Prosocial behavior toward estranged persons modulates the interaction between midline cortical structures and the reward system

ABSTRACT

Good reputation enhances positive self-image, which motivates prosocial behavior, a phenomenon known as indirect reciprocity. Thus, good reputation should promote prosocial behavior toward estranged people to whom affective responses leading to direct reciprocity are suppressed. We predicted that such behaviors involve an interrelationship between self-image, processed in the medial prefrontal cortex (mPFC) and precuneus, and social reward, processed in the reward system. To test our hypothesis, we performed fMRI on 21 participants during a virtual ball-toss game after subjects formed negative impressions (estrangement) or neutral impressions of other players. During some blocks of the game, the other players did not receive tosses, and participants could increase tosses to them (i.e. engage in prosocial behavior). Participants significantly increased tosses to all isolated players; therefore, prosocial behavior occurred irrespective of estrangement. Prosocial behavior toward estranged players enhanced positive self-image and increased activation of the anterior mPFC and precuneus. The precuneus exhibited enhanced functional connectivity with the striatum. Thus, a positive self-image, represented by an interaction between the midline cortical structures and striatum, plays key roles in prosocial behavior toward estranged people.

KEYWORDS:

• Fmri
• prosocial behavior
• impression
• midline cortical structure
• self-image

Acknowledgments

We wish to thank M. Matsunaga, K. Yoshihara, and T. Koike for their assistance and thoughtful comments throughout the study. This study was partly supported by Grant-in-Aid for Scientific Research (S) no. 21220005 (N.S.), Grant-in-Aid for Scientific Research (A) no. 15H01846 (N.S.), Grant-in-Aid for Challenging Exploratory Research no. 16K13488 (H.K.), and Grants-in-Aid for Young Scientists (B) no. 25750407 (H.K.) and no. 15K21602 (S.K.S.) from the Japan Society for the Promotion of Science. Part of this study was an aspect of the “Development of biomarker candidates for social behavior” project, carried out under the Strategic Research Program for Brain Sciences of the Ministry of Education, Culture, Sports, Science and Technology of Japan. This study was supported by the Cooperative Study Program of the National Institute for Physiological Sciences.

Disclosure statement

No potential conflict of interest was reported by the authors.

Authors’ contributions

H.K. designed the experiments, conducted the experiments, analyzed the experimental data, and wrote the manuscript. S.K.S. designed and conducted the experiments. Y.H.H. and K.M participated in experimental design and conducted the experiments. T.K., Y.K., Y.O., and S.S. participated in experimental design and discussion of the analyzed data. N.S. supervised the overall project and edited the manuscript.

Additional information

Funding

This work was supported by the Japan Society for the Promotion of Science [Grant-in-Aid for Challenging Exploratory Research,Grant-in-Aid for Scientific Research (A) no. 15H01,Grant-in-Aid for Scientific Research (S) no. 21220,Grants-in-Aid for Young Scientists (B) no. 15K2160,Grants-in-Aid for Young Scientists (B) no. 2575040]; Ministry of Education, Culture, Sports, Science and Technology [“Development of biomarker candidates for social behavior"]; the Strategic Research Program for Brain Sciences from Japan Agency, AMED [JP18dm010715h0003].