Emotional salience network involved in constructing two-dimensional fear space in humans

Abstract

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.