Lyu Jing, Li Jiayue, Ding Rui, Zhao Hui, Liu Chao, Qin Shaozheng
State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China.
IDG / Mc Govern Institute for Brain Research, Beijing Normal University, China.
Neurobiol Stress. 2024 Oct 11;34:100677. doi: 10.1016/j.ynstr.2024.100677. eCollection 2025 Jan.
Fear learning is pivotal for organismal survival, ensuring the ability to avoid potential threats through learning based on experiencing minimal fear information. In reality, fear learning requires to form a structured representation of fear experiences from multiple dimensions in order to support flexible use in ever-changing environment. Yet, the underlying neural mechanisms of constructing dimensional fear space remain elusive. Here we set up an innovative approach with two-dimensional fear learning, by utilizing the probability (uncertainty) and subjective pain intensity of threatening mild electric shock with five levels of each dimension. Behaviorally, individuals constructed a two-dimensional fear space after learning phase, as evidenced by significant changes in participant's fearful ratings for each cue associated with a five-by-five grid after (relative to before) learning phase. Analysis of neuroimaging data revealed that the medial temporal lobe, in conjunction with the amygdala, the insula, the anterior cingulate cortex (ACC), the hippocampus, and the dorsolateral prefrontal cortex (dlPFC), collectively contribute to the construction of a two-dimensional fear space consisting of uncertainty and intensity. Activation in the parahippocampal gyrus, insula, and dlPFC was associated with mental navigation within two-dimensional fear space, whereas the engagement of insula, ACC, amygdala, the hippocampus, the dlPFC was associated with a unified fearful scoring cross uncertainty and intensity dimensions after fear learning. Our findings suggest a neurocognitive model through which emotional salience network underlies the construction of a structured representation of fear experiences from multiple dimensions.
恐惧学习对于生物体的生存至关重要，它能确保生物体通过基于极少恐惧信息的学习来避免潜在威胁的能力。实际上，恐惧学习需要从多个维度形成恐惧体验的结构化表征，以便在不断变化的环境中灵活运用。然而，构建维度恐惧空间的潜在神经机制仍然难以捉摸。在这里，我们通过利用威胁性轻度电击的概率（不确定性）和主观疼痛强度（每个维度有五个级别），建立了一种二维恐惧学习的创新方法。在行为上，个体在学习阶段后构建了一个二维恐惧空间，这体现在学习阶段后（相对于学习阶段前）参与者对与一个五乘五网格相关的每个线索的恐惧评分有显著变化。神经影像数据分析表明，内侧颞叶与杏仁核、脑岛、前扣带回皮质（ACC）、海马体和背外侧前额叶皮质（dlPFC）共同促成了一个由不确定性和强度组成的二维恐惧空间的构建。海马旁回、脑岛和dlPFC的激活与二维恐惧空间内的心理导航有关，而脑岛、ACC、杏仁核、海马体、dlPFC的参与与恐惧学习后跨不确定性和强度维度的统一恐惧评分有关。我们的研究结果提出了一种神经认知模型，通过该模型，情绪显著性网络构成了从多个维度构建恐惧体验结构化表征的基础。
