Original Research ARTICLE

Front. Neurosci., 03 March 2011 | doi: 10.3389/fnins.2011.00027

Vicarious reinforcement in rhesus macaques (Macaca mulatta)

Steve W. C. Chang1,2*, Amy A. Winecoff1 and Michael L. Platt1,2,3,4
  • 1 Center for Cognitive Neuroscience, Duke University, Durham, NC, USA
  • 2 Department of Neurobiology, Duke University, Durham, NC, USA
  • 3 Department of Evolutionary Anthropology, Duke University, Durham, NC, USA
  • 4 Department of Psychology and Neuroscience, Duke University, Durham, NC, USA

What happens to others profoundly influences our own behavior. Such other-regarding outcomes can drive observational learning, as well as motivate cooperation, charity, empathy, and even spite. Vicarious reinforcement may serve as one of the critical mechanisms mediating the influence of other-regarding outcomes on behavior and decision-making in groups. Here we show that rhesus macaques spontaneously derive vicarious reinforcement from observing rewards given to another monkey, and that this reinforcement can motivate them to subsequently deliver or withhold rewards from the other animal. We exploited Pavlovian and instrumental conditioning to associate rewards to self (M1) and/or rewards to another monkey (M2) with visual cues. M1s made more errors in the instrumental trials when cues predicted reward to M2 compared to when cues predicted reward to M1, but made even more errors when cues predicted reward to no one. In subsequent preference tests between pairs of conditioned cues, M1s preferred cues paired with reward to M2 over cues paired with reward to no one. By contrast, M1s preferred cues paired with reward to self over cues paired with reward to both monkeys simultaneously. Rates of attention to M2 strongly predicted the strength and valence of vicarious reinforcement. These patterns of behavior, which were absent in non-social control trials, are consistent with vicarious reinforcement based upon sensitivity to observed, or counterfactual, outcomes with respect to another individual. Vicarious reward may play a critical role in shaping cooperation and competition, as well as motivating observational learning and group coordination in rhesus macaques, much as it does in humans. We propose that vicarious reinforcement signals mediate these behaviors via homologous neural circuits involved in reinforcement learning and decision-making.

Keywords: vicarious reinforcement, social reward, gaze, social interaction, rhesus macaques

Citation: Chang SWC, Winecoff AA and Platt ML (2011) Vicarious reinforcement in rhesus macaques (Macaca mulatta). Front. Neurosci. 5:27. doi: 10.3389/fnins.2011.00027

Received: 05 January 2011; Accepted: 20 February 2011;
Published online: 03 March 2011.

Edited by:

Daeyeol Lee, Yale University School of Medicine, USA

Reviewed by:

Mehrdad Jazayeri, University of Washington, USA
James Rilling, Emory University, USA

Copyright: © 2011 Chang, Winecoff and Platt. This is an open-access article subject to an exclusive license agreement between the authors and Frontiers Media SA, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.

*Correspondence: Steve W. C. Chang, Center for Cognitive Neuroscience, B203 Levine Science Research Center, Duke University, Box 90999, Durham, NC 27708, USA.e-mail: steve.chang@duke.edu

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