A key feature of most social relationships is that we like seeing good things happen to others. Research has implicated the anterior cingulate cortex (ACC) in attaching value to social outcomes. For example, single neurons in macaque ACC selectively code reward delivery to the self, a partner, both monkeys, or neither monkey. Here, we assessed whether the ACC’s contribution to social cognition is causal by testing rhesus monkeys (Macaca mulatta) on a vicarious reinforcement task before and after they sustained ACC lesions. Prior to surgery, actors learned that 3 different visual cues mapped onto 3 distinct reward outcomes: to self (“Self”), to the other monkey (“Other”), or to neither monkey (“Neither”). On each trial, actors saw a cue that predicted one of the 3 juice offers and could accept the offer by making a saccade to a peripheral target or reject the offer by breaking fixation. Preoperatively, all 6 actors displayed prosocial preferences, indicated by their greater tendency to give reward to Other relative to Neither. Half then received selective, bilateral, excitotoxic lesions of the ACC, and the other half served as unoperated controls. After surgery, all monkeys retained the social preferences they had demonstrated with the preoperatively learned cues, but this preference was reduced in the monkeys with ACC lesions. Critically, none of the monkeys in the ACC lesion group acquired social preferences with a new set of cues introduced after surgery. These data indicate that the primate ACC is necessary for acquisition of prosocial preferences from vicarious reinforcement.

大多数社会关系的一个关键特征是我们喜欢看到好事发生在别人身上。研究表明前扣带皮层 (ACC) 与社会结果的价值相关。例如，猕猴 ACC 中的单个神经元选择性地编码将奖励传递给自己、伴侣、两只猴子或都不给猴子。在这里，我们通过测试恒河猴（Macaca mulatta）在 ACC 损伤前后的替代强化任务来评估 ACC 对社会认知的贡献是否具有因果关系。在手术之前，演员了解到 3 种不同的视觉线索映射到 3 种不同的奖励结果：对自己（“自我”）、对另一只猴子（“其他”）或对两只猴子（“两者都不是”）。在每次试验中，演员都会看到一个提示，该提示可以预测 3 个果汁提议中的一个，并且可以通过向外围目标进行扫视来接受该提议，或者通过打破固定来拒绝该提议。术前，所有 6 名参与者都表现出亲社会偏好，这表明他们更倾向于给予其他人相对于“两者都不是”的奖励。然后一半接受选择性、双侧、ACC 兴奋性毒性损伤，另一半作为未手术对照。手术后，所有猴子都保留了它们通过术前习得的线索所表现出的社交偏好，但这种偏好在有 ACC 损伤的猴子中有所减弱。关键的是，ACC 损伤组中的猴子都没有通过手术后引入的一组新线索获得社交偏好。这些数据表明，灵长类 ACC 对于通过替代强化获得亲社会偏好是必要的。