Neuronal reference frames for social decisions in primate frontal cortex

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Abstract

Social decisions are crucial for the success of individuals and the groups that they comprise. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders such as autism and sociopathy. We examined the manner in which neurons in three frontal cortical areas encoded the outcomes of social decisions as monkeys performed a reward-allocation task. Neurons in the orbitofrontal cortex (OFC) predominantly encoded rewards that were delivered to oneself. Neurons in the anterior cingulate gyrus (ACCg) encoded reward allocations to the other monkey, to oneself or to both. Neurons in the anterior cingulate sulcus (ACCs) signaled reward allocations to the other monkey or to no one. In this network of received (OFC) and foregone (ACCs) reward signaling, ACCg emerged as an important nexus for the computation of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas.

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Figure 1: Reward-allocation task.
Figure 2: Behavior in the reward-allocation task.
Figure 3: Single neurons and population responses from ACCg.
Figure 4: Single neurons and population responses from ACCs and OFC.
Figure 5: Population biases for self, other and neither rewards.
Figure 6: Anatomical projections of recorded locations of all ACCg, ACCs and OFC cells.
Figure 7: Prosocial behavior and the fidelity of neuronal responses on other:neither trials.

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Acknowledgements

We thank J.M. Groh, J.M. Pearson, D.L. Barack, R.B. Ebitz, E.S. Bromberg-Martin, K.K. Watson and B.Y. Hayden for helpful discussions. We are very grateful to S.P. Wise and C. Padoa-Schioppa for insightful discussions and comments on earlier versions of the manuscript. We also thank M.L. Carlson for general technical assistance. This work was supported by a T32 Postdoctoral Training Grant on Fundamental and Translational Neuroscience (S.W.C.C., 2T32NS051156–06), a Ruth K. Broad Biomedical Foundation Postdoctoral Grant (S.W.C.C.), a Canadian Institutes of Health Research Doctoral research award (J.-F.G., 84765), the National Institute of Mental Health (M.L.P. and S.W.C.C., MH095894) and the Department of Defense (M.L.P. and S.W.C.C., W81XWH-11-1-0584).

Author information

S.W.C.C. and M.L.P. designed the study and wrote the paper. S.W.C.C. and J.-F.G. performed the experiments and S.W.C.C. analyzed the data.

Correspondence to Steve W C Chang.

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The authors declare no competing financial interests.

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Chang, S., Gariépy, J. & Platt, M. Neuronal reference frames for social decisions in primate frontal cortex. Nat Neurosci 16, 243–250 (2013) doi:10.1038/nn.3287

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