrus and the bilateral middle and posterior cingulate gyrus (N = 187). Furthermore, GABA concentrations and this FC were negatively correlated, and the FC mediated the association between GABA levels and PB (N = 171). Our results from a minimally biased, large-scale sample provide new insights into the neurometabolic and neurofunctional correlates of prosocial development during early adolescence.",

author = "Naohiro Okada and Noriaki Yahata and Daisuke Koshiyama and Kentaro Morita and Kingo Sawada and Sho Kanata and Shinya Fujikawa and Noriko Sugimoto and Rie Toriyama and Mio Masaoka and Shinsuke Koike and Tsuyoshi Araki and Yukiko Kano and Kaori Endo and Syudo Yamasaki and Shuntaro Ando and Atsushi Nishida and Mariko Hiraiwa-Hasegawa and Edden, {Richard A.E.} and Barker, {Peter B.} and Akira Sawa and Kiyoto Kasai",

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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 - Barker, Peter B.

AU - Sawa, Akira

AU - Kasai, Kiyoto

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Human prosocial behavior (PB) emerges in childhood and matures during adolescence. Previous task-related functional magnetic resonance imaging (fMRI) studies have reported involvement of the medial prefrontal cortex including the anterior cingulate cortex (ACC) in social cognition in adolescence. However, neurometabolic and functional connectivity (FC) basis of PB in early adolescence remains unclear. Here, we measured GABA levels in the ACC and FC in a subsample (aged 10.5–13.4 years) of a large-scale population-based cohort with MR spectroscopy (MEGA-PRESS) and resting-state fMRI. PB was negatively correlated with GABA levels in the ACC (N = 221), and positively correlated with right ACC-seeded FC with the right precentral gyrus and the bilateral middle and posterior cingulate gyrus (N = 187). Furthermore, GABA concentrations and this FC were negatively correlated, and the FC mediated the association between GABA levels and PB (N = 171). Our results from a minimally biased, large-scale sample provide new insights into the neurometabolic and neurofunctional correlates of prosocial development during early adolescence.

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Neurometabolic and functional connectivity basis of prosocial behavior in early adolescence

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