Unselfishness is one of the admired facilitators for human group endeavors, especially in times of urgent calls for global collaboration. Despite its importance, the neural dynamics behind its formation is scarcely understood. With 26 triads interacting as turn-taking pairs in a coordination game, we investigated reciprocal interactions in this tri-fMRI hyperscanning experiment. The critical role of the right temporal-parietal junction (rTPJ) was examined by adopting both time- and frequency-domain analyses. For the former, in the successful versus failed “reciprocity” contrast, brain regions associated with the mirror neuron system (MNS) and the mentalizing system (MS) were identified. In addition, the differences of connectivity between the rTPJ (seed region) and the abovementioned network areas (e.g., the right Inferior Parietal Lobule, rIPL) were negatively correlated with the individual reward. These results both verified the experimental design, which favored ‘reciprocal’ participants/triads with larger gains, and supported the opposition of rTPJ (other-) vs. rIPL (self-concerned) areas during successful social exchanges. Furthermore, the cerebral synchronization of the rTPJs emerged between the interacting pairs, and the coupling between the rTPJ and the right Superior Temporal Gyrus (rSTG) was found between those interacting simultaneously with others of the same group. These coherence findings not only echoed our previous findings, but also reinforced the hypotheses of the rTPJ-rTPJ coupling underpinning simultaneous collaboration and the rTPJ-rSTG coupling for decontextualized shared meaning emergence. Taken together, these results support two of the multi-functions (other-concerning and decontextualizing) subserved by the rTPJ, and highlight its interaction with other self-concerning brain areas in reaching co-benefits.