Computing Social Value Conversion in the Human Brain
- Haruaki Fukuda1,2,3,
- Ning Ma1,2,
- Shinsuke Suzuki1,2,4,5,
- Norihiro Harasawa1,2,
- Kenichi Ueno2,6,
- Justin L Gardner7,8,
- Noritaka Ichinohe9,
- Masahiko Haruno10,
- Kang Cheng5,11, and
- Hiroyuki Nakahara1,2,12
- 1Laboratory for Integrated Theoretical Neuroscience, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan
- 2RIKEN Center for Brain Science, Wako, Saitama 351-0198, Japan
- 3Department of General System Studies, The University of Tokyo, Meguro, Tokyo 153-8902, Japan
- 4Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Sendai, Miyagi 980-8578, Japan
- 5Institute of Development, Aging and Cancer, Tohoku University, Sendai, Miyagi 980-8575, Japan
- 6Support Unit for Functional Magnetic Resonance Imaging, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan
- 7Department of Psychology, Stanford University, Stanford, Stanford, California 94305-2025, USA
- 8Laboratory for Human Systems Neuroscience, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan
- 9Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo 187-8502, Japan
- 10Center for Information and Neural Networks, National Institute of Information and Communication Technology, Suita, Osaka 565-0871, Japan
- 11Laboratory for Cognitive Brain Mapping, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan
- 12Department of Intelligence Science and Technology, Kyoto University, Kyoto, Kyoto 606-8501, Japan
- Corresponding author: Hiroyuki Nakahara, PhD, Laboratory for Integrated Theoretical Neuroscience, RIKEN Center for Brain Science, Wako, Saitama 351-0198, Japan, E-mail: hiro{at}brain.riken.jp
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Author contributions: H.F., N.M., S.S., and H.N. designed research; H.F., N.H., K.U., and H.N. performed research; H.F. and N.M. analyzed data; H.F., N.M., and H.N. wrote the first draft of the paper; N.M. and H.N. wrote the paper; S.S., K.U., J.L.G., N.I., M.H., K.C., and H.N. edited the paper; J.L.G., N.I., and M.H. contributed unpublished reagents/analytic tools.
Abstract
Social signals play powerful roles in shaping self-oriented reward valuation and decision-making. These signals activate social and valuation/decision areas, but the core computation for their integration into the self-oriented decision machinery remains unclear. Here, we study how a fundamental social signal—social value (others' reward value)—is converted into self-oriented decision-making in the human brain. Using behavioral analysis, modeling, and neuroimaging, we show three-stage processing of social value conversion from the offer to the effective value and then to the final decision value. First, a value of others' bonus on offer, called offered value, was encoded uniquely in the right temporoparietal junction (rTPJ), and also in the left dorsolateral prefrontal cortex (ldlPFC), which is commonly activated by offered self-bonus value. The effective value, an intermediate value representing the effective influence of the offer on the decision, was represented in the right anterior insula (rAI), and the final decision value was encoded in the medial prefrontal cortex (mPFC). Second, using psychophysiological interaction (PPI) and dynamic causal modeling (DCM) analyses, we demonstrated three-stage feedforward processing; from the rTPJ and ldPFC to the rAI and then from rAI to the mPFC. Further, we showed that these characteristics of social conversion underlie distinct sociobehavioral phenotypes. We demonstrate that the variability in the conversion underlies difference between prosocial and selfish subjects, as seen from the differential strength of the rAI and ldlPFC coupling to the mPFC responses, respectively. Together, these findings identified fundamental neural computation processes for social value conversion underlying complex social decision-making behaviors.
SIGNIFICANCE STATEMENT
In daily life, we make decisions based on self-interest but also in consideration for others' status. These social influences modulate valuation and decision signals in the brain, suggesting a fundamental process called value conversion that translates social information into self-referenced decisions. However, little is known about the conversion process and its underlying brain mechanisms. We investigated value conversion using human fMRI with computational modeling and found three essential stages in a progressive brain circuit from social to empathic and decision areas. Interestingly, the brain mechanism of conversion differed between prosocial and individualistic subjects. These findings reveal how the brain processes and merges social information into the elemental flow of self-interested decision-making.
Footnotes
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The authors declare no competing financial interests.
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This work was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI grants (26120732 and 16H06570 to H.N.). We thank C. Yokoyama and Y. Mochizuki for helpful discussions and comments on the manuscript, and Drs. T. Asamizuya and C. Suzuki for technical assistance with the fMRI experiments.
- Received December 5, 2018.
- Revision received March 30, 2019.
- Accepted April 14, 2019.
- Copyright © 2019 the authors





