Resolving temporal threat uncertainty by observational learning involves the amygdala, hippocampus and anterior insula

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Abstract

By relying on the observation of others’ experiences, humans learn about threat while avoiding harmful experiences. Yet, previous neuroscience research has focused on observational threats that are predictable. While the neurobiological distinction between temporally predictable (cued) and unpredictable (contextual) threats has been well-characterized in firsthand learning. In this study, we developed a novel observational paradigm in which participants learned from predictable (P) and unpredictable (U) observational threats, as well as a no-threat (N) condition and encountered the same conditions during an expression phase based on the NPU paradigm to investigate how the brain encodes predictable and unpredictable threat cues observed in others. Participants in Experiment 1 (n=20, male and female) and Experiment 2 (n=23, male and female) successfully learned threat contingencies, showing heightened threat expectations for predictable cues and unpredictable contexts. This converged with neural (fMRI, Experiment 2) responses in the anterior insula during the expression phase. Reflecting the dynamic process of learning, the amygdala responded to predictable threat cues with a linear decrease across trials. Interestingly, we found that responses to others’ pain was enhanced within the amygdala, insula and hippocampus, when participant could learn to predict threats, as compared to unpredictable conditions. Our findings suggest that humans learn to resolve temporal uncertainty, relying solely on observation, which thereby lays a foundation to the concept of fear and anxiety in social groups.

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