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Anatomo-functional basis of emotional and motor resonance elicited by facial expressions
Brain ( IF 14.5 ) Pub Date : 2024-02-16 , DOI: 10.1093/brain/awae050
Maria Del Vecchio 1 , Pietro Avanzini 1 , Marzio Gerbella 2 , Sara Costa 2 , Flavia Maria Zauli 3 , Piergiorgio d’Orio 3 , Elena Focacci 2 , Ivana Sartori 3 , Fausto Caruana 1
Affiliation  

Simulation theories predict that the observation of other’s expressions modulates neural activity in the same centers controlling their production. This hypothesis has been developed by two models, postulating that the visual input is directly projected either to the motor system for action recognition (motor resonance) or to emotional/interoceptive regions for emotional contagion and social synchronization (emotional resonance). Here we investigated the role of frontal/insular regions in the processing of observed emotional expressions by combining intracranial recording, electrical stimulation and effective connectivity. First, we intracranially recorded from prefrontal, premotor or anterior insular regions of 44 patients during the passive observation of emotional expressions, finding widespread modulations in prefrontal/insular regions (anterior cingulate cortex, anterior insula, orbitofrontal cortex and inferior frontal gyrus) and motor territories (rolandic operculum and inferior frontal junction). Subsequently, we electrically stimulated the activated sites, finding that (a) in the anterior cingulate cortex and anterior insula, the stimulation elicited emotional/interoceptive responses, as predicted by the ‘emotional resonance model’, (b) in the rolandic operculum it evoked face/mouth sensorimotor responses, in line with the ‘motor resonance’ model, and (c) all other regions were unresponsive or revealed functions unrelated to the processing of facial expressions. Finally, we traced the effective connectivity to sketch a network-level description of these regions, finding that the anterior cingulate cortex and the anterior insula are reciprocally interconnected while the rolandic operculum is part of the parieto-frontal circuits and poorly connected with the formers. These results support the hypothesis that the pathways hypothesized by the ‘emotional resonance’ and the ‘motor resonance’ models work in parallel, differing in terms of spatio-temporal fingerprints, reactivity to electrical stimulation and connectivity patterns.

中文翻译:

面部表情引起的情绪和运动共振的解剖功能基础

模拟理论预测,对他人表情的观察会调节控制其表达的同一中心的神经活动。这一假设由两个模型提出,假设视觉输入直接投射到运动系统以进行动作识别(运动共振),或投射到情绪/内感受区域以进行情绪传染和社会同步(情绪共振)。在这里,我们通过结合颅内记录、电刺激和有效连接,研究了额叶/岛叶区域在处理观察到的情绪表达中的作用。首先,我们在被动观察情绪表达过程中对 44 名患者的前额叶、前运动或前岛叶区域进行了颅内记录,发现前额叶/岛叶区域(前扣带皮层、前岛叶、眶额皮层和额下回)和运动区存在广泛的调节(罗兰盖和额下交界处)。随后,我们对激活部位进行电刺激,发现(a)在前扣带皮层和前岛叶中,刺激引起了情绪/内感受反应,正如“情绪共振模型”所预测的那样,(b)在它引起的罗兰迪克盖中面部/嘴巴感觉运动反应,符合“运动共振”模型,以及(c)所有其他区域均无反应或显示与面部表情处理无关的功能。最后,我们追踪了有效的连接性,以勾画出这些区域的网络级描述,发现前扣带皮层和前岛叶是相互关联的,而罗兰迪克盖是顶叶回路的一部分,与前者的连接较差。这些结果支持这样的假设:“情绪共振”和“运动共振”模型假设的通路并行工作,在时空指纹、对电刺激的反应性和连接模式方面有所不同。
更新日期:2024-02-16
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