Encoding of social state information by neuronal activities in the macaque caudate nucleus

Abstract

Social animals adjust their behavior according to social relationships and momentary circumstances. Dominant–submissive relationships modulate, but do not completely determine, their competitive behaviors. For example, a submissive monkey's decision to retrieve food depends not only on the presence of dominant partners but also on their observed behavior. Thus, behavioral expression requires a dynamic evaluation of reward outcome and momentary social states. The neural mechanisms underlying this evaluation remain elusive. The caudate nucleus (CN) plays a pivotal role in representing reward expectation and translating it into action selection. To investigate whether their activities encode social state information, we recorded from CN neurons in monkeys while they performed a competitive food-grab task against a dominant competitor. We found two groups of CN neurons: one primarily responded to reward outcome, while the other primarily tracked the monkey's social state. These social state-dependent neurons showed greater activity when the monkeys freely retrieved food without active challenges from the competitor and reduced activity when the monkeys were in a submissive state due to the competitor's active behavior. These results indicate that different neuronal activities in the CN encode social state information and reward-related information, which may contribute to adjusting competitive behavior in dynamic social contexts.

Keywords:

• Decision making
• Dominance
• Caudate nucleus
• Reward
• Social context

Acknowledgments

We thank A. Iriki for his overall generous support of this project; T. Higashi, U. Yamauchi, and T. Hashimoto for assistance with programming and analysis; T. Notoya for assistance with the experiments; and Dr K. Nakamura for helpful comments for revising an early draft of the manuscript. This work was supported by the 2006 RIKEN Strategic Program for R&D. H.N. was partially supported by KAKENHI grant 21300129 (Japan Society for the Promotion of Science), and KAKENHI grant 20020034 (Ministry of Education, Culture, Sports, Science, and Technology).

Notes

*These authors contributed equally to this work.