Systems Neuroscience of Primate Social Cognition

人类和其他灵长类动物的大脑对社会信息进行了调整。从出生的那一刻起，我们的社交伙伴就会引起我们的兴趣。观察他人不仅能帮助我们优化自己的决定(“社交学习”)，还能帮助我们理解伴侣的想法，预测他们的意图和行为(“心理化”)。在自闭症、社交焦虑症、精神分裂症和相关的人类疾病中，由于特定大脑回路的功能障碍，这些社会认知能力严重受损。然而，我们对这些大脑回路中的神经元如何处理信息以实现社会认知和社会互动知之甚少。这是一个重要的问题，因为神经元是大脑中交换信息的基本计算元素。要了解类似人类的社会认知及其障碍，我们需要了解神经元和分布式大脑系统在社会互动过程中如何处理信息。我们通过记录猴子在解决奖励引导和基于规则的决策问题时大脑特定部分的单个神经元的活动来解决这个问题。当动物在社交、互动的环境中执行这些决策任务时，记录神经元的活动使我们能够解决特定的问题：当猴子观察并学习彼此的选择时，神经元如何处理社会伴侣的选择选项的价值？具体地说，神经元是否会从伴侣独特的主观角度来处理这种奖赏价值，即使这个角度与自己的不同？这一过程被称为精神化，在自闭症中严重受损。此外，当猴子在认知问题解决任务中互动学习抽象规则时，神经元是否会根据被观察伙伴的选择更新对当前有效规则的预期？他们是否会追踪伴侣关于哪条规则当前有效的信念，即使这一信念与自己的信念不同？在研究了这些任务中的神经元活动后，我们还可逆地干扰了任务执行过程中特定的大脑区域，这将帮助我们了解哪些大脑区域对社会认知做出了重要贡献。最后，基于获得的数据，我们将建立我们研究的大脑回路的计算机模型，以更好地理解在这些大脑区域进行的信息处理机制和计算。我们专注于杏仁核和部分前额叶皮质等大脑区域，我们已经知道这些区域在人类社会认知障碍中扮演着重要角色。我们在这项研究中使用猴子是因为它们具有接近人类的复杂社会能力，而且它们适合记录单个神经元的活动。尽管人脑成像可以帮助识别大脑的哪些区域参与社会认知，但成像信号太慢，空间上也不精确，无法揭示单个神经元中动态的、毫秒级的精确信息流。同样，尽管对啮齿动物的研究可以揭示基本社会行为的神经元机制，如攻击性和交配，但他们无法研究高级的、人类典型的社会认知，如社会规则学习、视角选择和精神化。

The brains of humans and other primates are tuned for social information. From the moment of birth, our social partners capture our interest. Observing others not only helps us optimise our own decisions ('social learning'), but also helps us understand our partners' minds and predict their intentions and behaviour ('mentalizing'). These social-cognitive abilities are profoundly impaired in autism, social anxiety, schizophrenia and related human conditions, due to dysfunction of specific brain circuits. Yet, we know very little about how neurons in these brain circuits process information to enable social cognition and social interactions. This is an important question because neurons are the basic computing elements of the brain that exchange information.To understand human-like social cognition and its disorders, we need to know how neurons and distributed brain systems process information during social interactions. We address this issue by recording the activity of individual neurons in specific parts of the brain while monkeys socially interact with each other to solve reward-guided and rule-based decision problems.Recording neuronal activity while the animals perform these decision tasks in a social, interactive context allows us to address specific questions: When monkeys observe and learn from each other's choices, how do neurons process the value of the social partner's choice options? Specifically, do neurons process such reward values from the partner's unique subjective perspective, even when this perspective differs from one's own? This process, known as mentalizing, is profoundly impaired in autism. Further, when monkeys interact to learn about abstract rules in a cognitive problem-solving task, do neurons update expectations about which rule is currently valid based on the observed partner's choices? And do they track the partner's belief about which rule is currently valid, even when this belief is different to one's own belief?After studying the neuronal activity in these tasks, we also reversibly interfere with specific brain areas during task performance, which will help us understand which brain areas make essential contributions to social cognition. Finally, based on the obtained data, we will build computer models of the brain circuits we study, to better understand the information-processing mechanisms and computations performed in these brain areas. We focus on brain areas such as the amygdala and parts of prefrontal cortex, which we already know play a role in human social-cognition disorders.We use monkeys in this research because they have sophisticated social abilities close to those of humans, and because they are suitable for recording the activity of individual neurons. Although human brain imaging can help identify which areas of the brain participate in social cognition, the imaging signal is too slow and spatially imprecise to reveal the dynamic, millisecond-precise information flow in single neurons. Likewise, although studies in rodents can uncover neuronal mechanisms for basic social behaviours such as aggression and mating, they cannot investigate advanced, human-typical social cognition such as social rule-learning, perspective-taking and mentalizing.