Neurometabolic and functional connectivity basis of prosocial behavior in early adolescence

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.

A Domain-General Developmental “Do-GooD” Network Model of Prosocial Cognition in Adolescence: A Systematic Review

“…Among the 25 included articles, seven reported prosocial neural correlates related to behaviors that were not imaged directly (see Table 1 , column “Prosocial Measure”). Two of these used the self-report Strengths and Difficulties Questionnaire’s (SDQ) prosocial subscale related to cortical thickness changes ( Ferschmann et al, 2019 ) and resting state functional connectivity ( Okada et al, 2019 ). The other five studies used a prosocial behavioral task after neuroimaging and related prior neural activations to subsequent prosociality ( Masten et al, 2010 ; Overgaauw et al, 2014 ; Tashjian et al, 2018 ; Tousignant et al, 2018 ; Spaans et al, 2020 ).…”

“…Eleven studies contrasted prosocial decision-making trials based on the actual prosocial choice such that decision-making with prosocial outcomes were compared to decision-making with non-prosocial outcomes (hereafter, “prosocial choices”) ( Telzer et al, 2011 , 2013 ; Güroğlu et al, 2014 ; Lemmers-Jansen et al, 2018 ; Schreuders et al, 2018 , 2019 ; Do and Telzer, 2019 ; Do et al, 2019 ; Spaans et al, 2020 ; van der Meulen et al, 2016 ; Brandner et al, 2021 ). Twelve studies analyzed neural activation during prosocial decision-making that correlated with the frequency of making prosocial choices, and therefore accounts for between-person differences (hereafter, “giving frequency” or “behavior frequency”) ( van den Bos et al, 2009 , 2011 ; Masten et al, 2010 ; Moor et al, 2012 ; Güroğlu et al, 2014 ; Overgaauw et al, 2014 ; Will et al, 2016 ; Schreuders et al, 2018 ; Tashjian et al, 2018 ; Tousignant et al, 2018 ; Ferschmann et al, 2019 ; Okada et al, 2019 ).…”

“…Studies also identified the ACC without the insula during prosocial decision-making ( van den Bos et al, 2011 ; Lemmers-Jansen et al, 2018 ; Will et al, 2018 ), prosocial choices ( Telzer et al, 2013 ), and prosocial choices when regressed with a prosocial questionnaire in young adults ( Telzer et al, 2011 ). Prosocial inclination also related to greater cortical thinning in the dACC across adolescent development ( Ferschmann et al, 2019 ) and greater resting state functional connectivity between the ACC and the bilateral PCC, middle cingulate cortex, and right precentral gyrus ( Okada et al, 2019 ). This same study also used magnetic resonance spectroscopy and found that gamma-aminobutyric acid (GABA) was the only neurotransmitter in the ACC to relate to prosocial inclination ( Okada et al, 2019 ).…”

“…Prosocial inclination also related to greater cortical thinning in the dACC across adolescent development ( Ferschmann et al, 2019 ) and greater resting state functional connectivity between the ACC and the bilateral PCC, middle cingulate cortex, and right precentral gyrus ( Okada et al, 2019 ). This same study also used magnetic resonance spectroscopy and found that gamma-aminobutyric acid (GABA) was the only neurotransmitter in the ACC to relate to prosocial inclination ( Okada et al, 2019 ).…”

“…Six studies found somatosensory regions related to prosocial behavior in the precentral gyri ( Schreuders et al, 2018 , 2019 ; Okada et al, 2019 ; Duell et al, 2021 ), the right postcentral gyrus ( Sakai et al, 2017 ; Schreuders et al, 2019 ; Duell et al, 2021 ), and the supplementary motor area ( Schreuders et al, 2018 ; Will et al, 2018 ). These findings were in both adolescents and young adults, and in studies focusing on prosocial decision-making, choices, frequency, and prosocial inclination from resting state functional connectivity.…”