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大脑如何编码“吝啬”或“慷慨”行为呢?

日常科普的 脑科学与脑技术 2022-04-17

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吝啬指自私小气,“抠门”这个词很形象地描述了吝啬,小气到连个门把手都舍不得装,开门的时候不得不用手去抠门缝,所以大家把吝啬的人说成是抠门。慷慨则相反,不吝啬,很无私。说到吝啬,西方文学上有四大吝啬鬼,大家最熟知的可能就是《威尼斯商人》(被选到语文课本里)中的夏洛克,他虽然腰缠万贯,却不享用,一心想着放高利贷;他无情地虐待克扣仆人,甚至连饭也不让人吃饱;他十分痛恨威尼斯商人安东尼奥,因为他慷慨大度,乐于助人,憎恶高利贷者。我们日常中也有很多“抠门”和“慷慨”的行为,有的人很不喜欢分享自己的东西,而有的人却很喜欢分享自己的东西,例如面对乞丐,有人慷慨解囊,有人冷漠走过?


“吝啬”和“慷慨”的行为,可以归属为社会决策行为(Social Decision-Making),其中“吝啬”是负向的利他偏好(negative other-regarding preference, negative ORP);e慷慨”是正向的利他偏好(positive other-regarding preference, positive ORP)。正向利他行为可以很好促进群体发展,而自私吝啬的行为则对群体发展不利。举个栗子:《威尼斯商人》中夏洛克极其吝啬,宁可要安东尼奥身上一块对他没用的人肉,也不想要安东尼奥的还款。这种极端吝啬行为对夏洛克自己没有益处,对安东尼奥更是没益处,对他们的关系更是,真是害人不利己。倘若夏洛克能慷慨一些,能去接受安东尼奥的还款,他自己也能真正得到更多收益,而安东尼奥也不用担心收到人身伤害,而且他们的关系也可以有修复,这就互利共赢了。


(图片来源https://readmoo.com/book/210020343000101 )


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?


首先要解析大脑如何编码一个行为,必须要确保读取大脑的活动的有效性。活体单细胞电生理记录是很有效的工具,通过在大脑具体脑区中埋置电极,可以记录具体脑区的局部场电位(Local field potential, LFP) 和单个神经元的发放(Spike)。由于埋置电极的损伤和侵入性,在健康的人类上无法实现,而有关啮齿类动物“吝啬”和“慷慨”的行为学范式设计存在困难、无法令人信服等原因,因此可以在灵长类动物上实现“吝啬”和“慷慨”的行为学范式研究,研究者使用了恒河猴作为实验对象,利用猴子(作为Self)决定是否向伙伴(作为Other)分享果汁,而巧妙地设计了“吝啬”和“慷慨”的两种情景,同时采集大脑的前扣带回皮(ACCg)和基底外侧杏仁核(BLA)两个脑区的神经元活动,再进一步计算分析。

为何要选取ACCg和BLA脑区呢?

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 Chang2015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ACCgBLA,来进一步解析该利他决策行为[3]


研究者设计了Self/Bothother/Bottle两种场景:在Self/Both场景中,猴子可以选择独自喝果汁(Self)或和同伴一起分享同样量的果汁(Both)。在other/Bottle场景中,猴子要决定把果汁分享给同伴(other)或是扔到垃圾桶中(Bottle)。如上图所示,可以发现在Self/Both场景中,猴子更偏向于独自喝果汁,这种行为属于是负向的利他偏好(negative other-regarding preference, negative ORP),即“吝啬”行为。在other/Bottle场景中,当猴子看着果汁被扔垃圾桶,他们更愿意把果汁分享给同伴,这种行为属于是正向的利他偏好(positive other-regarding preference, positive ORP),即“慷慨”行为。为了解析以上行为下的神经元活动的机理,他们主要分析了峰电位-场电相干(Spike-field coherence, SFC)和信息流(information flow),同时使用线性判别分析(Linear Discriminant Analysis)来验证SFC能否编码猴子做出“吝啬”和“慷慨”的决策。


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])


ACCgBLA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)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BLAACCgβ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ACCgBLA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BLAACCg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BLAACCg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BLAACCg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.


感谢雷灼贵的投稿

感谢刘雪梅博士的审核


脑科学与脑技术


中科院深圳先进技术研究院

脑认知与脑疾病研究所

深港脑科学创新研究院


严谨治学  创新驱动

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