Autonomic arousal tracks outcome salience not valence in monkeys making social decisions

Abstract

The evolutionary and neural underpinnings of human prosociality are still largely unknown. A growing body of evidence suggests that some species find the sight of another individual receiving a reward reinforcing, often called vicarious reinforcement. One hypothesis is that vicarious reward is reinforcing because it is arousing like a primary reward. We evaluated this hypothesis by measuring the autonomic pupil response of eight monkeys across two laboratories in two different versions of a vicarious reinforcement paradigm. Monkeys were cued as to whether an upcoming reward would be delivered to them, another monkey, or nobody and could accept or decline the offer. As expected, all monkeys in both laboratories showed a marked preference for juice to the self, together with a reliable prosocial preference for juice to a social partner compared to juice to nobody. However, contrary to the autonomic arousal hypothesis, we found that pupils were widest in anticipation of juice to the self, moderately-sized in anticipation of juice to nobody, and narrowest in anticipation of juice to a social partner. This effect was seen across both laboratories and regardless of specific task parameters. The seemingly paradoxical pupil effect can be explained by a model in which pupil size tracks outcome salience, prosocial tendencies track outcome valence, and the relation between salience and valence is U-shaped.

The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys

“…In intact (i.e., unoperated) monkeys, preference for Other is dependent on the presence of the partner monkey; baseline prosocial preferences are absent in the Nonsocial condition [30]. In the Nonsocial sessions of the retention test of this study, only one monkey (C3) showed a numerical preference for giving juice to the collection jar, but this was not significant (S2 Fig; t 19 = 0.87, p = 0.398).…”

“…Preoperatively, all 6 actor monkeys showed a reliable prosocial preference for Other trials over Neither trials [30], and the magnitude of this preference did not differ between the groups designated to serve as controls or receive surgery (Fig 2A; t 3 = 0.37, p = 0.735).…”

“…However, pupillary responses are complex [39], pupil size is affected by factors other than anticipated value [40,41], and even reliable value-related pupil changes are more nuanced than a simple model in which high anticipated value always produces large pupils [42]. Indeed, our own measures of pupil response during vicarious reinforcement demonstrate some of this nuance [30]. Regardless, our results suggest that the ACC is not a part of the neural circuitry responsible for producing the socially modulated pupil response seen during vicarious reinforcement.…”

“…Preoperatively, monkeys' autonomic arousal was dissociated from their preferences, in that pupil size was larger for the less preferred Neither outcomes than for the more preferred Other outcomes [30]. Importantly, this difference in autonomic arousal between the Other versus Neither reward conditions was specific to the Social condition, as pupil size associated with delivering juice rewards to the juice collection jar did not differ from the Neither condition PLOS BIOLOGY [30]. Postoperatively, pupil size remained dissociated from social preference.…”

“…To focus on the previously reported prosocial preferences, our critical comparison is the proportion of trials monkeys completed in the Other and Neither conditions. In a previous study of the autonomic correlates of vicarious reinforcement, we showed that monkeys had a reliable prosocial preference for accepting more Other offers than Neither offers and that pupils were paradoxically larger in anticipation of the less preferred Neither trials than the more preferred Other trials [30]. Here, we evaluated the degree to which this prosocial preference and autonomic arousal changed as a result of selective ACC damage ( Fig 1E).…”