Neural mechanisms of social decision-making in the primate amygdala
Edited by Michael S. Gazzaniga, University of California, Santa Barbara, CA, and approved November 9, 2015 (received for review July 26, 2015)
Significance
Making social decisions requires evaluation of benefits and costs to self and others. Long associated with emotion and vigilance, neurons in primate amygdala also signal reward and punishment as well as information about the faces and eyes of others. Here we show that neurons in the basolateral amygdala signal the value of rewards for self and others when monkeys make social decisions. These value-mirroring neurons reflected monkeys’ tendency to make prosocial decisions on a momentary as well as long-term basis. We also found that delivering the social peptide oxytocin into basolateral amygdala enhances both prosocial tendencies and attention to the recipients of prosocial decisions. Our findings endorse the amygdala as a critical neural nexus regulating social decisions.
Abstract
Social decisions require evaluation of costs and benefits to oneself and others. Long associated with emotion and vigilance, the amygdala has recently been implicated in both decision-making and social behavior. The amygdala signals reward and punishment, as well as facial expressions and the gaze of others. Amygdala damage impairs social interactions, and the social neuropeptide oxytocin (OT) influences human social decisions, in part, by altering amygdala function. Here we show in monkeys playing a modified dictator game, in which one individual can donate or withhold rewards from another, that basolateral amygdala (BLA) neurons signaled social preferences both across trials and across days. BLA neurons mirrored the value of rewards delivered to self and others when monkeys were free to choose but not when the computer made choices for them. We also found that focal infusion of OT unilaterally into BLA weakly but significantly increased both the frequency of prosocial decisions and attention to recipients for context-specific prosocial decisions, endorsing the hypothesis that OT regulates social behavior, in part, via amygdala neuromodulation. Our findings demonstrate both neurophysiological and neuroendocrinological connections between primate amygdala and social decisions.
Acknowledgments
This work was supported by National Institute for Mental Health R00-MH099093 (to S.W.C.C.); Simons Foundation 304935 (to M.P.); R01-MH095894 (to M.L.P., S.W.C.C., and A.V.U.); T32 Postdoctoral Training Grant (to K.T.); Department of Defense Grant W81XWH-11-1-0584 (to M.L.P. and S.W.C.C.); National Institute for Environmental Health Sciences Big Data to Knowledge Career Award K01-ES-025442-01 (to J.M.P.); JSPS Postdoctoral Fellowships for Research Abroad (to K.T.); and the Uehara Memorial Foundation (K.T.).
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Cover image: Pictured is a snapshot of a dog lapping water, showing the backward curl of the dog's tongue and the column of water drawn up when the tongue retracts. Sean Gart et al. constructed a physical model of tongue–water interactions that occur when dogs drink. The model showed that dogs time their bite to coincide with the moment when the water column pinches off from the tongue, thus maximizing the water intake per bite. The model also suggests that curling the tongue might increase the size of the water column by increasing the surface area of the tongue in contact with the water. See the article by Gart et al. on pages 15798–15802. Image courtesy of John J. Socha, Sean Gart, and Sunghwan Jung.
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Freely available online through the PNAS open access option.
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Published online: December 14, 2015
Published in issue: December 29, 2015
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Acknowledgments
This work was supported by National Institute for Mental Health R00-MH099093 (to S.W.C.C.); Simons Foundation 304935 (to M.P.); R01-MH095894 (to M.L.P., S.W.C.C., and A.V.U.); T32 Postdoctoral Training Grant (to K.T.); Department of Defense Grant W81XWH-11-1-0584 (to M.L.P. and S.W.C.C.); National Institute for Environmental Health Sciences Big Data to Knowledge Career Award K01-ES-025442-01 (to J.M.P.); JSPS Postdoctoral Fellowships for Research Abroad (to K.T.); and the Uehara Memorial Foundation (K.T.).
Notes
This article is a PNAS Direct Submission.
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Competing Interests
The authors declare no conflict of interest.
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