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Selective Prefrontal-Amygdala Circuit Interactions Underlie Social and Nonsocial Valuation in Rhesus Macaques
Journal of Neuroscience ( IF 5.3 ) Pub Date : 2022-07-13 , DOI: 10.1523/jneurosci.0794-21.2022
Maia S Pujara 1 , Nicole K Ciesinski 1 , Joseph F Reyelts 1 , Sarah E V Rhodes 1 , Elisabeth A Murray 2
Affiliation  

Lesion studies in macaques suggest dissociable functions of the orbitofrontal cortex (OFC) and medial frontal cortex (MFC), with OFC being essential for goal-directed decision-making and MFC supporting social cognition. Bilateral amygdala damage results in impairments in both of these domains. There are extensive reciprocal connections between these prefrontal areas and the amygdala; however, it is not known whether the dissociable roles of OFC and MFC depend on functional interactions with the amygdala. To test this possibility, we compared the performance of male rhesus macaques (Macaca mulatta) with crossed surgical disconnection of the amygdala and either MFC (MFC x AMY, n = 4) or OFC (OFC x AMY, n = 4) to a group of unoperated controls (CON, n = 5). All monkeys were assessed for their performance on two tasks to measure the following: (1) food-retrieval latencies while viewing videos of social and nonsocial stimuli in a test of social interest and (2) object choices based on current food value using reinforcer devaluation in a test of goal-directed decision-making. Compared with the CON group, the MFC x AMY group, but not the OFC x AMY group, showed significantly reduced food-retrieval latencies while viewing videos of conspecifics, indicating reduced social valuation and/or interest. By contrast, on the devaluation task, group OFC x AMY, but not group MFC x AMY, displayed deficits on object choices following changes in food value. These data indicate that the MFC and OFC must functionally interact with the amygdala to support normative social and nonsocial valuation, respectively.

SIGNIFICANCE STATEMENT Ascribing value to conspecifics (social) versus objects (nonsocial) may be supported by distinct but overlapping brain networks. Here, we test whether two nonoverlapping regions of the prefrontal cortex, the medial frontal cortex and the orbitofrontal cortex, must causally interact with the amygdala to sustain social valuation and goal-directed decision-making, respectively. We found that these prefrontal-amygdala circuits are functionally dissociable, lending support for the idea that medial frontal and orbital frontal cortex make independent contributions to cognitive appraisals of the environment. These data provide a neural framework for distinct value assignment processes and may enhance our understanding of the cognitive deficits observed following brain injury or in the development of mental health disorders.



中文翻译:

选择性前额叶-杏仁核回路相互作用是恒河猴社会和非社会评价的基础

猕猴的病变研究表明,眶额叶皮层 (OFC) 和内侧额叶皮层 (MFC) 具有可分离的功能,其中 OFC 对于目标导向的决策至关重要,而 MFC 支持社会认知。双侧杏仁核损伤导致这两个领域的损伤。这些前额区和杏仁核之间存在广泛的相互联系;然而,OFC 和 MFC 的可分离作用是否取决于与杏仁核的功能相互作用尚不清楚。为了测试这种可能性,我们比较了雄性恒河猴 ( Macaca mulatta ) 与杏仁核交叉手术断开以及 MFC (MFC x AMY, n = 4) 或 OFC (OFC x AMY, n= 4) 到一组未操作的控件 (CON, n = 5)。评估所有猴子在两项任务中的表现以衡量以下内容:(1) 在社交兴趣测试中观看社交和非社交刺激视频时的食物检索延迟,以及 (2) 使用增强物贬值根据当前食物价值选择对象在目标导向的决策测试中。与 CON 组相比,MFC x AMY 组而非 OFC x AMY 组在观看同种视频时显示食物检索延迟显着降低,表明社会价值和/或兴趣降低。相比之下,在贬值任务中,组 OFC x AMY,而不是组 MFC xAMY,在食物价值发生变化后,在对象选择上表现出缺陷。这些数据表明 MFC 和 OFC 必须在功能上与杏仁核相互作用以分别支持规范的社会和非社会评估。

重要性声明不同但重叠的大脑网络可能支持赋予同种(社会)与对象(非社会)价值。在这里,我们测试前额叶皮层的两个非重叠区域,内侧额叶皮层和眶额叶皮层,是否必须与杏仁核因果相互作用以分别维持社会评价和目标导向的决策。我们发现这些前额叶-杏仁核回路在功能上是可分离的,支持内侧额叶和眶额叶皮层对环境的认知评估做出独立贡献的观点。这些数据为不同的价值分配过程提供了一个神经框架,并可能增强我们对脑损伤后或精神健康障碍发展过程中观察到的认知缺陷的理解。

更新日期:2022-07-14
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