Abstract
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.
Highlights
Reinforcement learning provides a powerful mechanism for associating stimuli and actions with the direct experience of reward and punishment (Rescorla and Wagner, 1972; Schultz et al, 1997; Sutton and Barto, 1998)
Monkeys exhibit vicarious reinforcement Two adult male rhesus monkeys served as actors (M1) and five adult male rhesus monkeys served as recipients (M2; see Materials and Methods)
On Pavlovian trials (Figure 1B, top), M1 and M2 both saw the same cue at the center of the display, and juice rewards were delivered to M1 (RSELF), M2 (ROTHER), both M1 and M2 (RBOTH), or neither (RNONE) depending on the color or shape of the cue (Figure 1C; Table 1)
Summary
Reinforcement learning provides a powerful mechanism for associating stimuli and actions with the direct experience of reward and punishment (Rescorla and Wagner, 1972; Schultz et al, 1997; Sutton and Barto, 1998). Fictive learning can be described formally in terms analogous to reinforcement learning (Lohrenz et al, 2007), and may depend on overlapping neural circuitry (Lohrenz et al, 2007; Hayden et al, 2009; Mobbs et al, 2009). Observing what happens to others powerfully shapes human learning and behavior (Berger, 1962; Bandura and McDonald, 1963; Bandura et al, 1963). Such other-regarding outcomes can drive observational learning (Mobbs et al, 2009; Jeon et al, 2010), and motivate other-regarding behaviors such as cooperation and charity, as well as spite and schadenfreude (Takahashi et al, 2009). The “warm glow” hypothesis (Andreoni, 1990) suggests that vicarious reward and punishment motivates individuals to prefer either
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