大脑如何编码“吝啬”或“慷慨”行为呢？

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这种对个人和群体都很重要的“吝啬”和“慷慨”行为，大脑是如何编码的呢？

这是一直让神经科学家非常着迷的问题。

美国耶鲁大学神经科学系的Steve Chang团队在今年2月24日发表于《自然神经科学》杂志的一项新研究为这个问题，给出了很重要的答案[1]。结合活体单细胞电生理技术和行为学，他们在恒河猴(rhesus macaques)上的实验，发现前扣带回(Anterior Cingulate Gyrus, ACCg)和杏仁基底外侧核(Basolateral Amygdala, BLA)的同步协调关系对于编码利他偏好行为非常重要，也就是说ACCg-BLA的协调关系在“吝啬”和“慷慨”行为中扮演很重要的角色。

（图片来源文章的fig. 1[1]）

怎样解析？

同样由Steve Chang为主的研究者于2013年在《自然神经科学》发表的工作发现，当猴子选择将果汁给予其他猴子而不是选择扔掉，即表现利他行为时，ACCg神经元活动编码了这行为，而不是ACC其他亚区[2]。Steve Chang于2015年在《美国国家科学院院刊》发表的工作发现，BLA的神经元编码猴子选择将果汁给予自己或其他猴子的决策行为。因此，这次该研究团队选择了ACCg和BLA,来进一步解析该利他决策行为[3]。

发现什么？

研究人员发现大脑两个区域之间的神经元活动相互作用，在两种情景下显著不同。当猴子表现得慷慨时（Positive ORP），两个脑区之间的相互作用，特别是BLA 神经元发放对ACCg场电位的β波段高度同步；当它们表现得吝啬时（Negative ORP），这种同步率显著降低了（如下图所示）。同时，ACCg神经元发放对BLA场电位的γ波段，也有类似的结果。

（图片来源文章的fig. 3[1]）

ACCg与BLA两个脑区之间的信息流是如何的呢？研究者使用了部分定向相干(partial directed coherence, PDC)分析方法来回答这问题。他们发现，在猴子进行慷慨行为时（Positive ORP），15-35 Hz处，显著是BLA流向ACCg，而当猴子进行吝啬行为时（Negative ORP）则有相反的结果，主要是ACCg流向BLA。

（图片来源文章的fig. 4[1]）

最后，研究者们想探究这些电生理的数据是否能直接编码猴子做出“慷慨”或“吝啬”的行为呢？他们使用了线性判别分析的方法，使用其中75%的峰电位-场电相干数据来作为模型的输入，来验证其能否在剩余的25%数据中来预测猴子的行为。如下图所示，使用BLA神经元发放对ACCgβ波场电的相干数据进行建模，发现在猴子做出“慷慨”行为(Positive ORP)前300ms开始，β波编码准确度显著高于对照组（图中上部分红线代表有显著性差异）。而在猴子做“吝啬”行为(Negative ORP)时也是显著更高。这说明，只要查看BLA对ACCgβ波场电的相干可以来预测猴子做出“吝啬”决定，还是“慷慨”决定。对于ACCg神经元发放对BLA场电的相干数据也有类似的结果，这说明ACCg与BLA的相干同步性可编码做出“吝啬”或“慷慨”决定。

（图片来源文章的fig. 5[1]）

有何意义？

这项研究，首次在灵长类动物上解析了BLA与ACCg脑区的同步相干性可编码 “吝啬”和“慷慨”的行为。提示我们，类似夏洛克的吝啬鬼，他们的BLA与ACCg脑区的同步相干性可能比较小。这也给了我们一些启发，如果能干预提升BLA与ACCg脑区的同步相干性，或许能促进产生慷慨的利他行为。

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参考文献：

1. Dal Monte O, Chu CCJ, Fagan NA, Chang SWC. Specialized medial prefrontal–amygdala coordination in other-regarding decision preference. Nat Neurosci. 2020:1–10.

Social behaviors recruit multiple cognitive operations that require interactions between cortical and subcortical brain regions. Interareal synchrony may facilitate such interactions between cortical and subcortical neural populations. However, it remains unknown how neurons from different nodes in the social brain network interact during social decision-making. Here we investigated oscillatory neuronal interactions between the basolateral amygdala and the rostral anterior cingulate gyrus of the medial prefrontal cortex while monkeys expressed context-dependent positive or negative other-regarding preference (ORP), whereby decisions affected the reward received by another monkey. Synchronization between the two nodes was enhanced for a positive ORP but suppressed for a negative ORP. These interactions occurred in beta and gamma frequency bands depending on the area contributing the spikes, exhibited a specific directionality of information flow associated with a positive ORP and could be used to decode social decisions. These findings suggest that specialized coordination in the medial prefrontal–amygdala network underlies social-decision preferences. 

2. Chang, S. W. C., Gariépy, J.-F. & Platt, M. L. Neuronal reference frames for social decisions in primate frontal cortex. Nat. Neurosci. 16, 243–250 (2013).

Social decisions are crucial for the success of individuals and the groups that they comprise. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders such as autism and sociopathy. We examined the manner in which neurons in three frontal cortical areas encoded the outcomes of social decisions as monkeys performed a reward-allocation task. Neurons in the orbitofrontal cortex (OFC) predominantly encoded rewards that were delivered to oneself. Neurons in the anterior cingulate gyrus (ACCg) encoded reward allocations to the other monkey, to oneself or to both. Neurons in the anterior cingulate sulcus (ACCs) signaled reward allocations to the other monkey or to no one. In this network of received (OFC) and foregone (ACCs) reward signaling, ACCg emerged as an important nexus for the computation of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas.

3. Chang, S. W. C. et al. Neural mechanisms of social decision-making in the primate amygdala. Proc. Natl Acad. Sci. USA 112, 16012–16017 (2015).

Social decisions require evaluation of costs and benefits to oneself and others. Long associated with emotion and vigilance, the amygdala has recently been implicated in both decision-making and social behavior. The amygdala signals reward and punishment, as well as facial expressions and the gaze of others. Amygdala damage impairs social interactions, and the social neuropeptide oxytocin (OT) influences human social decisions, in part, by altering amygdala function. Here we show in monkeys playing a modified dictator game, in which one individual can donate or withhold rewards from another, that basolateral amygdala (BLA) neurons signaled social preferences both across trials and across days. BLA neurons mirrored the value of rewards delivered to self and others when monkeys were free to choose but not when the computer made choices for them. We also found that focal infusion of OT unilaterally into BLA weakly but significantly increased both the frequency of prosocial decisions and attention to recipients for context-specific prosocial decisions, endorsing the hypothesis that OT regulates social behavior, in part, via amygdala neuromodulation. Our findings demonstrate both neurophysiological and neuroendocrinological connections between primate amygdala and social decisions.

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